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Essential Ornithology
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Essential Ornithology
Second Edition
Graham Scott
Director, Teaching Excellence Academy, University of Hull, UK
1
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1
Great Clarendon Street, Oxford, OX2 6DP,
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Second Edition published in 2020
Impression: 1
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DOI: 10.1093/oso/9780198804741.001.0001
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For Lisa and Adam who have been very, very patient (again),
for my parents, Mary and Bill who indulged my passion for birds,
and for Will who keeps me birding!
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Preface
As was the case with the first edition of Essential
Ornithology this book is intended to be an introduction to what I consider to be the essentials of ornithology; those areas of the broader biology of birds
that are, in my view, the minimum that a student of
ornithology should know. In writing the second
edition I have attempted to take on board feedback
that I have had from students (my own included)
and from teachers who I am pleased to say have
found Essential Ornithology to be a useful resource.
I remain aware that in places I could have included
more depth, and that in places I could have provided
a broader treatment, but my aim was once again to
produce a relatively short useful text and so I was
unable to follow through every avenue of thought—
no matter how much I should have liked to!
Instead, by covering a breadth of material and by
restricting myself to case studies that should be
accessible to all, I hope that I have provided the
reader with a ‘way in’ to academic ornithology.
Essential Ornithology. Second Edition. Graham Scott, Oxford University Press (2020). © Graham Scott (2020).
DOI: 10.1093/oso/9780198804741.001.0001
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Acknowledgements
A book such as this one may have a single
author—but it would be impossible to write without access to all of the published works produced
by active researchers/writers in ornithology; I am
indebted to them all. Similarly, I owe a debt of
thanks to friends and colleagues who have provided their views on sections of the text; provided
most of the pictures that are included in it, and
assisted in the publication progress. At the risk of
missing any one of them, they are: Lisa Scott, Will
Scott, Bill Scott, Phil Wheeler, Margaret Boyd,
James Spencer, Robin Arundale, Peter Dunn, Ian
Robinson, Ian Grier, Les Hatton, Shirley Millar,
Andy Gosler, Stanislav Pribil, Sjirk Geets, Kyle
Elliott, José Tella, Simone Tenório, and the very
patient Ian Sherman.
Essential Ornithology. Second Edition. Graham Scott, Oxford University Press (2020). © Graham Scott (2020).
DOI: 10.1093/oso/9780198804741.001.0001
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Contents
1
2
Evolution of birds
1.1 Birds are dinosaurs
1.2 Archaeopteryx
1.3 The evolution of modern birds
1.4 The phylogeny of birds
1.4.1 Morphological phylogeny
1.4.2 Character conservation and convergence
1.4.3 Biomolecular phylogeny
1.5 Adaptive radiation and speciation
1.5.1 Darwin’s finches
1.5.2 Genes and evolution
1.5.3 Hybrids
Summary
Appendix 1 Familiar names of the members of the Orders
and Families of modern birds
1
1
3
6
7
7
7
8
10
10
13
13
17
17
Feathers and flight
2.1 Feathers
2.1.1 Feather types
2.1.2 Contour feathers
2.1.3 Down feathers and semiplumes
2.2 Feather tracts
2.3 Feather colour
2.4 Feather damage
2.5 Feather maintenance
2.6 Moult
2.6.1 Moult strategies
2.7 Flight
2.7.1 Gliding and soaring
2.7.2 Flapping flight
2.7.3 Respiration and flight energetics
2.7.4 Flying high
2.7.5 Flight speeds
2.8 The evolution of flight and flightlessness
Summary
21
21
21
22
22
24
26
26
28
28
30
33
34
36
38
39
41
45
47
xi
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xii
CONTENTS
3
Movement: migration and navigation
3.1 The ecology of migration
3.2 Genes and migration
3.3 Physiology and migration
3.3.1 Seasonality and coordination of migration
3.3.2 Hormones and the control of migration
3.3.3 Fuelling migration
3.3.4 Long haul flights
3.4 The weather and migration
3.5 Navigation
3.5.1 Navigational cues
Summary
48
51
52
57
57
58
59
62
63
65
68
72
4
Eggs, nests, and chicks
4.1 Sex and the gonads of birds
4.2 The egg
4.3 Clutch size
4.4 Egg shell colouration and patterning
4.4.1 Camouflage
4.4.2 Egg mimicry
4.4.3 Egg recognition
4.4.4 Signals of quality
4.4.5 Pigments and shell quality
4.5 Nests
4.6 Incubation
4.7 Hatching
4.8 Chicks
Summary
73
73
75
77
81
81
82
82
84
84
85
87
91
91
93
5
Reproduction
5.1 Males and females are different
5.2 Mating systems
5.3 Courtship and mate choice
5.3.1 Resource provision
5.3.2 Ornaments and displays
5.3.3 Sharing a mate
5.4 Song
5.4.1 Song learning
5.4.2 Functions of song
5.4.3 Synchronized singing
5.5 Raising a family
5.5.1 Begging
5.5.2 Imprinting and independence
Summary
94
94
97
99
99
101
101
105
106
107
110
113
113
118
119
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CONTENTS
xiii
6
Foraging and avoiding predators
6.1 Finding food and capturing prey
6.1.1 Sharing information
6.1.2 Foraging flocks
6.1.3 Do herbivores cooperate?
6.2 Optimal foraging
6.2.1 Feeding territories
6.3 Risk and foraging
6.4 Predator avoidance
6.4.1 Camouflage
6.4.2 Predator distraction displays
6.4.3 Tonic immobility
6.4.4 Alarm calls
6.4.5 Mobbing
6.4.6 Flocks and colonies
Summary
120
120
122
123
125
125
126
130
131
131
132
133
134
136
136
139
7
Populations, communities, and conservation
7.1 Populations
7.1.1 Life history strategies influence population growth
7.1.2 Population change
7.2 Communities
7.2.1 Communities are dynamic
7.2.2 Niche divergence
7.2.3 Niche shifts, ecological release, and competition
7.3 Extinction and conservation
7.3.1 Conservation can be a success
7.3.2 The task that faces us as ornithologists
Summary
140
140
140
142
144
145
147
148
150
151
153
154
Index
155
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C H A PT ER 1
Evolution of birds
‘Creation is never over. It had a beginning but it has no ending.’
Immanuel Kant, A General Natural
History of the Heavens (1755)
I often ask my students, ‘what is a bird?’, it’s a question that I was asked when I was a student and then
as now the most common answer is ‘a flying vertebrate’. Well of course this is only partly right. Birds,
like fish, amphibians, reptiles, and mammals do
have vertebrae (and the other defining characteristics of that group) and are therefore vertebrates—
but not all birds fly, nor are all flying vertebrates
birds (what about bats?). In practice it can be surprisingly difficult to define a bird, although we all
know what one is. A feathered vertebrate may do
the job because the only extant vertebrates to have
feathers are the birds. Feathers however can no
longer be claimed to belong uniquely to the birds
following the discovery of fossilized specimens of a
number of feathered dinosaurs such as Ornithomimus
and Sinosauropteryx. Many of the other defining features of birds are in fact shared with one or more
vertebrate groups and so only set birds apart when
considered in concert. Like most reptiles they lay
eggs and their young develop outside of the body
of the parent. Like crocodilians and mammals
they have a four-chambered heart. Like mammals
they are warm blooded and have a high metabolic
rate, which in turn requires that they feed regularly.
Uniquely among vertebrates they lack teeth and
have a beak. They have bones that are pneumatized
(they have air-filled cavities) and are therefore light
compared with the solid bones of other vertebrates,
their clavicles are fused to form a furcula or wishbone, and they have a deeply keeled sternum for
the attachment of large flight muscles. These and
many other features particular to birds are related
to flight and will be discussed in more detail in
chapter 2. Here in chapter 1, I want to consider not
so much what birds are, but rather to explore their
evolutionary history.
And the answer to my opening question? Well I
vividly recall my own incredulity as a student when
my smiling tutor declared ‘Birds are the last of the
dinosaurs!’
Chapter overview
1.1
1.2
1.3
1.4
1.5
Birds are dinosaurs
Archaeopteryx
The evolution of modern birds
The phylogeny of birds
Adaptive radiation and speciation
1.1 Birds are dinosaurs
Although the first suggestions that birds might be
related to reptiles were made when Archaeopteryx
was first described in the 1860s, it wasn’t until late in
the twentieth century that the idea that birds evolved
from dinosaurs began to be generally accepted.
There were initially two main theories to explain the
evolutionary origins of birds. Both agreed that birds
arose from reptiles, as of course did mammals. But
whereas the mammals were thought to have their
origins in the synapsid reptiles, the birds were
thought to have evolved from the diapsid reptiles.
The numerous species of lizard and snake living
today are diapsids, but to uncover the evolutionary
Essential Ornithology. Second Edition. Graham Scott, Oxford University Press (2020). © Graham Scott (2020).
DOI: 10.1093/oso/9780198804741.003.0001
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ESSENTIAL ORNITHOLOGY
Neornithes
Ichthyomis
Hesperornithiformes
Vorona
Enantiornithes
Sapeornis
Confuciusornithiformes
Jeholomis
Reptiles are classified into one of two types depending
upon the morphology of the skull, or more precisely
upon the arrangement of fenestrae (windows) in the
skull. Synapsid reptiles have a single fenestration behind
the eye socket, whereas the skulls of diapsids have two,
one above the other. As a result diapsids have a lighter
and generally more ‘open’ skull. They also tend to have
a lighter skeleton and more slender body—they are
more bird-like.
Troodontidae
Dromaeosauridae
Oviraptorosauria
Tyrannosaurus
Sauropods
omithischians
crocodiles
Lizards
Mammals
Concept
Synapsids vs diapsids
145 130 120 100
Ornithorthoraces
Pygostylia
Avialae/Aves (Birds)
174 163
237
250
Triassic
Ornithurae
Ornithuromorpha
Paraves
Wings
Maniraptora
201
Jurassic
Cretaceous
66
Cz
Amphibians
roots of birds we need to look back to the now extinct
archosaurs, perhaps the most successful of the
diapsid groups historically—giving rise as it did to
the thecodonts, the pterosaurs, and most notably to
the dinosaurs. From the fossil record it has become
increasingly apparent that birds evolved from dinosaurs over a period of some 100 million years, gradually developing the features of modern birds
(Figure 1.1). It is also apparent that their closest
dinosaur relatives are the small, fast, feathered, and
perhaps relatively intelligent (by virtue of large
brain size) dromaesaurs such as Velociraptor.
Archaeopteryx
2
Theropoda/Coelurosauria
Keeled
sternum
Pygostyle
(fused tail)
Vaned feathers
Furcula (wishbone)
Saurischia
Dinosauria
Archosauria
Diapsida
Amniota
Tetrapoda
Simple filamentous feathers
Hinge-like ankle
Figure 1.1 A summary phylogeny of birds. This genealogical tree shows the relationship between the birds, their dinosaur ancestors, and the
wider vertebrate tree. The thick line between the Cretaceous and the Cenozoic (CZ) represents the asteroid impact-induced mass extinction event
and the arrows above that line show which lineages survived that event. From the figure it can be seen that the anatomical features of birds
evolved over a period of around 100 million years. Adapted from Brusatte, S.L., O’Connor, J.K., and Jarvis, E.D. (2015) The Origin and Diversification
of Birds. Current Biology 25(19), R888-R898. With permission from Elsevier.
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EVOLUTION OF BIRDS
Flight path: evolution of feathers and flight,
pages 26 and 45.
1.2 Archaeopteryx
In 1860, just one year after the publication of Charles
Darwin’s world-changing book On the Origin of
Species, a fossil was discovered in the Solnhofen
lithographic limestone of southern Germany that
caused a sensation. The fossil was that of a single
secondary flight feather and it was the first conclusive evidence of the existence of prehistoric birds.
Within weeks, in 1861, a second fossil was
3
announced from the same region—that of an almost
complete feathered skeleton (called the London specimen it resides in London at the Natural History
Museum, Figure 1.2 is the more complete Berlin specimen). A bird—but not just a bird, a bird with reptilian
or dinosaur features—exactly the putative ‘missing
link’ that Darwin had predicted in his book. This
fossil was destined to become one of the most familiar and at the same time most fiercely debated in
history. It is important to note that although I have
used the word ‘bird’ to describe Archaeopteryx, I have
done so in the sense that it is a member of the group
Aves, a group that is represented in the extant fauna
Figure 1.2 Archaeopteryx
Archaeoptery lithographica, the Berlin
specimen. © Markéta Machovà, from
Pixabay.
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4
ESSENTIAL ORNITHOLOGY
by the Neornithes, the members of which are the
modern birds.
From the handful of Archaeopteryx fossils that
have been discovered we now know that it was
feathered in a way consistent with flight and that it
had a broadly bird like skeleton (Figure 1.3). However,
because it lacked the well developed sternal keel of
the modern birds we cannot be sure that it was
capable of powered flight and so it may have been
more of an accomplished glider. But then again it
did have a reduced pelvis (like modern flying
birds), an enlarged furcula (wishbone) and coracoid, and a broad sternum, all of which would have
facilitated the limb flapping essential for flight. So
perhaps it did fly in the true sense of the word.
It does seem to have been at home on the ground
and has relatively long/strong running legs—perhaps
it was a wader, or darted through scrub like a
modern Roadrunner Geococcyx sp. Significantly it
had an arrangement of toes similar to that of modern perching birds, three of them pointing forwards
and one pointing backwards. This backwardspointing toe, which is properly termed the hallux, is
not found in any of the known non-avian dinosaurs.
It had well developed forelimbs and in fact these
may have been more important in locomotion than
1
2
3
4
6
5
(B)
(A)
Figure 1.3 The skeleton of Archaeopteryx (A) in comparison with that of a modern domestic pigeon (B). Note the expansion of the modern brain
case (1), the fusion of the modern hand bones (the wing) (2), the fusion of the pelvic bones and reduction of the tail to form the modern pygostyle
(3 and 4), the development of the sternum in the modern birds (to facilitate the attachment of large flight muscles (5), and the strengthening of
the modern rib cage (6). From Colbert, E.H. (1955) Evolution of vertebrates. John Wiley and Sons Inc., New York.
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EVOLUTION OF BIRDS
5
reconstructions of the conditions at the time that the
fossil bearing sediments were laid down suggest
a habitat of scrubby islands in shallow lagoons.
A predatory habit is further supported by the suggestion that this was a large-eyed animal with a
degree of binocular vision and a larger brain capacity
than contemporary animals (although not yet on a
par with modern birds).
Although Archaeopteryx does have a significant
role to play in the story of the evolution of birds, it
is not in itself the ancestor of the birds we see today.
It seems more likely that it represents a dead-end
branch on the bird evolutionary tree; one that died
out before the end of the Jurassic period (145.5 million
years ago (mya)).
the legs, being longer, stronger, and equipped with
claws. Perhaps it swam like a young Hoatzin
Opisthacomus hoazin. It had fingers suited to climbing and it had claws typical in curvature of modern
perching birds (Figure 1.4). We know this because
of the work of Derek Yalden and Alan Feduccia who
have obtained curvature measurements of the claws
of a large number of species of living bird and shown
that they form three natural groupings: ground dwellers like the pheasants with relatively straight claws,
tree climbers like the woodpeckers with strongly
curved claws, and perching birds like the finches
with intermediate claw curvature. The mean claw
curvature value of the available Archaeopteryx specimens together with the presence of the backwardspointing hallux makes it highly likely that this was
a bird capable of perching.
Classification and the nomenclature of birds,
an example
The House Sparrow:
Key reference
Yalden, D.W. (1985) Forelimb function in
Archaeopteryx. In The Beginnings of Birds. Hecht, M.,
Ostrom, J., Viohl, G., and Wellnhofer, P. (eds) Freunde
des Jura-museum, Eichstätt.
Class
Subclass
Superorder
Order
Family
Genus
Species
The teeth of Archaeopteryx suggest a carnivorous
diet and it may be that the clawed hands were used
to catch and grasp large invertebrates or small vertebrates. Perhaps it ate fish—after all, palaeoecological
Aves
Neornithines
Neognathae
Passeriformes
Passeridae
Passer
domesticus
200
180
Claw (Curvature)
160
140
120
100
Climbers
80
Perchers
60
40
Ground
20
0
0
20
10
Species
30
Figure 1.4 The variation in claw curvature in 30 species of
modern bird, grouped according to life-style characteristics. The
mean curvature of the claws of fossilized Archaeopteryx foot
claws are plotted as a solid line (amongst the perchers), those of
the hand/wing are plotted as a solid line amongst the climbers.
From Feduccia, A. (1993) Evidence from claw geometry indicating
arboreal habits of Archaeopteryx. Science 259, 790–3. Reprinted
with permission from AAAS.
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ESSENTIAL ORNITHOLOGY
1.3 The evolution of modern birds
Since the discovery of Archaeopteryx, new fossil finds
have considerably enhanced our understanding of
the evolution of the modern birds from their dinosaur ancestors. It is also becoming increasingly evident that many of the key features of birds evolved
initially in the dinosaur ancestors and as Figure 1.1
indicates, the transition from dinosaur to bird was
a gradual one, taking place over millions of years.
In the 1990s the fossilized remains of a significant
number of feathered dinosaurs were discovered in
the Liaoning province of northeast China (a collection of fossils referred to as the Jehol biota). They
included primitive birds similar at some levels to
Archaeopteryx and specimens that possessed the features of more modern birds, indicating that the bird
lineage had diversified considerable by the early
Cretaceous (145–100 mya).
The fossils included species like Sinosauropteryx
prima a small (1 m long), bipedal dinosaur (125 mya)
that was partially covered with bristle-like structures that are thought to be simple filamentous
feathers. Another of the Liaoning fossils, Microraptor
gui (120 mya) had plumulaceous feathers on its head
and body and long asymmetrical pennaceous feathers
on its tail and on both its fore and hind limbs (yes it
had four wings!), these feathers closely resemble
those of modern birds. Microraptor could certainly
glide and, because it had feathers like those of modern birds, it may have been able to exert some control over its flight. But because it lacked the skeletal
structures required for the attachment of large breast
muscles and had a long flexible tail (not good for inflight control) it may not have been capable of true
powered flight. The tail bones of modern birds are
fused during embryological development to form
the pygostyle (perhaps familiar to you as the bony
part of the ‘parsons nose’ of a chicken). The pygostyle provides a solid support for the tail feathers,
enabling them to be moved during flight so that the
bird can maintain flight path control. The earliest
examples of pygostyle-like structures are found in
fossils from the early Cretaceous period, like those
of Confuciusornis a primitive bird that also possessed
a toothless beak. Interestingly Confuciusornis is a
contemporary of the fish-eating and tooth-beaked
Icthyornithiformes (gull-like flying birds) and
Hesperornithiformes (diver-like birds, some of which
were flightless). There are of course no toothed modern birds (hence the expression ‘as rare as hens’
teeth’). The Icthyornithiformes and Hesperornithiformes
occur in the fossil record right up to the end of the
Cretaceous but none are found in the next geological
time period, the Tertiary. This is because 66 mya at
the Cretaceous/Tertiary (K/T) boundary an asteroid
collided with the earth and triggered the mass
extinction event that wiped out some 75 per cent of
life on the planet, including the dinosaurs and the
avian ancestors of the modern birds.
Key references
Feduccia, A. (2014) Avian extinction at the end of the
Cretaceous: Assessing the magnitude and subsequent
explosive radiation. Cretaceous Research 50, 1–15.
Jarvis, E.D., Mirarab, S., Aberer, A.J., et al. (2014)
Whole-genome analyses resolve early branches in the
tree of life of modern birds. Science 346(6251),
1320–31.
Jetz, W., Thomas, G.H., Joy, J.B., et al. (2012) The global
diversity of birds in space and time. Nature 491, 444–8.
There is strong fossil evidence that this event
resulted in the extinction of the majority of the bird
lineages that had evolved through the Cretaceous
period. Alan Feduccia has described the fossil
record at the K/T boundary as being scrappy and as
a result it is currently difficult to be absolutely certain, on the basis of paleontological evidence, which
types of birds had survived the mass extinction,
and which therefore diversified prior to it. But there
is some fossil evidence to support the idea that the
true modern birds evolved towards the end of the
Cretaceous and that the survivors of the mass
extinction were shorebirds or water birds. Erich
Jarvis and his colleagues have used molecular techniques to shed further light on this period of the
evolution of birds. Through a whole genome comparison of the extant orders of birds, they have
determined that the modern birds did diverge from
their ancestors during the late Cretaceous. Their
analyses date the divergence of the two major groups
of modern birds; the Palaeognathae (Tinamous and
Ostriches) and the Neognathae (all other modern
birds) to the late Cretaceous (around 100 mya).
The Neognathae subsequently diverged to form
the Galloanseres (the waterfowl) and the Neoaves
around 90 mya. Then, during the K/T transition
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EVOLUTION OF BIRDS
(around 66 mya), there was a period of rapid (10–15
million years) evolutionary radiation as species
evolved to take advantage of the diversity of ecological niches left empty as a result of the asteroid
impact and all of the modern sub-groups became
established. Moreover, phylogenetic analyses carried out by Walter Jetz and his colleagues have
shown that during the last 50 million years there
has been a significant increase in the rate of species’
diversification particularly among the Passeriformes
(songbirds) and the Anseriformes (waterfowl).
Concept
Dating evolutionary change
Palaeontologists are able to date fossil remains through
their association with sediment deposits of known
age—i.e. they use a geological clock. Molecular
biologists on the other hand are able to calibrate
rates of gene mutation within organisms through
evolutionary time—i.e. they use a molecular clock.
1.4 The phylogeny of birds
1.4.1 Morphological phylogeny
There is at present no single accepted phylogeny of
the modern birds, that is to say we do not yet have a
definitive statement of the evolutionary relationships
of different groupings of birds. Traditionally taxonomists have attempted to uncover evolutionary relationships through the comparison of morphological
characters. Figure 1.3 provides an example of this
kind of comparison, the bones highlighted are basic
characters shared by both Archaeopteryx and the modern domestic pigeon. If we were to add to this comparison the skeleton of a Passenger Pigeon Ectopistes
migratorius we would be able to use the closer similarities between the two pigeons than between either
and Archaeopteryx to infer that the pigeons were the
more closely related pair in an evolutionary sense.
1.4.2 Character conservation and convergence
However, it is not always the case that apparent
similarity of shared characters equates to close evolutionary ties. The order Passeriformae comprises
more than 5,000 species or more than half of all
extant bird species. As such they can reasonably be
described as being the dominant component of the
7
world’s avifauna. Passerines also occupy a bewildering array of ecological niches and exhibit an amazing
range of morphologies. However we can be confident that they form what is known as a monophyletic group, i.e. all of the current passerine species
have evolved from a single common ancestor.
We know this because all passerine birds share
features in common that are unique to the passerine
order. For example, most birds have a preen gland
(or uropygial gland) low on their back, just above the
base of the tail. This gland produces an oily secretion
that is used by birds to maintain the physical quality
of their feathers and to regulate bacterial and fungal
communities that grow on them. In the case of aquatic
birds the preen gland is particularly large and its
secretions are important in feather water-proofing.
Preen glands vary in their structure but all passerines
share a unique preen gland morphology. The passerines also all share a unique sperm morphology.
The spermatozoa of the birds of most orders are
straight whereas those of the passerines are helical
in structure and move forwards via a spinning
action. The passerine preen gland and sperm type
are therefore conserved characters; i.e. they have
evolved once in the early passerine ancestor and
been retained throughout the passerine radiation.
Generally those characters that remain fixed in
the face of ecological adaptation, so called conservative characters, are the most useful in classification.
Where characters do respond readily to ecological
selection pressures convergence in evolution may lead
to confusion in apparent relationships. For example,
all passerine birds have a foot that is adapted for
perching, having three forward and one backward
pointing toes. This toe arrangement is termed anisodactyly and is illustrated in Figure 1.5.
Anisodactyly is a conserved character that can
be used to confirm membership of the passerine
order (because it is only exhibited by birds that also
exhibit all of the other uniquely passerine features).
It has evolved once in the passerine ancestor and
has been retained thereafter. Figure 1.5 also illustrates
an alternative toe arrangement—zygodactyly. The
zygodactyl foot does not indicate membership of a
single order. In fact close examination of the precise
arrangement of bones of the foot suggests that zygodactyly is an example of character convergence; i.e. it
has evolved on a number of independent occasions
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8
ESSENTIAL ORNITHOLOGY
Anisodactyl
3
2
4
1
Blue Jay (Cyanocitta cristata)
Zygodactyl
2
3
1
4
Grey-faced Woodpecker (Picis canus)
Figure 1.5 Examples of the toe arrangements of two modern birds: the anisodactyl Blue Jay Cyanocitta cristata, a perching bird (A); and the
zygodactyl Grey-faced Woodpecker Picis canus, a climbing bird (B). These are just two of 15 different avian toe arrangements. Adapted from
Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology: Avian Structure and Function. Yale University Press, New Haven.
in a range of unrelated species and orders including
the Osprey Pandion haliaetus, the woodpeckers
(Picidae), the owls (Strigidae), and some swifts
(Apodidae).
Not all of the characters used in taxonomy are
skeletal/anatomical however and comparisons of
plumage, behaviour, vocalizations, and even
ectoparasites have all been used in attempts to elucidate avian evolutionary relationships. But perhaps the most exciting development in efforts to
unravel the avian phylogenetic tree in recent times
is the use of biomolecular information—information about genes and their chemical products.
Concept
DNA deoxyribonucleic acid
The nuclei of our cells contain chromosomes; paired
strands of DNA arranged in the iconic double helix with
which we are all no doubt familiar.
Sequences of the basic units of these strands act
as templates for the production of proteins—these
templates are our genes. We inherit one strand of each
of our chromosomes from our father and one from our
mother.
Mitochondria, the powerhouses of our cells, also
each contain a small circle of DNA. This mtDNA we
inherit only from our mothers.
When genes are inherited they may change, either as
a result of the recombination of nuclear DNA from two
parental sources, or as a result of mutations, accidental
copying errors in either nuclear DNA or mtDNA.
Key references
Sibley, C.G. and Ahlquist, J.E. (1990) Phylogeny and
classification of birds. Yale University Press, New Haven.
Jarvis, E.D., Mirarab, A., Aberer, A.J., et al. (2014) Whole
genome analyses resolve early branches in the tree of
life of modern birds. Science 346(6215), 1320–31.
Prum, R.O., Berv, J.S., Field, D.J., et al. (2015) A
comprehensive phylogeny of birds (Aves) using targeted
next-generation sequencing. Nature 526, 569–73.
1.4.3 Biomolecular phylogeny
In 1990 Sibley and Ahlquist published a phylogeny
of avian families based on the process of DNA-DNA
hybridization. In simple terms they directly compared
the chemical structure of the DNA of different bird
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EVOLUTION OF BIRDS
species. Their work pioneered the use of biochemical
characters in avian phylogeny, but their results did
not produce a definitive avian tree and were limited
because of the small units of DNA used and therefore the limited number of characters involved in
tree construction. Subsequent workers in the field
have used improved molecular techniques to gain a
better level of discrimination between taxa, particularly but not exclusively, at the species level,
through the comparison of mitochondrial DNA and
nuclear gene sequences. I began this section by stating that there is no single accepted phylogeny of
birds and that remains the case. Since the publication of the first molecular phylogeny of birds there
9
have been numerous attempts to elucidate the relationships of the extant bird taxa and almost 300
putative trees had been published during the 30
years prior to my writing this. Attempts to arrive at
a definitive phylogeny are dogged by data availability and trees vary depending upon the method and
data used to construct them. However, Sushma
Reddy and her colleagues have carried out an analysis
comparing a number of recently proposed phylogenies and the methodologies used in their construction and have proposed the consensus tree that I
have included as Figure 1.6. But this is an exciting
and rapidly moving field and I would recommend
that any student with an interest in this area regularly
Ostrich Struthioniformes
Tinamous Tinamiformes
Waterfowl Anseriformes
Landfowl Galliformes
Flamingos Phoenicopteriformes
Grebes Podicipediformes
Doves Columbiformes
Sandgrouse Pterocliformes
Mesites Mesitornithiformes
Shorebirds Charadriiformes
Cranes, Rails Gruiformes
Hoatzin Opisthocomiformes
Nightjars & allies Caprimulgiformes
Swifts Caprimulgiformes
Hummingbirds Caprimulgiformes
Turacos Musophagiformes
Bustards Otidiformes
Cuckoos Cuculiformes
Tropicbirds Phaethontiformes
Sunbittern Eurypygiformes
Loons Gaviiformes
Pelicans & allies Pelecaniformes
Tubenoses Procellariiformes
Penguins Sphenisciformes
New World vultures Accipitriformes
Eagles, Hawks Accipitriformes
Owls Strigiformes
Mousebirds Coliiformes
Cuckoo-roller Leptosomiformes
Trogons Trogoniformes
Hornbills & allies Bucerotiformes
Bee-eaters& allies Coraciiformes
Woodpeckers & allies Piciformes
Seriemas Cariamiformes
Falcons Falconiformes
Parrots Psittaciformes
Passerines Psittaciformes
Figure 1.6 A phylogeny of birds. Adapted from
Reddy, S., Kimball, R.T., Pandey, A., et al. (2017) Why
do phylogenetic data sets yield conflicting trees? Data
type influences the avian tree of life more than taxon
sampling. Systematic Biology 66(5), 857–79, by
permission of Oxford University Press. The tree is a
consensus of their own Early Bird II tree and trees
previously proposed by Erich Jarvis and Richard Prum.
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10
ESSENTIAL ORNITHOLOGY
consult the excellent websites https://tree.open
treeoflife.org and the Encyclopedia of Life http://
www.eol.org for updates.
1.5 Adaptive radiation and speciation
One of the first things that a bird watcher notices is
that there is an amazing diversity of form even
within groups of closely related bird species. Living,
as I do, on the coast, the bills of the wading birds are
my favourite example of this phenomenon. I regularly see as many as a dozen species feeding along
the same area of shore, all of them members of the
same order the Charidriiformes, but ranging in bill
morphology from the tiny, straight bill of the Little
Ringed Plover Charidrius dubius used to delicately
pick isopods from the strand line, to the long decurved bill of the Eurasian Curlew Numenius arquata
used to probe deep into wet sand to drag out large
polychaetes, to the heavy hammering bill of the
Eurasian Oystercatcher Haematopus ostralegus ideal
for smashing open the shells of bivalve molluscs
(Figure 1.7).
Flight path: foraging behaviour and the concept of
niche, page 147.
This diversity of bill shape allows the birds to coexist
without competing too closely for food—they each
Eurasian Bar-tailed
Curlew Godwit
occupy their own feeding niche. As such their bills
and associated mode of feeding can be described as
evolutionary adaptations which enhance their individual survival by reducing the interspecific competition that they experience.
The observed diversity in bill morphology is one
visible outcome of a process of adaptive radiation—
we can presume that at one time the ancestral
Charidriiform bill was pretty uniform, but that
through evolutionary time and in parallel with the
evolution of all of the various wader species, it has
evolved as a result of natural selection.
1.5.1 Darwin’s finches
This is the same phenomenon that has given rise to
perhaps the most iconic of examples of adaptive
radiation, that of the finches of the Galapagos and
Cocos Islands. There are 15 species of so-called
Galapagos finch, 14 of them are endemic to the
Galapagos Islands and one is only found on the
Cocos Islands. Galapagos, or Darwin’s finches as
they are also often called (Charles Darwin did collect the first specimens of these species, but they
were not quite as pivotal in the development of his
ideas as is often assumed to be the case) have been
presumed to have evolved from an ancestral species that accidentally colonized these isolated
Eurasian
Oyster- Common Red
catcher Redshank Knot
Little
Gray Ringed Ruddy
Plover Plover Turnstone
4 cm
Figure 1.7 Because their bill morphology varies, species of wading shore birds are able to forage alongside one another with minimal
competition. From Gill, F.B. (2007) Ornithology. 3rd edn Freeman, New York (after Goss-Custard, J.D. (1975) Beach feast. Birds
September/October 23–6).
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EVOLUTION OF BIRDS
islands from the South American mainland close to
1,000 km away. Through the comparison of nuclear
DNA and mtDNA sequences of the Galapagos
finches and a range of putative mainland relatives,
Sato and colleagues have recently deduced that the
closest living mainland relative of the Galapagos
finches is the Dull-coloured Grassquit Tiaris obscura,
a species which inhabits humid forest edges, farmland, and scrub throughout Venezuela, Colombia,
western Ecuador, and western and southern Peru,
habitats not dissimilar to those encountered in the
islands by the colonists. T. obscura is not the direct
ancestor of the Galapagos finches, but it is likely
that they shared a common ancestor.
Key reference
Sato, A., Tichy, H., O’hUigin, C., et al. (2001) On the
Origin of Darwin’s Finches. Molecular Biology and
Evolution 18(3), 299–311.
Concept
Species
The species is the unit we use to measure biological
diversity. Typically species are defined as populations of
potentially interbreeding individuals that are reproductively
isolated from one another (Biological Species Concept).
The early colonists probably arrived on just one of
the islands and found an environment devoid of
competition but rich in potential resources. They
are presumed to have formed a self-sustaining
population from which groups of individuals went
on to eventually colonize the other islands in the
group. Living on these isolated islands, each population of birds may have become a specialist in the
exploitation of a particular resource and through the
process of natural selection their populations will have
diverged from one another in terms of ecology, behaviour, and crucially, genetics. Through time these isolated populations of birds may have diverged from
one another to such a level that, if two populations
were to re-colonize the same island and coexist, they
would remain isolated from one another in the
sense that they would have evolved to become separate species.
The coexistence of two or more finch species on a
single island would probably have increased the
rate of divergence as birds increased their levels of
behavioural/ecological isolation from one another
as they became increasingly specialized to avoid
interspecific competition. Box 1.1 provides more
information about natural selection and the results
of a natural experiment that demonstrates evolution in action.
Box 1.1 Evolution in action: natural selection and the morphology of finch bills
I am sure that if you take the time to think about the characteristics of populations you will note the following:
• Not all individuals are the same. That is to say there is
considerable variation within a species.
• Offspring resemble their parents. This is because heritable
variations are passed from parents to their offspring
through their genes.
• Reproductive over-production is common. Many more
individuals are produced than can ever survive to mature
and reproduce.
These basic observations, a prodigious amount of patient
work, and probably a touch of genius, allowed Charles
Darwin to construct his theory of evolution by natural selection. Long before the importance of genes was appreciated he
realized that some heritable property of certain individuals
11
placed them at an advantage relative to others of their kind.
Through time, the differential survival of these individuals
should result in a shift in the makeup of the population such
that animals without the advantage become increasingly
rare (or perhaps disappear) and those possessing it become
more common (Figure 1.8). He proposed a scenario under
which beneficial traits were selected for and detrimental
traits were selected against.
We now understand that selection can be strongly directional in the way that I have just described, leading to the
increasing dominance of a trait or to its eradication, or it can act
in a disruptive way resulting in the evolution of two populations
that have very different but successful phenotypes. Selection
can also act in a stabilizing way to maintain the status quo.
continued
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ESSENTIAL ORNITHOLOGY
Box 1.1 Continued
A
B
A
C
Seed abundance (g/m2)
12.0
10.0
8.0
6.0
4.0
2.0
B
So can we see evolution by natural selection actually happening? Well thanks to the work of Peter Grant, Peter Boag,
and their colleagues we can. They have carried out a very
detailed study of the population of the Medium Ground Finch
Geospiza fortis on the tiny island of Daphne Major, one of the
Galapagos Islands. Since the mid 1970s these researchers
have ringed and measured almost all of the G. fortis on the
island, they have recorded year on year survivorship and have
regularly trapped birds to take measurements from them.
These measurements include mass, wing length, tarsus
length, and bill length and depth. During the early years of
their study Daphne Major received regular seasonal rainfall
(around 130 mm per year) and the finch populations did well.
But in 1977 the island suffered an intense drought with just
24 mm of rain falling during the wet season. The impact upon
the birds was dramatic. They made no breeding attempts,
many birds delayed their moult, or failed to moult at all, and
significant levels of mortality were recorded (an 85 per cent
decline in the population in just one season).
The drought did not just affect the birds on the island.
Many plants failed to set seed leading to a food shortage for
the finches and most of the finch mortality could be attributed either directly or indirectly to starvation. However some
birds did survive. They tended to be the bigger birds in the
population with bigger beaks (Figure 1.9).
1400
Population size
Figure 1.8 The effect of directional (A), stabilizing (B), and
disruptive (C) selection upon a hypothetical population. In each
case an arrow indicates the direction of the selection taking place,
the solid line describes the pre-selection population, and the
broken line the post-selection population(s). From Scott,
G.W. (2005) Essential Animal Behavior. Blackwell Science,
Cambridge.
1000
800
200
C
1.0
Males
0.8
Principal component 1
12
0.6
0.4
All birds
0.2
0.0
–0.2
Females
–0.4
J S N J MM J S N J MM J S N J MM J S N J
1975
1976
1977
1978
Figure 1.9 Under drought conditions in 1977/78 seed
production on the Galapagos islands fell (A). Without food the
finch population crashed (B) but some birds did survive. The
principal component plotted in graph C is a mathematical measure
of the morphology of the finch population. As the drought
progresses morphology clearly changes. In fact by 1978 only larger
birds with larger beaks remain in the population. Adapted from
Boag, P.T. and Grant, P.R. (1981) Intense natural selection in a
population of Darwin’s finches (Geospizinae) in the Galapagos.
Science 214, 82–825. Reprinted with permission from AAAS.
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EVOLUTION OF BIRDS
In effect what has happened here is a burst of intense directional selection. Initially the population exhibited size variation—smaller birds with smaller beaks and bigger birds with
bigger beaks. When the seed crop failed the available seeds
were used up quickly, and initially it seems that smaller seeds
were consumed preferentially. When seeds became scarce the
bigger birds changed their feeding behaviour to exploit the bigger seeds, but the smaller birds did not have the beak morphology needed to crack these seeds and starved. Thus some of
the observed variation in beak size was lost from the population which became dominated by bigger birds. But surely that
wasn’t the first drought to have occurred so why were there
small birds in the population? By continuing to study the finch
population of Daphne Major these dedicated researchers seem
to have the answer. Although natural selection favours large
size in response to drought, small size is favoured in response
to particularly wet years (when there are many more smaller
seeds than larger seeds) and during the first year of a bird’s life
(possibly for metabolic reasons). It would seem therefore that
in effect, size in G. fortis is an example of oscillating selection,
repeated bursts of opposing directional selection in response to
extremes of climate and associated fluctuations in food supply
(Figure 1.10). This work demonstrates two important things: it
shows us that we can see evolution in action and it shows us
that very long term studies are important.
1.5.2 Genes and evolution
Advances in genome level analysis are providing
exciting insights into the genes that are directly
involved in the changes that take place during the
evolutionary process. For example it has recently
been demonstrated that variations in the gene ALX1,
a gene known to be involved in the development of
the cranium and facial features of humans, is linked to
beak morphology in the Galapagos finches (although
an exact role has yet to be determined). An interacting effect of two other genes CaM and BMP4 and
their products has also been demonstrated to be
important. Calmodulin (CaM) is a calcium-binding
protein, and bone morphometric protein (BMP4) is
involved in bone and cartilage development. Variation
in the expression of these genes and the actions of
their protein products have been shown to be involved
in the differential growth of finch beaks (Figure 1.11).
These genes might therefore be important in the
speciation of these finches. Similarly the identification of the genes involved in the evolution of new
migratory strategies in the Blackcap Sylvia atricap-
1976–77
1984–85
13
WT
WG
TAR
BL
BD
BW
WT
WG
TAR
BL
BD
BW
0
Smaller Direction of Selection
Larger
Figure 1.10 Oscillating selection for finch size in response to
climate. During dryer periods (such as the mid 1970s) selection
favours bigger birds. However, following wet periods (such as the
El Niño of 1982/83) smaller size is favoured. Biometrics listed
include: WT, weight; WG, wing length; TAR, tarsus length; BL, bill
length; BD, bill depth; and, BW, bill width. Adapted from Gibbs,
L.H. and Grant, P.R. (1987) Oscillating selection on Darwin’s
finches. Nature 327, 511–513.
illa, a European songbird, and those associated with
morphological change in populations that are
becoming isolated as a result of differential migration, may provide further insights into the genetic
changes taking place during speciation events. This
is a topic that will be returned to in chapter 3.
Flight path: evolution and bird migration, page 52.
Key references
Abzhanov, A., Protas, M., Grant, B.R., et al. (2004)
Bmp4 and morphological variation of beaks in
Darwin’s Finches. Science 305, 1462–5.
Lamichaney, S., Berglund, J., Almén, M.S., et al.
(2015) Evolution of Darwin’s finches and their beaks
revealed by genome sequencing. Nature 518, 371–5.
1.5.3 Hybrids
When the behavioural and genetic isolation between
two species is incomplete it may be possible for
hybridization to occur. In some cases these hybrids
might be sterile and so make no genetic contribution
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ESSENTIAL ORNITHOLOGY
(B)
Depth
(A)
D
Upper
beak
R
Sharp-beaked finch
C
dth
us
bin
ct
g ca
Pro
rui
flow
/f
era
t
Pr
flo obin
we g
rs cac
/fr tu
ui s
t
Wi
V
Length
Low CaM;
short beak
Mixed diet of
seeds and insects
Low BMP4:
low beak dept/width
Crusing seeds
14
C
l a r r ush
g e in
se g h
ed ar
s d/
Low BMP4:
low beak depth/width
Low-mod. BMP4:
Mod. BMP4:
mod. beak depth/width mod. beak depth/width
Early/high BMP4:
high beak depth/width
High CaM;
elongated beak
High CaM;
elongated beak
Low CaM;
short beak
Cactus finch
Large cactus finch
Low CaM;
short beak
Medium ground
finch
Large ground finch
Figure 1.11 The morphology of a beak can vary along three axes: depth, width, and length (A) BMP- and CaM-dependent signalling regulates
growth along these axes resulting in a broad range of beak shapes. (B) The figure illustrates the way in which CaM/BMP variation has resulted in
the development of a range of beak morphologies. Adapted from Abzhanov, A., Kuo, W.P., Hartmann, C., et al. (2006) The calmodulin pathway and
evolution of elongated beak morphology in Darwin’s finches. Nature 442, 563–67.
to the next generation themselves, as such they
are an evolutionary dead end and should probably
be regarded as no more than a curiosity. But
occasionally these hybrids are fertile and may
reproduce either amongst themselves, or with one
or other of their parent species. There are two
main outcomes possible as a result of this phenomenon. In some cases hybrid zones are formed
when the stable ranges of two geographically
adjacent species overlap. In other cases transient
hybridization, or genetic swamping, occurs as the
range of one species expands and previously isolated species are brought into contact with one
another.
The classic example of the stable hybrid zone is
that of the black and grey Hooded Crow Corvus cornix of northern and eastern Europe and the all black
Carrion Crow Corvus corone of southern Europe.
Along the narrow (2,100 km long but only 50–120
km wide) contact zone between the populations of
these two crows they freely interbreed and their
hybrids exhibit a plumage that is intermediate
between the two types (black with varying amounts
of grey).
One fascinating example of transient hybridization is that of the Blue-winged and Golden-winged
warblers Vermivora pinus and V. chrysoptera of
North America. Ornithologists 200 years ago would
have known the Blue-winged Warbler as a southern species, and the Golden-winged warbler as a
species found in the north, but today the ranges of
the two species overlap and that of the Blue-winged
Warbler is increasing whilst the Golden-winged
Warbler is becoming increasingly scarce. This shift in
the range of the Blue-winged Warbler is a response
to an increase in their preferred secondary scrub
habitat and is largely a result of human clearances
of forested areas. Increased scrub cover also benefited Golden-winged Warblers initially but where
the two species do overlap, Golden-wings eventually disappear. This disappearance takes about 50
years so it isn’t simply the case that the Blue-wings
see off the competition immediately. In fact the two
species do coexist initially but where they do, two
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EVOLUTION OF BIRDS
new ‘species’ also appear. These are hybrids. One,
Brewster’s Warbler Vermivora chrysoptera x pinus, or
V. ‘leucobronchialis’, is a bird with the body plumage
of a Golden-winged Warbler and the face pattern of
a Blue-winged Warbler. The other is Lawrence’s
Warbler Vermivora pinus x chrysoptera or V. ‘lawrencei’ which has a Golden-wing face pattern and
Blue-wing body (Figure 1.12).
The pattern of the hybrids’ appearance is predictable whenever the two parent species come into
contact. Initially there are good numbers of Goldenwings in a population, but as numbers of immigrant
Blue-wings increase the numbers of Brewster’s type
hybrids also increases. These hybrids are fertile and
backcross with both of the parent species resulting
in intermediate types and in the rarer Lawrence’s
15
type hybrid. As this process of hybridization and
backcrossing continues, Golden-winged Warblers
become increasingly rare. Eventually Blue-winged
Warblers dominate the community, Golden-winged
Warblers have all but gone and hybrid types are
rarely seen. However, as a result of the backcrossing of hybrids, the genes of the Golden-winged
Warblers may persist in the Blue-winged Warbler
population with the result that an occasional aberrant form may appear. This process of genetic takeover is referred to as ‘swamping’. Where a species is
introduced to habitat outside of its natural range
hybridization can become a major issue. Box 1.2
provides a real example of the threat of hybridization and of the difficult decisions and actions that
environmental managers sometimes have to take.
Lawrence’s Warbler
(Vermivora pinus x chrysoptera,
or V. ‘lawrencei’ )
Brewster’s Warbler
(Vermivora chrysoptera x pinus,
or V. ‘leucobronchialis’ )
Blue-winged Warbler
(Vermivora pinus)
Golden-winged Warbler
(Vermivora chrysoptera)
Figure 1.12 The Blue-winged Warbler/Golden-winged Warbler hybrid types. From Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology: Avian
Structure and Function. Yale University Press, New Haven.
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ESSENTIAL ORNITHOLOGY
Box 1.2 Hybridization and duck conservation
The White-headed Duck Oxyura leucocephala is an eastern
European and central Asian species with a small isolated
population in Spain. Populations are fragmented and under
increasing pressure due to loss of habitat. This coupled with
the fact that populations are small and declining makes this
species globally endangered (the Spanish population fell to
just 22 birds in 1977, and the main central Asian population
fell from 100,000 in the 1930s to 10,000 in 2000). In
Europe the species faces another threat—genetic swamping
through hybridization with an alien invader!
The alien in question is the Ruddy Duck Oxyura jamicensis
a close relative of the White-headed Duck but one that
would naturally be isolated from it by the Atlantic Ocean. In
their native range (North and South America) Ruddy Duck
are a successful species with an increasing population (of
more than half a million birds). They are an attractive duck
and have been popular additions to wildfowl collections for
many years. In Britain in the 1950s or early 1960s, Ruddy
Duck from such collections were accidentally released and a
feral population quickly established itself such that the
population grew from a handful of original birds to some
6,000 individuals in 50 years.
If the British Ruddy Duck population had stayed in Britain
it may not have posed much of a problem, but as the population grew increasing numbers of Ruddy Duck, presumed to
originate from Britain, were reported from a number of
European countries. It was first recorded in Spain in the
1980s and in 1991 the first hybrids between invading Ruddy
Duck and Spanish White-headed Duck were quickly reported.
The hybrids were fertile and second generation hybridization
was observed. In this situation there is obviously the possibility that the genome of the Ruddy Duck would swamp that
of the White-headed Duck in Spain and another valuable
population would disappear. And if the Ruddy Duck were to
spread across Europe and invade central Asia, the Whiteheaded Duck might disappear as a distinct species.
Extinction by genetic swamping might seem far-fetched,
but Judith Mank and others have demonstrated that in the
case of at least one other duck species this might be just
what is happening. Mank and colleagues have compared
the genomes of American Black Duck Anas rubripes and
European Mallard Anas platyrhynchos. Mallard were introduced to the Americas probably by early settlers and they did
very well there. They are closely related to Black Duck and so
it is not very surprising that Mank and her colleagues found
genetic similarities between them. But as well as making a
comparison of today’s populations she also took material
from museum specimens collected between 1900 and 1935,
and was therefore able to establish their contemporary and
historical relatedness. Her results showed that the genetic
distinction between the two species is shrinking, presumably
as a result of continuing hybridization and genetic swamping. In the conclusion to her paper, Mank makes the somewhat sombre statement that ‘The implications of our findings
for the conservation of the black duck are grim. Without
preventing hybridization, conservation of pristine black duck
habitat will be ineffective in preserving the species’. So can
hybridization be prevented in such a situation?
In the case of the White-headed Duck situation it may
not be too late. There are various articles of legislation
that are used by the international community to bring
pressure upon nation states to take action for conservation.
In this case the relevant agreement is the Bonn Convention:
the Convention on the Conservation of Migratory Species.
Within the convention there is an agreement, The AfricanEurasian Migratory Water bird Agreement (AEWA) designed
to provide a legal framework for the conservation and
management of 172 species of bird that are ecologically
dependent upon wetland habitats. There are 116 signatory
nations to the AEWA in Europe, Africa, north-east Arctic
Canada, Greenland, Asia Minor, the Middle East, Kazakhstan,
Turkmenistan, and Uzbekistan. The list includes a number of
states which have White-headed Duck populations. Amongst
other conservation measures the AEWA encourages states
to assess the impact that alien species might have in the
context of wetlands. Article III of the agreement requires signatories to prohibit the deliberate introduction of non-native
water birds into the wild and to take all reasonable measures to prevent their accidental release. This is very positive,
but these steps will not solve the Ruddy Duck problem—the
birds are already out there. However, the AEWA also requires
that signatories ‘ensure that when non-native species or
hybrids thereof have already been introduced into their territory, those species or their hybrids do not pose a potential
hazard to the population listed’. So here is the legal requirement for the control of the Ruddy Duck in Europe. If that was
insufficient in itself, the Council of Europe have published a
specific action plan for the conservation of White-headed
Duck and the Bern Convention has put forward a strategy
for the eradication of the Ruddy Duck throughout the
Western-Palaearctic region. Ruddy Duck control measures
are now in place and birds have been culled throughout
Europe. Eradication efforts in Spain and the UK have been
particularly successful; Ruddy Duck and hybrids are now a
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EVOLUTION OF BIRDS
rarity in Spain and the UK population is almost extinct. At a
European level the population of Ruddy Duck in 2013 had
been reduced to just 7 per cent of that in 2000. The picture
does vary country by country, but the long term goal of
the complete removal of Ruddy Duck from the European
continent does seem to be achievable. We can be optimistic
that this particular threat to the White-Headed Duck can be
overcome, but of course the future security of the species
will depend upon other conservation actions to protect
specific habitats and populations.
Summary
Birds are specialist vertebrates thought to have
evolved from theropod dinosaurs. The evolutionary
relationships of modern birds species are not yet
fully understood, but advances in phylogeny and
new molecular techniques are bringing them within
our grasp. Like all organisms, birds continue to adapt
and evolve in the face of environmental pressure.
Appendix 1
Familiar names of the members of the Orders
and Families of modern birds
The list follows Joseph del Hoyo and Nigel
Collar’s Illustrated Checklist of the Birds of the World
volume 1 (2014, Non-Passerines) and volume 2 (2016,
Passerines), Lynx Edicions, Barcelona. As I highlighted earlier in this chapter, the phylogeny of
birds is a fast-moving field and so this list should
not be considered to be a definitive.
Struthioniformes
Struthionidae
Rheidae
Tinamidae
Casuariidae
Apterygidae
Galliformes
Megapodiidae
Cracidae
Numididae
Odontophoridae
Phasianidae
Ostrich
Rheas
Tinamous
Cassowaries and emu
Kiwis
Megapodes
Curassows, guans, and chachalas
Guineafowl
New world quail
Pheasants, partridges, grouse turkeys, old
world quail
References and further reading
Mank, J.E., Carlson, J.E., and Brittingham, M.C. (2004) A century of
hybridization: Decreasing genetic distance between American
black ducks and mallards. Conservation Genetics 5, 395–403.
Rehfisch, M.M., Blair, M.J., McKay, H., and Musgrove, A.J. (2004) The
impact and status of introduced waterbirds in Africa, Asia Minor,
Europe and the Middle East. Acta Zoologica Sinica 52, 572–5.
Robertson, P.A., Adriaens, T., Caizergues, A., et al. (2015) Towards
the European eradication of the North American ruddy duck.
Biological Invasions 17, 9–12.
Anseriformes
Ahnhimidae
Anseranatidae
Anatidae
Podicipediformes
Podicipedidae
Screamers
Magpie goose
Ducks, geese, and swans
Grebes
Phoenicopteriformes
Phoenicopteridae
Flamingoes
Phaethontiformes
Phaethontidae
Tropicbirds
Eurypygiformes
Euripygidae
Rhynochetidae
Sunbittern
Kagu
Mesitornithiformes
Mesitornithidae
Mesites
Columbiformes
Columbidae
Pigeons and doves
Pterocidiformes
Pteroclididae
Sandgrouse
Caprimulgiformes
Steatornithidae
Podargidae
Nyctibiidae
Caprimulgidae
Aegothelidae
Apodidae
Trochilidae
Oilbirds
Frogmouths
Potoos
Nightjars or goatsuckers
Owlet-nightjars
Swifts
Hummingbirds
Opisthocomiformes
Opisthocomidae
Hoatzin
Cuculiformes
Cuculidae
Cuckoos, roadrunners, and anis
Gruiformes
Hellornithidae
Rallidae
Psophiidae
Aramidae
Finfoots
Rails, gallinules, and coots
Trumpeters
Limpkin
17
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ESSENTIAL ORNITHOLOGY
Gruidae
Cranes
Otidiformes
Otididae
Bustards
Musophagiformes
Musophagidae
Gaviiformes
Gaviidae
Sphenisciformes
Spheniscidae
Accipitriformes
Sagittariidae
Pandionidae
Accipitridae
Secretary-bird
Osprey
Hawks, eagles, kites, old world vultures
Turacos
Coliiformes
Coliidae
Mousebirds
Divers or loons
Leptosomiformes
Leptosomatidae
Trogoniformes
Trogonidae
Trogons
Bucerotiformes
Bucerotidae
Upupidae
Phoeniculidae
Hornbills
Hoopoes
Woodhoopoes
Coraciiformes
Meropidae
Coraciidae
Brachypteraciidae
Todidae
Momotidae
Alcedinidae
Bee-eaters
Rollers
Ground-rollers
Todies
Motmots
Kingfishers
Piciformes
Galbulidae
Bucconidae
Ramphastidae
Capitonidae
Semnornithidae
Megalaimidae
Lybiidae
Indicatoridae
Picidae
Jacamars
Puffbirds
Toucans
New world barbets
Prong-billed barbets
Asian barbets
African barbets
Honeyguides
Woodpeckers and allies
Cariamiformes
Cariamidae
Seriemas
Falconiformes
Falconidae
Falcons and caracaras
Psittaciformes
Strigopidae
Cacatuidae
Psittacidae
New Zealand parrots
Cockatoos
Parrots
Passeriformes
Acanthisittidae
Pittidae
Philepittidae
Eurylamidae
Sapayoidae
Calyptomenidae
Thamnophilidae
Conopophagidae
Melanopareiidae
Grallariidae
Rhynocryptidae
Formicariidae
New Zealand wrens
Pittas
Asites
Typical broadbills
Sapayoa
African and green broadbills
Typical ant birds
Gnateaters
Crescentchests
Antpittas
Tapaculos
Ground-antbirds
Penguins
Procellariiformes
Oceanitidae
Hydrobatidae
Diomedidae
Procelariidae
Southern storm-petrels
Northern storm-petrels
Albatrosses
Shearwaters and petrels
Ciconiiformes
Ciconiidae
Storks
Pelecaniformes
Threskiornithidae
Ardeidae
Scopidae
Balaenicipitidae
Pelicanidae
Ibises and spoonbills
Herons, egrets, and bitterns
Hamerkop
Shoebill
Pelicans
Suliformes
Fregatidae
Sulidae
Phalacrocoracidae
Anhingidae
Frigatebirds
Boobies and gannets
Cormorants
Anhingas
Charadriiformes
Burhinidae
Chionididae
Pluvianellidae
Pluvianidae
Haematopodidae
Ibidorhynchidae
Recurvirostridae
Charadriidae
Pedionomidae
Thinocoridae
Rostratulidae
Jacanidae
Scolopacidae
Turnicidae
Dromadidae
Glareolidae
Laridae
Stercorariidae
Alcidae
Thick-knees
Sheathbill
Magellanic plovers
Egyptian plovers
Oystercatchers
Ibisbill
Avocets and stilts
Plovers
Plains-wanderer
Seedsnipe
Painted-snipe
Jacanas
Sandpipers
Button-quails
Crab-plover
Coursers and pratincoles
Gulls, terns, and skimmers
Skuas
Auks
Strigiformes
Tytonidae
Strigidae
Barn owls
Typical owls
Cathartiformes
Cathartidae
New world vultures
Cuckoo-roller
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Furnariidae
Pipridae
Cotingidae
Tityridae
Tyrannidae
Menuridae
Atrichornithidae
Ptilonorhynchidae
Climacteridae
Maluridae
Dasyornithidae
Meliphagidae
Pardalotidae
Acanthizidae
Orthonychidae
Pomatostomidae
Mohouidae
Eulacestomidae
Neosittidae
Oriolidae
Paramythiidae
Oreoicidae
Cinclosomatidae
Falcunculidae
Pachycephalidae
Psophodidae
Vireonidae
Campephagidae
Rhagologidae
Artamidae
Machaerirhynchidae
Vangidae
Platysteiridae
Aegithinidae
Pityriasidae
Malaconotidae
Rhipiduridae
Dicruridae
Ifritidae
Monarchidae
Platylophidae
Laniidae
Corvidae
Melampittidae
Corcoracidae
Paradisaeidae
Callaeidae
Notiomystidae
Melanocharitidae
Cnemophilidae
Picathartidae
Eupetidae
Chaetopidae
Petroicidae
Hyliotidae
Stenostiridae
Ovenbirds
Manakins
Cotingas
Tityras and allies
Tyrant-flycatchers
Lyrebirds
Scrub-birds
Bowerbirds
Australasian treecreepers
Fairywrens
Bristlebirds
Honeyeaters
Pardalotes
Thornbills
Logrunners
Australian babblers
Mohouas
Ploughbill
Sittellas
Old world orioles
Painted berrypeckers
Australo-Papuan bellbirds
Quail-thrushes and jewel-babblers
Shrike-tits
Whistlers
Whipbirds and wedgebills
Vireos
Cuckoo-shrikes
Berryhunter
Woodswallows and butcherbirds
Boatbills
Vangas and allies
Batises and wattle-eyes
Ioras
Bristlehead
Bush-shrikes
Fantails
Drongos
Ifrit
Monarch-flycatchers
Crested jay
Shrikes
Crows and jays
Melampittas
Australian mudnesters
Birds-of-paradise
New Zealand wattlebirds
Stitchbird
Berrypeckers and longbills
Satinbirds
Picathartes
Rail-babbler
Rockjumpers
Australasian robins
Hyliotas
Fairy flycatcher and allies
Paridae
Remizidae
Alaudidae
Panuridae
Nicatoridae
Macrosphenidae
Cisticolidae
Acrocephalidae
Pnoepygidae
Locustellidae
Donacobiidae
Bernieridae
Hirundinidae
Pycnonotidae
Phylloscopidae
Scotocercidae
Aegithalidae
Sylviidae
Zosteropidae
Timaliidae
Pellormeidae
Leiotrichidae
Certhiidae
Sittidae
Polioptilidae
Troglodytidae
Cinclidae
Buphagidae
Sturnidae
Mimidae
Turdidae
Muscicapidae
Regulidae
Dulidae
Hypocoliidae
Hylocitreidae
Bombycillidae
Ptiliogonidae
Elachuridae
Promeropidae
Modulatricidae
Irenidae
Chloropseidae
Dicaeidae
Nectariniidae
Prunellidae
Peucedramidae
Urocynchramidae
Ploceidae
Estrildidae
Viduidae
Passeridae
Motacillidae
Fringillidae
Calcariidae
Tits and chickadees
Penduline-tits
Larks
Bearded reedling
Nicators
Crombecs and allies
Cisticolas and allies
Reed-warblers
Cupwings
Grasshopper-warblers and Grassbirds
Donacobius
Tetrakas
Swallows and martins
Bulbuls
Leaf-warblers
Bush-warblers
Long-tailed tits
Old world warblers and parrotbills
White-eyes
Scimitar-babblers and allies
Ground babblers
Laughing thrushes and allies
Treecreepers
Nuthatches
Gnatcatchers
Wrens
Dippers
Oxpeckers
Starlings
Mockingbirds and thrashers
Thrushes
Old world flycatchers
Kinglets and firecrests
Palmchat
Hypocolius
Hylocitreas
Waxwings
Silky-flycatchers
Elachura
Sugarbirds
Spot-throat and allies
Fairy-bluebirds
Leafbirds
Flowerpeckers
Sunbirds
Accentors
Olive warbler
Przevalski’s Rosefinch
Weavers
Waxbills
Whydahs and indigobirds
Old world sparrows
Wagtails and pipits
Finches
Longspurs
19
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ESSENTIAL ORNITHOLOGY
Rhodinocichlidae
Emberizidae
Passerellidae
Zeledoniidae
Teretistridae
Icteridae
Parulidae
Thrush-tanager
Old world buntings
New world sparrows
Wren thrush
Cuban warblers
New world blackbirds
New world warblers
Phaenicophilidae
Spindalidae
Nesospingidae
Calyptophilidae
Mitrospingidae
Cardinalidae
Thraupidae
Hispaniolan tanagers
Spindalises
Puerto Rican tanagers
Chat-tanagers
Mitrospingid tanagers
Cardinals
Tanagers
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C H A PT ER 2
Feathers and flight
‘Birds are pilot and aircraft in one.’
John Videler (2006)
‘No bird soars too high if he soars on his own wings.’
William Blake, (1793)
Although not unique to birds, the power of flight
and feathers are probably their distinguishing feature in the eyes of most people. In this chapter I
want to take some time to consider the feathers that
make flight possible, their growth, their maintenance, and their replacement through moult. I will
also describe the anatomical adaptations of birds to
flight, and the process of flight itself.
Chapter overview
2.1
2.2
2.3
2.4
2.5
2.6
2.7
2.8
Feathers
Feather tracts
Feather colour
Feather damage
Feather maintenance
Moult
Flight
The evolution of flight and flightlessness
2.1 Feathers
Feathers were once thought to be one of, if not the,
defining character of birds. But recent discoveries of
fossil dinosaur feathers, indistinguishable from
those of modern birds, prove that this is not the
case. It has also been a commonly held belief that
feathers evolved in association with the evolution
of flight, but this too can be discounted. Feathers
of the modern type have been found on fossils of
non-flying dinosaurs, including the ancestors of
Tyrannosaurs rex. The significance of this will be
returned to towards the end of this chapter. There is
no doubt that feather types have evolved to make
flying more efficient, but their original function
must have been very different. Among modern
birds, feathers are essential in flight, for waterproofing, and insulation. They often have a role in communication, for courtship or competition, and in
predator avoidance through camouflage. In some
cases they even have a tactile function, an example
being the feather-derived bristles around the
mouths of some insectivores and some nocturnal
birds.
Flight path: evolution of birds from dinosaurs,
page 6.
2.1.1 Feather types
I am sure that you have in your mind a picture of
the typical feather (perhaps something like the quill
of the medieval scribe?). But if you took some time
to think about all of the feather types that you have
ever experienced, their variety might start to bewilder you; ranging as it does from the simple bristles
around the beak of some flycatchers, to the magnificently ornate tail plumes of male Indian Peafowl
Pavo cristatus, to the fluffy down that fills your
jacket and keeps you warm when birding in cold
weather. Thankfully for the purpose of this book we
can reduce this bewildering array to essentially two
basic types: contour feathers and downs.
Essential Ornithology. Second Edition. Graham Scott, Oxford University Press (2020). © Graham Scott (2020).
DOI: 10.1093/oso/9780198804741.003.0002
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ESSENTIAL ORNITHOLOGY
2.1.2 Contour feathers
The contour feathers are all of those feathers that
form the outline of the bird. They therefore include
the tail feathers (rectrices), the feathers of the wing
(remiges), those covering the body of the bird,
and the highly modified bristles that are often
found around the head of the bird and may bear a
superficial resemblance to mammalian hairs. The
arrangement and extent of these various feather
types is illustrated in Figure 2.1, and a range of
typical feather types and structures are illustrated
in Figure 2.2.
The typical contour feather has at its base a bare
quill, or calamus, this is the part of the feather that
sits inside the feather follicle and is attached to the
body of the bird. The calamus extends into the often
long and tapering central shaft of the feather that is
more properly termed the rachis. In the case of most
contour feathers (but not the bristles) the rachis
supports two vanes, the blades of the feather. The
vanes are actually composed of two opposite rows
of barbs, projections of the rachis which in their
turn support two parallel rows of smaller projections or barbules.
The barbules themselves are sculptured to allow
them to lock together like Velcro, giving the vane its
sheet-like quality, Specifically those barbules which
project from the barb and point forwards towards
the tip of the feather (distal barbules) have a comb
like arrangement of hooked barbicels which lock
into ridges on the adjacent backwards pointing
barbules (proximal barbules). Most feathers have a
basal area of the vane (i.e. the area closest to the
calamus) the barbs of which lack barbicels, resulting in a more open structure that can only really be
described as ‘fluffy’. A vane or vane area with this
open structure is properly referred to as being
plumulaceous, and the alternative locked sheet
structure is referred to as being a pennaceous vane.
The pennaceous vane structure is what gives feathers
their strength. Thus the outer plumage acts as a
light but relatively impenetrable armour against
wind, water, and abrasion; and, the overlapping
vanes of the open wing form the solid aerofoil
required for flight. The strength of the rachis of the
tail feathers of tree climbing species like the woodpeckers and treecreepers is such that they are able
to use their tails as a support when clinging to the
trunk of a tree.
One particular class of contour feather, the filoplumes, do have a somewhat atypical structure.
They have a rachis that is almost naked, having
only a small tuft of plumulaceous barbs at its tip.
These feathers protrude through the plumage and
are thought to be important in providing the bird
with sensory information (via motion sensing cells
at their base) concerning wind movements and
feather alignment.
2.1.3 Down feathers and semiplumes
Down feathers and semiplumes (which can be
classed as an intermediate between a contour
feather and a down feather) do have a calamus,
rachis, and vane anatomy similar to that of the contour feathers but their rachis is usually short and
the vanes are entirely plumulaceous. As a result
they often resemble more of a tuft than a typical
feather. These are the feathers that cover nestlings,
providing them with excellent insulation, and in
some situations with a degree of protection against
cannibalism. For example in some colonial situations
newly hatched (wet) gull chicks are often swallowed whole by neighbouring adults—but when
they have dried out, their stiff feathers make them
difficult to swallow and cannibalism rates decline.
In adult birds, down feathers and semiplumes are
usually found beneath the contour feathers where
they continue to perform an insulatory role and
in species of waterbirds they contribute towards
buoyancy. Interestingly, species that experience
environmental temperature fluctuations in their
annual cycle, such as the Redpoll Carduelis flammea
of the northern forests, often have a greater number
of down feathers immediately after completing
their moult in the autumn to provide extra insulation during the colder months. Presumably these
feathers are lost as a result of wear and tear, or are
shed to reduce insulation as the warmer spring and
summer proceed.
One particular class of down feather, the powderdown feathers, grow continuously but constantly
break at their tip resulting in the production of the
powder of feather wax particles that give them their
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Crest
General Topography
Blue Jay (Cyanocitta cristata)
Crown
Lore
Forehead
Upper Mandible
Supercilium
Auriculars
Primaries and Secondaries
are collectively called ‘Remiges’
Back
Secondaries
Primaries
Upper Tail
Coverts
23
Lower Mandible
Nape
Chin
Malar
Throat or Jugulum
Scapulars
Breast
Upper Wing Coverts
Side
Rectrices of the Tail
Flank
Undertail coverts
or Crissum
Alula
Belly
Crural feathers
Crest
Tarsus
Crown
Hallux
(hind toe)
Scapulars
Forehead
Lore
Nape
Rictal Bristles
Tertials
Back
Gape
Throat
Marginal
Coverts
Middle Secondary
Coverts
Alula
Rump
Scapulars
11
Gr. Secondary Coverts
Greater
Primary
Coverts
2
1
1
2
3
4
3
4
6
5
8
7
Upper Tail
Coverts
10
9
Secondaries
Note how the numbering of the
remiges proceeds from this point.
Rectrices
Primaries
5
6
7
10
9
8
Figure 2.1 The general topography of a bird. The species illustrated is the Blue Jay Cyanocitta cristata. From Proctor N.S. and Lynch, P.J. (1993)
Manual of Ornithology: Avian Structure and Function. Yale University Press, New Haven.
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ESSENTIAL ORNITHOLOGY
Pheasant contour
feather
Anterior vane
Aftershaft
Rachis (shaft)
Calamus (quill)
Rachis
Diagrammatic
view of Vane
Structure
Distal
barbule
Cortex
Barb
Proximal barbule
Posterior vane Longitudinal
groove Ventral ridge
Barbs
Vaned flight
feather (remex)
Superior umbilicus
Drawings are not to scale
Calamus (quill)
Inferior umbilicus
Down feather
Calamus (quill)
Figure 2.2 Feather structure. Adapted from Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology: Avian Structure and Function. Yale
University Press, New Haven.
name. It is presumed that this powder has a role in
the maintenance of feather waterproofing.
Flight path: Poorer quality juvenile feathers can be a
cost worth paying if predation risk is high, page 92.
2.2 Feather tracts
Based upon observations of a living bird about its
daily business it could be assumed that the body of
a bird is evenly covered with feathers. After all with
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(A)
25
(B)
Inter-ramal tract
Capital tracts
Malar tract
Spinal tract, cervical region
Submalar tract
Scapular apterium
Ventral cervical tract
Humeral tract
7
Primaries
5
31
1
3
5
Eutaxic wing
Secondaries
Spina tract, dorsal
7
9
Ventral sternal tract
Upper tail coverts
Spinal tract, pelvic
Uropygial gland
Upper tail coverts
Rectrices of the tail
Ventral abdominal tract
Anal circlet
Tail
6
1
3
Undertail coverts
Figure 2.3 The dorsal (A) and ventral (B) feather tracts of a typical passerine bird. Adapted from Proctor, N.S. and Lynch, P.J. (1993) Manual of
Ornithology. Yale University Press, New Haven.
the exception of the typically bare legs, and the
areas adjacent to the beak and eyes, no skin is usually visible. But it would be wrong to assume that
this superficial impression of feather-covered skin
equates to an even distribution of feathers across
the skin in the same way that hair follicles are
evenly distributed across a human scalp for example.
A similarly even distribution of feather follicles
does occur very rarely (examples include the penguins (Spheniscidae) and the Ostrich Struthio camelus) but in almost all birds, feather follicles are
restricted to well defined areas of skin—the feather
tracts or pterylae which are separated from one
another by areas of naked skin, the apteria.
Figure 2.3 illustrates the feather tracts of a generalized passerine, while those of a Greenfinch Cardeulis
chloris can be seen in Figure 2.4.
Along the feather tracts individual feathers grow
from specialized groups of skin cells arranged as a
feather follicle. These follicles begin as placodes,
thickenings of the epidermis and dermis (skin)
which develop to take on a typical ‘goose-bump’
morphology by a simultaneous evagination of the
skin around the feather germ (sometimes called a
Figure 2.4 This adult European Greenfinch Carduelis chloris is
moulting. Lines of new contour feathers just emerging from their
sheaths clearly show the position of the ventral sternal feather tract
(© Peter Dunn).
feather bud) and an upwards growth of the tubular
proto-feather as cells at its base proliferate. The dermal pulp in the centre of the feather bud provides
the nutrients required for feather growth and the
pigments that will give it its characteristic colour.
As the feather germ lengthens, layers of cells
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ESSENTIAL ORNITHOLOGY
forming the tubular feather differentiate, the outer
cells becoming the protective sheath of the growing
feather, while the inner cells establish the barb
ridges that will form the barbs of the developed
feather. Finally the feather bursts from the sheath
and unfurls into its final form. The particular properties of each feather type, the stiffness of a primary
flight feather or the softness of a down feather for
example, depend upon the different combinations
of proteins they are made from (predominantly
corneous beta-proteins together with keratins and
histadine-rich proteins). Genomic analysis has
revealed that in the domestic chick more than 130
genes are involved in the production of these proteins
and that the properties of different feathers are a result
of the activity of different genes. For example, whilst
the beta-proteins of the softer contour feathers are the
product of 13 FCbetaPs genes found on chromosome
25, those of the stiffer flight feathers are the product of
a different set of 13 FCbetaPs genes found on chromosome 2. These genes are active during initial feather
growth and then reactivated periodically to support
the growth of new feathers during the moult.
Key references
Alibardi, L. (2017) Review: cornification, morphogenesis
and evolution of feathers. Protoplasma 254, 1259–81.
Prum, R.O. (1999) Development and evolutionary
origin of feathers. Journal of Experimental Zoology
285, 291–306.
2.3 Feather colour
Birds have a reputation as being amongst the most
colourful of vertebrates and much of this reputation
they owe to the incredible range of colours of their
feathers. Some colours—white, greens, and blues
for example, are the result of the way that structural
features of the feather reflect light. For example the
interaction of reflective pigment granules, complex
layering patterns in the keratin of the feather, and
the angle of the observer relative to the bird are
responsible for the iridescence of hummingbirds
(Trochillidae) and starlings (Sturnidae). Recent fossil discoveries have demonstrated that this type of
structural iridescence was a feature of the feathers
of the four-winged Microraptor gui and other dinosaur ancestors of the modern birds.
Other colours—browns, blacks, yellows, and
reds for example, are the result of pigments that
are laid down within the growing feather. Black,
grey, and browns are the result of melanins (specifically eumelanin and pheomelanin); pigments
that are synthesized by birds as a result of the oxidation of the amino acid tyrosine. Darker feathers
have more melanin than lighter ones. Most white
birds have black, melanin-rich, wing tips, this is
because melanin pigments are associated with
the deposition of extra keratin which strengthens
the feathers. Without this additional strength the
wing tips would quickly abrade and flight efficiency would be compromised. Reds, red-browns,
and the green colour of Turacous (Musophagidae)
are derived from porphyrins (specifically turacoveradin (green), uroporphyrin (red), and coproporphyrin
III (red-brown)). Porphyrins too are synthesized by
birds. In this case they are a product of the breakdown of haemoglobin by the liver. Birds are unable
to synthesize the pigments that result in yellows
and bright reds (principally leutins and carotenoids),
instead they obtain them through their diet directly
from the environment. As we will see in chapter 5
yellows and reds often feature significantly in the
courtship plumage of birds, perhaps because they
are a signal of male quality.
Flight path: Feather colour, male quality, and sexual
selection, page 101.
2.4 Feather damage
Although the growing feather does have a blood
supply, and the feather itself can be moved by
muscles that attach to it below the skin, feathers
are inert/dead structures and they cannot be
repaired. Feathers may be damaged when birds
fight or during encounters with predators or prey,
and they abrade when they rub against one
another or against objects in the environment (try
pushing your hand through a briar or bramble
patch and imagine the abrasion that birds nesting
in there must suffer!). Figure 2.5 shows the
extreme wear on the tail feathers of Whitethroat
Sylvia communis, this bird was captured before it
underwent post-breeding moult and after a summer of skulking in thorny vegetation. Feathers are
degraded as a result of photochemical reactions
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F E AT H E R S A N D F L I G H T
Figure 2.5 The tail feathers of the Whitethroat Sylvia communis
exhibit extreme wear. (© Peter Dunn).
when the ultraviolet component of sunlight alters
the physical structure of the keratin that they are
composed of. They are also under attack by an
array of bacteria, fungi, and ectoparasites such as
mites and lice. There are however some situations
when feather wear can be an advantage, as shown
in Box 2.1.
In the face of such relentless pressure why aren’t
all birds as bald as the proverbial coot! Well of
course feathers are absolutely essential to bird survival and so birds engage in regular feather maintenance activities to minimize the impact of damage
and wear when it occurs. They also periodically
shed and replace all of their feathers in a process
known as moult.
Box 2.1 Taking advantage of feather wear
Although feather wear can generally be regarded as a bad
thing—necessitating as it does the periodic replacement of
feathers—there are birds of a range of species that turn
wear to their advantage.
When I catch male Common Redstarts Phoenicurus phoenicurus for ringing (banding) in the UK during their southwards
autumn migration I am always struck by how dull they are. An
adult male Redstart during the breeding season is a joy to
behold, it is an explosion of colour with its red tail, bright orange/
red breast, glossy black face and bib, and powder blue crown
and nape. But in autumn they look, well—dull. Muted versions
of their breeding colours are apparent but overlying them they
have a rather dull beige tinge that is often described by birders as
a frosting. Figure 2.6 shows this difference in plumage.
I confess that I did initially presume that this was a nonbreeding plumage that would be lost during a winter moult in
their sub-Saharan African winter grounds. But as I became more
(A)
27
experienced (and did some background reading rather than
guessing) I discovered that I was wrong. Adult birds of this species complete a full post-breeding moult in the UK before they
migrate and then return the following spring with the same
feathers intact. So how do they become brighter? Well if you
were able to examine closely the facial feathers of the autumn
bird you would see that they are indeed glossy black—but not
at their tips—here they each have a pale fringe (hence the
beige frosting). These fringes are less durable than the black
parts of the feather ‘behind’ them—possibly because they contain less of the pigment melanin—and they wear away over the
course of the winter. Because this wear takes place over all of
the body they do in effect become brighter as the breeding season arrives. So come spring they are in prime condition and,
without the need to undergo a time- and energy-consuming
moult, they are able to get on with the serious business of
impressing their mates (and bird watchers like me).
(B)
Figure 2.6 In spring male Common Redstarts Phoenicurus phoenicurus have a glossy black throat, grey crown, and rusty red breast (A;
© Ian Grier). This bird was trapped and ringed in Cyprus in spring when presumably it was migrating northwards into Europe. On the other
hand the male bird shown in B (© Peter Dunn) was trapped in the UK during its southwards autumn migration and exhibits the dull fringing
typical of freshly moulted birds.
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ESSENTIAL ORNITHOLOGY
2.5 Feather maintenance
The keratin that feathers are made from is one of
the strongest and most durable of biological substances. This is an advantage on one hand, having
resilient feathers is a good thing, but from another
perspective it can be a problem. When a feather is
wrongly aligned, as can happen very easily, it will
rub against those around it and might cause increased
abrasion. So, one of the most basic of feather maintenance activities undertaken by birds is regular
preening. During preening birds smooth their
feathers back into place by passing them through
their beak. This has the double effect of restoring
them to their correct position and ‘zipping’ back
together any barbicles and barbules that have
become detached (a process rather like smoothing
together the parts of a Velcro fastening). The effect
of preening is often enhanced because prior to
feather smoothing, birds rub onto their beaks the
secretions of their preen gland. The preen gland
(or uropygial gland) is situated low on the back
just above the base of the tail (see Figure 2.3A).
It produces an oily secretion that is used by
birds to maintain the physical quality of their
feathers and to regulate bacterial and fungal communities that grow on them. In the case of aquatic
birds the preen gland is particularly large and its
secretions are important in feather waterproofing. Figure 2.7 shows a roosting bird busily preening to dislodge and remove dirt particles and
ectoparasites, those such as the mites and lice
that feed directly on feathers, and also the ticks,
fleas, and Hippoboscid flies that feed on the birds
themselves.
Similarly, bathing in sand or water, scratching
(with bill or feet), and having a good shake out
can also be useful in feather realignment but are
probably most important in the physical removal
of parasites and foreign bodies. Sunning (when
birds prostrate themselves with their feathers outstretched or stand with their wings open in the full
sun) probably also aids in ectoparasite reduction.
However, the most intriguing of feather maintenance
behaviours are without doubt anting and smoking.
In the case of the latter I have often watched with
amusement as Jackdaws Corvus monedula stand
on the lip of a chimney pot and extend first one
wing and then another into the rising smoke from
the fire below. Presumably the smoke rids the bird
of parasites and perhaps an unpalatable smoky
residue coats the feathers deterring the activity of
feather-eating mites? During anting, birds position
themselves on top of a swarm and allow the insects
to crawl through their feathers and over their bodies, presumably the ants pick off parasites. In some
cases birds actively select particular ants and rub
them onto their feathers, it is assumed that in this
case the bird is taking advantage of chemicals produced by the ants that perhaps serve as a parasite
deterrent.
2.6 Moult
Figure 2.7 Roosting birds such as this Dunlin Calidris alpina spend
a considerable proportion of their time carefully preening their
feathers (© Ian Grier).
Moult occurs when a new feather begins to develop
in the follicle and simply pushes out the old feather
above it. The production of new feathers is expensive in terms of raw materials and the consequences
of a lack of resources during feather growth can
often be seen in the feathers of passerines that have
recently fledged and are still in juvenile plumage.
Close examination of the retrices or tail feathers of
such birds often reveals fault-bars, easily visible
lines running across the vanes of all of the feathers
and aligned across the width of the tail (see for
example Figure 2.8). These are structural weaknesses caused as a result of a period of resource
shortage (perhaps that section of the feather grew
on a particularly wet day when the parent bird was
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Figure 2.8 A series of faults are evident in the tail feathers of this
Chaffinch Fringilla coelebs. Because they line up across the tail we can
deduce that this is a juvenile bird, and all of these feathers were
grown at the same rate in the nest. However the faults are absent
from the three outer feathers on the right side of the tail, suggesting
that they have been replaced (© Peter Dunn).
unable to provide sufficient food to the growing
nestling). The width of the bars is a measure of the
duration of the resource shortage and they line up
because as a nestling all of the feathers of the tail
are grown at the same time. Possibly, because they
do grow their plumage in such a short time period,
the feathers of most juvenile birds are of poorer
quality than those of adults and so a post-juvenile
moult involving all or most of the plumage is common. This often involves a change in plumage colouration as birds progress from a more cryptic
appearance and/or one that may protect them
from the competitive attentions of their elders to
the patterns typical of adults of their species. Young
European Robins Erithacus rubecula do not gain the
red breast feathers characteristic of their species
until they have dispersed away from their natal territory. This is an advantage because adult Robins
are strongly motivated to attack anything that is
red in colour.
Fault bars are also occasionally evident in the tail
feathers of birds which have undergone a moult
into their adult plumage, but these bars will usually
only be seen in one or two feathers and they will not
line up across the width of the tail. This is because
an adult bird moults its tail feathers in sequence,
often (but not in all cases) from the centre outwards
in pairs. Adult birds almost certainly moult this
way to both spread the raw material costs of feather
29
Figure 2.9 An example of wing moult in the European Starling
Sturnus vulgaris. This bird was trapped for ringing in the late summer
and is moulting out of its brown juvenile plumage into its glossy adult
plumage. Using the numbering conventions explained in Figure 2.1,
the wing feathers are dropped and replaced sequentially starting with
primary 1 (in the centre of the wing). In this case three new (darker)
feathers are visible (primaries 1, 2, and 3, one feather (primary 4) is
missing and primaries 5–9 (older brown feathers) can clearly be seen.
The small, 10th primary is not visible. Secondary moult has not yet
started (© Graham Scott).
production and to maintain aerodynamic efficiency
(see Figure 2.9). So moult may also be costly because
it prevents or impairs normal feather function. A
bird with gaps in its tail and wing is less able to fly
efficiently and so may be less able to forage or to
avoid predators. This is possibly why moulting
birds tend to skulk and be less active, or undergo
migrations to specific moulting grounds.
Flight path: Flocking is an effective anti predator
strategy, page 137.
Extreme examples of this are the annual moults of
some species of ducks, swans, and geese many of
which form large, flightless flocks on or close to
their breeding grounds. These birds are flightless
for a period of some weeks between the end of the
breeding season and the onset of migration (often
adults resume flight to coincide with the onset of
flight in their attendant young). By flocking it is
likely that these birds reduce the predation risks
that they face. In the case of some species of sea
duck such as Steller’s Eider Polysticta stelleri,
post-breeding flocks are established in estuaries
and on the open sea often with hundreds of thousands of flightless birds congregating to complete
their moult. Some species have developed behaviour to minimize the impact of moult, see Box 2.2.
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ESSENTIAL ORNITHOLOGY
Box 2.2 Minimizing the impact of moult
2.6.1 Moult strategies
As has already been mentioned moult is essential to
birds, enabling as it does the replacement of worn
and damaged plumage. In some species however it
serves a further purpose in that it allows birds to
change their appearance to suit their needs at a
given stage of their life cycle. For example male
birds of a number of species (as diverse as ducks and
buntings) annually moult all or some of their feathers
to enable them to shift from a non-breeding/eclipse
plumage to a breeding/nuptial plumage and back
17.2
Standardized body mass (g)
The wing of a bird acts as an aerofoil providing both lift and
thrust during flight. To maintain flight efficiency it has been
assumed that birds optimize their body mass to wing area
ratio. A great number of experiments have been carried out to
demonstrate that birds can/cannot fly following wing manipulations such as the removal of feathers, feather cutting,
and even surgical separation of the propatagium (the flap of
skin along the bones of the wing to which the feathers are
attached). The results of such mutilations have shown for
example that pigeons are able to fly in a wind-free laboratory
environment with as little as 50 per cent of their wing area
intact. But such studies do not tell us much about the real
impact of natural wing area reductions, for example during
moult. It has been suggested that moulting birds would suffer reduced flight performance to the extent that they might
be less able to forage or to escape from predators. We might
therefore have expected natural selection to have resulted in
a solution to this problem. Joan Senar and colleagues have
carried out a remarkably elegant experiment to show just
how Great Tits Parus major maintain flight efficiency during a
simulated moult, and their experiment was all the more
remarkable because they carried it out in the field and
because they did not mutilate their birds in any way.
The researchers captured a sample of wild Great Tits and
divided them into two groups, A and B. Group A birds had
primary feathers 5, 6, and 7 (those in the middle of the outer
wing) taped together to simulate an 8 per cent reduction in
wing area (a reduction typical during the moult of this species). Group B birds were not taped. All of the birds were
weighed and then released. Two weeks later the birds were
recaptured and re-weighed. Group A birds then had their
tapes removed whilst group B birds were taped (primaries 5,
6, and 7 again), prior to release. After a further two weeks
control
17
control
16.8
16.6
16.4
taped
16.2
16
taped
Capture
20–21 August
Recapture
3–4 September
Recapture
10–12 September
Figure 2.10 Birds with experimentally reduced flight efficiency
compensate by adjusting their body mass. From Senar, J.C.,
Domènch, J., and Uribe, F. (2001) Great Tits (Parus major) reduce
body mass in response to wing area reduction: a field experiment.
Behavioural Ecology 13(6), 725–7. Reprinted by permission of
Oxford University Press.
the birds were captured for a third time. They were reweighed, all tapes were removed and they were all released.
Following the usual strategy for this species, as autumn
approaches group B birds increased in mass following
their initial capture, but the taped (group A) birds did not
(Figure 2.10). After the second capture, group A birds (no
longer taped) did increase their mass to that typical of
autumn birds, but look at what happened to the newly taped
group B birds. Their mass has fallen. These results are evidence
that birds strategically alter their body mass in response to a
change in wing area to maintain an optimum wing area to
mass ratio.
again; and montane/high latitude birds such as the
Ptarmigan Lagopus mutus moult into and out of a
whiter winter plumage for camouflage.
The particular moult strategy employed by any
given species is likely to have evolved as an adaptive response to a range of conflicting pressures such
as the availability of resources, the time available
before a necessary migration, the need to allocate
available resources to reproduction etc. Some species, particularly those at high latitudes, take advantage of a superabundance of resources and increased
day length to breed and moult simultaneously.
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F E AT H E R S A N D F L I G H T
For example, Ivory Gulls Pagophila eburna begin
their moult prior to egg laying and Alaskan populations of Glaucous Gulls Larus hyperboreus moult
whilst incubating. In the tropics lengthy periods of
parental care, perhaps a result of high competition
for patchily distributed resources, often result in the
onset of adult moult overlapping the end of the
breeding season. The moults of smaller birds tend
to be completed more quickly than those of larger
birds and in the cases of some large bird species,
one moult cycle may overlap with the next and so
moult will overlap with the whole of the annual
cycle (although it may only be active moult during
some periods of the year, being suspended at others).
Some species time their moult around migration,
see Box 2.3.
Box 2.3 Moult strategies of the old world warblers
Many of the species of old world warbler migrate annually
between northern European breeding grounds and African
wintering areas. The timing of the moult and particular
sequence and extent of feather replacement varies from species to species, but all of them have to fit the need to moult
around the need to migrate.
Among the Sylvia warblers those species that are relatively sedentary tend to spend longer on their post-breeding
moult than do those which undertake long migrations. So for
example non-migratory populations of the Blackcap Sylvia
atricapilla take around 80 days to complete the same moult
that birds of the migratory population of the United Kingdom
undertake in just half of that time. Most Sylvia warblers complete their moult on or close to their breeding grounds, but
those with longer migrations may start a moult pre-migration,
interrupt it, and then complete it at a suitable staging post
en route. The birds of those populations which do have a
particularly long migration, such as the Garden Warbler
Sylvia borin which breeds in northern and eastern Europe
and winters in Africa some 30ºS of the equator, delay their
moult until they reach their winter grounds. This is possibly
because the distances travelled are so great that Garden
Warblers arrive late and are forced to leave their breeding
grounds very early in the migration season and simply do not
have the time to complete a moult once they have finished
breeding. Once on their winter grounds, birds are probably
able to complete a moult at a more leisurely pace (not having to fit in a breeding event) and as a consequence are able
to begin the northwards return journey with a set of fresh
primaries. It has been suggested that this is in itself significant because the spring migration tends to be a bit of rush
to arrive in time to secure the best breeding territories and in
such a race primaries in good condition are likely to confer
an advantage.
A similar trend is observed in the moult/migration strategies
of the species of another genus of old world warbler, the
Phylloscopus warblers. The Chiffchaff Phylloscopus collybita
31
is a typical shorter distance migrant and one which undergoes a moult before it begins the autumn migration. The
closely related Greenish Warbler Phylloscopus trochiloides
however begins its moult before migrating, but completes it
once it has reached its winter territory. Notice here that I
referred to a winter territory rather than a winter area—this
was quite deliberate. Remember that the first birds to arrive
secure the best territories. Greenish Warbler establish and
defend a winter territory and so presumably are in just as
much of a hurry in the autumn as they and the other species I have mentioned are in the spring. Finally another
Phylloscopus, the Willow Warbler Phylloscopus trochilus
moults not once but twice each year. Willow warblers
undergo a rapid and complete moult prior to both the
autumn and spring migration. Members of this species
undergo particularly long migrations, breeding further north
and wintering further south than Chiffchaff for example. It is
likely that they moult twice because their flight feathers are
simply not sufficiently robust to make the trip twice.
In order to understand the impact of migration upon the
moult strategies of the old world warblers and other old
world species Yosef Kiat and Nir Sapir have collected a data
set involving the measurement of individuals of 134 passerine bird species resident in, or migrating through Israel.
Some of these species have relatively short migratory movements whilst others are long distance migrants. Furthermore
the adult birds who typically undertake a complete annual
post-breeding pre-migration moult have a slightly different
strategy to juveniles who undertake a partial post-fledging
moult that typically involves the replacement of body but
not flight feathers and complete their moult in their winter
quarters. Their idea was that birds of both age classes
should be expected to vary the timing and/or extent of their
moult in a way that was related to the length of their migratory journey and hence to the time available to them to fit a
continued
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ESSENTIAL ORNITHOLOGY
Box 2.3 Continued
moult into their annual cycle. Their results (Figure 2.11) confirmed that adults of species with shorter migratory journeys took longer over their moult than those with longer
journeys. Similarly they found that juveniles with shorter
journeys were likely to moult more of their body feathers
prior to migration than birds with longer journeys (who
complete their moult in their winter quarters). Juveniles
moulting more feathers extended their moult over a longer
period than those moulting fewer. The results of studies like
(A)
this are important because they help us to understand the
age-specific responses of species to pressures that vary
across an annual cycle.
References
Shirihai, H., Gargallo, G., and Helbig, A.J. (2001) Sylvia
Warblers. Helm, London.
Ginn, H.B. and Melville, D.S. (1983) Moult in Birds. The
British Trust for Ornithology, Tring.
(B)
1.0
160
0.8
Post-juvenile moult extent (proportion)
Post-breeding moult duration (days)
140
120
100
80
60
0.6
0.4
0.2
40
0.0
0–2500
2500–5000
>5000
Migration distance (km)
0–2500
2500–5000
>5000
Migration distance (km)
Figure 2.11 Adult birds migrating less far take longer over their post-breeding moult (A), and juvenile birds moult less of their feathers
before migration when they have longer migrations to undertake (B). Adapted from Kiat, Y. and Sapir, N. (2017) Age-dependent modulation
of songbird summer feather moult by temporal and functional constraints. The American Naturalist 189(2), 184–95.
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2.7 Flight
I am confident that there is not a single reader of
this book who, when watching birds fly, has not
asked the question ‘how do they do that?’ To remain
airborne and fly a bird relies upon two forces: lift
and thrust, which must be sufficient to counteract
two opposing forces: gravity and drag. Figure 2.13A
illustrates the opposing directions of these forces in
a hypothetical situation. Gravity acts upon the mass
of a bird pulling it downwards towards the earth.
To remain aloft therefore, it must generate sufficient
lift. Drag forces (the friction forces which result as
the bird moves through the air) will push it backwards. To counter this a bird must produce sufficient thrust either directly through powered flight
or more subtly by the manipulation of the lift/drag
relationship. Swifts Apus apus spend almost their
entire life on the wing, coming to earth only to breed.
They even sleep on the wing, climbing to high altitudes and flap-gliding through the night. As aerial
hunters of insects, speed and agility in the air are
essential to them and I have to admit that watching
screaming parties of young swifts gathering prior to
their autumn migration is one of the thrills of my
birding year. During these bouts of aerobatics, and
when watching hunting swifts, I am amazed by their
ability to gather speed and to perform seemingly
impossible direction changes without flapping their
(A) Dynamic soaring wing
(B) Elliptical wing
33
wings. They make these manoeuvres by altering
their wing shape, that is to say by morphing them.
Lentik and co-workers have carried out wind tunnel
experiments on the paired wings of dead swifts (the
birds died during rehabilitation and were not sacrificed for the experiments). They morphed the wings
into a variety of shapes based upon observations of
flying birds and found that fully extended wings
(long and thin and at 90° to the body) generate maximal lift, but are suited to lower speeds and slow,
shallow turns. Wings swept back (to 45º relative to
the body) generate less lift, but minimize drag and so
increase glide speed and enable a bird to turn sharply
at speed. So by morphing between these wing shapes
(and using intermediates between them) swifts
are able to control their glide. Key adaptations for
powered flight are set out in Box 2.4.
Key reference
Lentik, D., Müller, U.K., Stamhuis, E.J., et al. (2007)
How swifts control their glide performance with
morphing wings. Nature 446, 1082–5.
Videler, J. (2005) Avian Flight. Oxford University Press,
Oxford.
So wings, and specifically the morphology of wings,
are the key to flight characteristics and to achieve
the various modes of flight that I am about to discuss there are four basic wing types (see Figure 2.12).
(C) High aspect ratio wing
(D) High lift ratio wing
Figure 2.12 Dynamic soaring wings (A) are long and narrow enabling birds such as Albatrosses, Petrels, and Shearwaters to glide at speed.
Elliptical wings (B) are broad and rounded; they are typical of birds requiring short bursts of speed and high manoeuvrability such as woodland
species and birds that are the prey of other birds. High aspect ratio wings (C) provide for speed and agility and are commonly found in aerial
hunters such as swallows and hawks. High lift ratio wings (D) are broad and fingered, they enable birds such as Storks and Vultures to soar but
have limited manoeuvrability. From Pough, G.H., Janis, C.M., and Heiser, J.B. (2002) Vertebrate Life. 6th edn Prentice Hall, New Jersey.
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ESSENTIAL ORNITHOLOGY
Box 2.4 Adaptations for flight
Birds have a number of key adaptations which enable
them to undertake powered flight efficiently. They will be
discussed in more detail throughout this book but the
main ones are summarized here:
1. Wings, fore limbs that are modified as aerofoils.
2. A skeleton that is strong and rigid, but that is very
light. This is achieved because bird bones are less solid
than those of mammals or reptiles. They are filled with
a honeycomb of air spaces and strengthened by internal
struts.
3. The coracoid bone, which acts as a support for the
shoulder.
4. An enlarged sternum with a deep keel for the attachment of the large muscles associated with powered
flight.
5. Large and powerful flight muscles. The pectoralis and
supracoracoideus provide the power for flight.
6. A highly efficient respiratory system.
7. Considerable modification of the bones of the forelimb. Fused hand bones, in some cases locking joints
and in others wrist joints that rotate almost fully.
8. The furcula or wishbone, which acts as a spring during
the wing-beat cycle.
I am not a physicist and do not propose to discuss
in detail the aerodynamics of bird wings or the
aerodynamic theory of bird flight, but for those
readers who do want to explore these areas I can
recommend Avian Flight, the excellent monograph
by John Videler, upon which the following sections
of this chapter draw heavily.
As a wing pushes through the air it produces an
area of high pressure in front of it. As the air ‘splits’
and moves quickly backwards across the upper and
less quickly across the lower surface of the open wing
before being deflected downwards behind it, further
pressure differentials develop. The net effect is that
air moves from the lower pressure areas towards the
higher pressure areas and the forces of lift and thrust
result. The balance of these two forces depends upon
the angle of the wing relative to the oncoming air
stream (Figure 2.13A). When, as in Figure 2.13B this
angle of attack (as it is termed) is low, little thrust is
generated but lift is produced. If the leading edge of
the wing is tilted forwards (Figure 2.13C and 2.13D)
both lift and thrust are generated and there is a net
movement of the bird forwards. Tilting the wing
upwards will of course increase drag and slow the
bird. Note that lift is generally produced by the inner
wing, as air moves over the surfaces of the secondaries, whereas thrust is produced by the primaries
of the outer wing (Figure 2.13E). The primaries are
asymmetrical and each of them acts as an aerofoil in
its own right—generating lift additional to that
produced by the wing itself. As the wing beats, the
primaries twist such that on the down stroke they
close to form a solid wing, but on the up stroke they
open, reducing wind resistance.
2.7.1 Gliding and soaring
Under the right conditions birds are able to utilize
the forces of lift and thrust generated by outstretched wings to travel considerable distances
with minimal energy expenditure. They achieve
this by gliding or soaring rather than by using energetically expensive flapping flight. Vultures, Storks
and other large birds are well known for their ability to achieve altitude by hitching a ride on a rising
column of heated air. From the tops of these thermals they are able to soar for long periods to find
food or to undertake stages of a migratory flight. By
soaring from the top of one thermal to the bottom of
another repeatedly they can travel considerable distances without the need to flap their wings. The
most accomplished of the gliders are probably the
Albatrosses and Giant Petrels of the southern
oceans. With their very long, slender wings they too
are able to travel large distances, and at considerable
speed, with almost no need to flap. To further
increase energy conservation they possess a modified wing joint morphology that allows them to lock
in position their fully stretched wings. Without this,
other species exert muscle energy to achieve the
same end. Unlike vultures, who use thermals to
achieve lift, these seabirds ride the pressure differentials that result when winds close to the ocean
surface move at a slower speed (due to friction)
than do the winds above them. This is termed
dynamic soaring and relies upon there being a constant wind, a perfect strategy then for the seabirds
of the roaring forties. Recent research involving the
monitoring of the fine scale flying behaviour of
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35
Total lift
(A)
Thrust
Total drag
M
R
Most of lift
(C)
(B)
Rest of lift
Thrust
Drag
Flow of
air across
inner wing
R
air
of p
w
o ti
Fl ing
W
Drag
ac
s
s
ro
M
(E)
(D)
Movement of bird
Movement
of wing-tip
relative
to bird
Act
ual
m
of
ent
m
e
ov
e to
tiv
ela
r
p
g ti
win
air
Vertical movement
Inner wing
Outer wings
(Primary feathers)
Inner wings
(Secondary feathers)
Vertical movement
wing tip
Figure 2.13 The forces acting upon, and generated by, a generalized flying bird. From Pough, G.H., Janis, C.M., and Heiser, J.B. (2002)
Vertebrate Life. 6th edn Prentice Hall, New Jersey.
Manx Shearwaters Puffinus puffinus with GPS trackers
has revealed that birds adjust their flapping/soaring
behaviour to maximize their efficiency as the wind
changes. Rory Gibb and his colleagues found that
tracked birds were more likely to soar in tailwinds
and crosswinds above 8 m per second, but at lower
speeds they were more likely to flap.
Key reference
Gibb, R., Shoji, A., Fayet, A.L., et al. (2017) Remotely
sensed wind speed predicts soaring behaviour in a
wide-ranging pelagic seabird. Journal of the Royal Society Interface 14, 20170262.
Smaller birds generally lack the wing area to adopt
gliding as a main mode of flight. But they are able to
reduce energy expenditure to some degree by punctuating their flapping flight with short glides or
bounds. Typically their flight path is sinusoidal,
gaining height during a burst of flapping and then
falling towards the end of the short glide. But the
savings gained by milliseconds of gliding are considerable. As an example, in a study of the bounding flight of the Zebra Finch Taeniopygia guttata
(Figure 2.14) Tobalske and co-workers have shown
that birds were able to reduce their flapping (and
presumably therefore their energy expenditure)
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ESSENTIAL ORNITHOLOGY
Altitude (mm)
Wingtip
excursion (mm)
36
40
0
–40
40
Flapping
20
Bounding
0
–20
0
50
100
150
200
Time (ms)
250
300
350
Figure 2.14 The flapping and bounding flight of the Zebra Finch. By flapping, the bird achieves height (altitude) and momentum so that during
a non-flapping bound it can conserve energy. Wing tip excursion is a descriptive for flapping activity. Adapted with permission from Tobalske, B.W.,
Peacock, W.L., and Dial, K.P. (1999) Kinematics of flapping flight in the zebra finch over a wide range of speeds. Journal of Experimental Biology
202(13), 1725–39.
by between 22 per cent and 45 per cent depending
upon their speed of travel.
2.7.2 Flapping flight
The power for flight comes from the flapping of the
wings. During a single beat cycle of the wing, in
some cases a period of just milliseconds, the wing
form and therefore its aerodynamic properties
changes a number of times. The inner wing (the secondaries) simply moves up and down during the
cycle and as it does so it acts in the same way as a
fixed wing during gliding in that it generates most
of the lift experienced by the bird. As was mentioned previously, the primary feathers twist during the beat, ‘closing’ the wing surface on the
down stroke and opening it to reduce wind resistance at it moves upwards. At the same time the
wrist joint (between the inner wing and the outer
wing) twists so that on the down stroke the wing
moves both down and forwards and on the up
stroke moves up and backwards. So the outer
wing is moving through the air in a sort of figure
of eight motion. As it moves forward and downward on the down stroke the angle of attack of the
wing is high and the lift generated has a forwards
direction—thrust.
To hover, to fly at a fixed point, birds have to
generate lift sufficient to support their weight but
generate no forwards thrust (or at least no more
thrust that is required to counter the drag that they
are experiencing). For the vast majority this is very
difficult and cannot be sustained for anything more
than short periods prior to landing, or striking at
food. But there is one group, the Hummingbirds
that have perfected hovering to the point that they
are able to hold their position in mid air for prolonged periods. They can also fly forwards, backwards, and even sideways. This is possible because
the wing of a Hummingbird has an anatomy unlike
that of any other bird (except their close relatives
the Swifts). The Hummingbird inner wing is relatively very short and is held in a fixed ‘v’ position
close to the body. The outer wing (with 10 long primaries) forms the main surface and accounts for more
than 80 per cent of the total wing (compared to c. 40
per cent in the Buzzard Buteo buteo for example).
The Hummingbird main flight muscles are far
larger (relative to body mass) than those of other
flying birds. The wrist joint is particularly flexible
enabling the outer wing to twist almost upside down
on the back stroke. When hovering, hummingbirds
generate lift and thrust on both the forward and
back stroke, both of which sweep so far that the
wing tips are brought close together. Their wing
beat, describing a figure of eight in the air that is
almost horizontal to the ground, is remarkably fast.
Speeds of as much as 200 beats per second have been
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37
x-rayed it 200 times per second while it flew! From
the figure we can see that the humerus is almost
parallel with the body at the start of the sequence
but that it moves upwards and rotates forwards as
the supracoracoideus contracts on the up stroke
(Figure 2.16B). The bones of the hand at this point
are held at approximately 90° to the body. They
remain there as the wing closes (Figure 2.16C) and
are swept backwards and down as the contraction
of the pectoralis causes the down stroke. This
research has also revealed the role of the furcula, or
wishbone, during flight. As the humerus rotates
forwards and moves downwards the heads of the
furcula move apart. As they bend, the arms of the
furcula act as a spring and store some of the force of
the down stroke. They then release the stored
energy as the furcula returns to its resting position
during the up stroke. The exact function of this process is not yet understood. The release of energy
may assist the supracoracoideus in raising the wing,
but it seems most likely that it has a respiratory
function because a relationship between the wing
beat cycle, the action of the furcula, and the compression of the air sacs has been identified.
recorded from the Ruby-throated Hummingbird
Archilochus colubris during courtship hovering,
although speeds between 10 and 80 beats per second might be more typical of the family.
So, we can see the path of the wing during flight
and infer from that the movement of joints, etc. But
what is going on inside the bird? Figure 2.15 illustrates schematically the main anatomical components of the wing. There are actually 45 different
muscles in the bird wing, but only the two thought
to be most significant (and currently best understood) are shown. These are the pectoralis and the
supracoracoideus, the two relatively large muscles
which attach to the deep keel (corina) of the sternum
and between them provide the power responsible
for the wing strokes of flapping flight. Contraction
of the pectoralis pulls the wing down and forwards
during the down stroke of flight. The supracoracoideus pulls it upwards and backwards during the
up stroke.
The effect of these muscular contractions upon
the bones of the wing can be seen in Figure 2.16
which was obtained by Farish Jenkins and colleagues when they trained a European Starling
Sturnus vulgaris to fly in a wind tunnel whilst being
filmed using radiographic film. Essentially they
Flight path: Energy, flight, and migration. page 59.
Carpometacarpus
Wrist joint
Alular digit
Major digit
Radiale
Shoulder joint
with trioseal canal
Vertebra
Ulnare
Propatagium
Scapula
Radius
Minor digit
Ulna
Humerus
Furcula
Rib cage
Elbow joint
Metapatagium
Coracoid
Tendon
Sternum
M. Supracoracoideus
(black)
Carina
M. Pectoralis
(grey)
Figure 2.15 An overview of the anatomy of the avian wing and rib cage. From Videler, J.J. (2005) Avian Flight. Oxford University Press, Oxford.
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ESSENTIAL ORNITHOLOGY
(A)
(B)
(C)
(D)
Figure 2.16 Skeletal movements of the European
Starling Sturnus vulgaris during flapping flight. From
Jenkins, F.A. Jr, Dial., K.P., and Goslow, G.E. Jr (1988)
A cineradiographic analysis of bird flight: The wishbone in
starlings is a spring. Science 241, 1495–8 , reprinted with
permission from AAAS.
2.7.3 Respiration and flight energetics
The lipids (fats), carbohydrates, and proteins of the
body provide the energy for metabolic activity,
including flight. The ‘burning’ of these compounds
in the presence of respiratory oxygen provides the
energy required for the splitting of cellular molecules
of ATP (adenosine triphosphate), which in turn
provide the energy needed to control the contraction of muscle fibres. Oxygen and fuel from feeding
(which will be discussed in chapter 6) are therefore
essential for flight. Terrestrial vertebrates obtain
oxygen when air is inhaled and the oxygen in it is
transferred across the walls of the lung to the blood
stream. Birds have a higher metabolic rate than
other terrestrial vertebrates, they have higher body
temperatures and faster heart rates, and they use
more oxygen in flight than mammals do when running. We might therefore expect the lungs of birds
to be particularly large, but in fact they are smaller
than those of similarly sized mammals. This is
probably a necessary adaptation to keep down
body mass for efficient flight. So how do birds get
the oxygen that they need? Well their lungs may be
small—but size for size they have a larger internal
surface area for oxygen transport. In mammalian
lungs inhaled air passes along bronchioles (tubes) to
alveoli (dead-end sacks) where oxygen is absorbed.
Exhaled air reverses back along these tubes in what
is called a tidal fashion. The lungs of birds are very
different. They lack the alveoli and instead the bird
lung is composed of a network of very thin tubes
termed parabronchi (the bird lung is often therefore
referred to as a parabronchial lung), each of which
divides into very many thinner capillaries where
gaseous exchange takes place. Inhaled and exhaled
air pass through the lung in the same direction (i.e.
a non-tidal flow) and in fact a complete cycle of respiration involves not one but two breaths. This is
possible because the lungs of birds are connected
to a network of air sacks within the body cavity
(Figure 2.17A).
During the first breath, inhaled air passes into
and through the lung and into the abdominal air
sac. Contraction of the abdomen during exhalation
forces air back out of the abdominal air sacks, back
through the parabronchi of the lung and gas
exchange takes place (Figure 2.17B). During the second breath, the ‘stale’ air in the parabronchial lung
is forced into the anterior air sacks on inhalation
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(A) 1
2
2a
3
7
5
2b
6
4
(B) Inhalation
Exhalation
5
1
2
4
3
Figure 2.17 Gaseous exchange in the respiring bird. Figure (A) illustrates the parabronchial lung (7) and air sack (1–6) system of a generalized
bird. Air sacks labelled include: 1, the infraorbital sinus; 2, the clavicular air sack; 3, the cervical air sack; 4, the cranial thoracic air sack; 5, the
caudal thoracic air sack; and, 6, the abdominal air sacks. Figure (B) illustrates the pattern of air-flow through the system during both inhalation
and exhalation. From Pough, G.H., Janis, C.M., and Heiser, J.B. (2002) Vertebrate Life. 6th edn Prentice Hall, New Jersey.
and out of them, and out of the bird, during exhalation
(Figure 2.17B). So in a bird oxygen uptake is happening on both inhalation and exhalation and bird
lungs are far more efficient at oxygen uptake than
those of similar sized mammals. After uptake, oxygen is transported through the bloodstream to the
tissues of the body by the carrier molecule haemoglobin. Avian haemoglobin has a lower affinity for
oxygen than that of mammals, but for birds with a
higher metabolic rate this is actually advantageous
because it results in a higher oxygen unloading rate
at the flight muscles and other tissues. Furthermore,
oxygen uptake by the flight muscles is very efficient
because volume for volume they have more blood
capillaries than comparative mammalian muscle,
their muscle fibres are shorter, and the mitochondria in those fibres are both more numerous per
unit area and closer to the cell surface. These adaptations combine to provide birds with the efficient
and effective respiration system that is essential for
flight.
2.7.4 Flying high
Although a relatively lower haemoglobin-oxygen
affinity is advantageous for most birds there are
situations when it could be something of a problem.
As we have discussed lower affinity can be an
advantage because it allows more efficient unloading for cellular respiration, but this is only the case
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ESSENTIAL ORNITHOLOGY
because the system is optimal at the partial pressure
of atmospheric oxygen close to the surface of the
earth. As altitude increases the partial pressure of
atmospheric oxygen decreases and under these
conditions haemoglobin with a low affinity for oxygen would be less efficient and respiration could
be compromised. So what is the solution? Joana
Projecto-Garcia and colleagues have compared the
haemoglobin function of a number of species of
Andean hummingbird, some of which like the
Great-billed Hermit Phaethornis malaris live at lower
altitudes and others like the Andean Hillstar
Oreotrochilus estrella live at altitudes up to 5,000 m
above sea level. They found a positive relationship
between altitude and haemoglobin oxygen affinity.
Furthermore, by comparing the haemoglobin of
Box 2.5 Formation flying saves energy
My home is right under the flight path that Pink-footed
Geese Anser brachyrhynchus follow as they migrate into the
UK in the autumn. It’s a joy to hear them calling and to see
their long, drawn out V-formations as they pass overhead.
Even non-birders notice them and I am usually asked why do
they fly in a V? Quite simply I say large birds fly in a V to
conserve energy. I am sure that you have been told the same
thing many times, but I guess it might surprise you to know
that hard data to support this explanation are actually quite
rare. Good data have however been recently provided by
Henri Weimerskirch and co-workers. They have made
detailed observations of the heart rates and wing beat rates
of free flying Great White Pelicans Pelecanus onocrolatus
singly and in flocks. They trained eight birds to fly behind a
moving motorboat and filmed them doing so. The birds had
been fitted with heart rate monitors and from the data from
these (Figure 2.18), and the films that they made, it was possible for the team to compare the individual heart rates and
wing-beat rates of all of the birds. These measures are presumed to correlate closely with energy expenditure during
flight.
Gliding lone pelicans and birds flying 50 m and 1 m above
the water flapped more often and had higher heart rates
than did birds flying in formation at 1 m (Figure 2.19). Birds
Figure 2.18 Flying in formation increases the individual flight efficiency of these migrating Pink-footed Goose Anser brachyrhynchus
(© Will Scott).
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Mean
wingheat frequency
Mean
(b.p.m)
heart rate (b.p.m)
F E AT H E R S A N D F L I G H T
41
at the front of the V have a wing-beat frequency similar
to that of single birds at the same height, but those
behind the leader clearly benefit. Although from the figure you should note that the benefits diminish slightly
the further from second place a bird flies. The researchers
also noticed that birds at the rear of the formation constantly adjusted their position relative to the group, presumably they were maximizing the energy savings that
they made.
105
90
75
60
45
12
0
200
190
180
170
160
150
1
Gliding Alone at Alone at
50 m
1m
2
3 4 5 Last
In
formation
closely related groups of high, mid, and low altitude hummingbirds they found that the same two
amino-acid replacements in the haemoglobin molecule explained the differences in haemoglobin
activity across several species groups suggesting
that the same adaptations had evolved several
times, an example of parallel evolution.
Key reference
Projecto-Garcia J., Natarajan, C., Moriyama, H., et al.
(2013) Repeated elevational transitions in haemoglobin
function during the evolution of Andean hummingbirds. Proceedings of the National Academy of Science
110(51), 20669–74.
2.7.5 Flight speeds
Some birds alter their flight speeds relative to
flock-mates to conserve energy (see Box 2.5) and
earlier in this chapter I described the way in which
a swift can adjust its flight speed by altering the
shape of its wings during a glide. But not all birds
are as accomplished at gliding as swifts and in
many cases to fly faster a bird must flap harder
Figure 2.19 Variation in heart beat rate (a measure of
energy expenditure) of gliding, solitary and formation flying
pelicans. Reprinted by permission from Weimerskirch, H.,
Martin, J., Clerquin, Y., et al. (2001) Energy saving in flight
formation. Nature 413, 697–8.
and therefore use more energy. This probably isn’t
a surprise to you. The relationship between power
(flapping) and speed seems to be a straightforward one. It is not however. Whilst it is true that
flying fast is energetically expensive, so is flying
slowly (remember that hovering is very expensive). Aerodynamic theory suggests that the
power curve (the relationship between power and
velocity) of flight should be U shaped. By flying
Magpie Pica pica, Barbary Dove Streptopelia risoria,
and Cockatiel Nymphicus hollandicus in wind
tunnels and directly measuring pectoralis muscle
activity, Tobalske, Dial, and colleagues have shown
that in the case of these species the power curves
which result are broadly U shaped (Figure 2.20).
Obviously there are times when a bird will have to
fly fast (to catch mobile prey or to escape a predator
for example), or perhaps fly slowly (to locate cryptic food or perhaps as part of a display, although in
such cases the function of the display may of
course be to advertise that you have energy to
spare) but based upon these observations we might
expect birds to select flying speeds that conserve
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ESSENTIAL ORNITHOLOGY
Pectoralis mass-specific
power (W kg–1)
250
200
Dove
150
Cockatiel
100
50
Magpie
0
0
5
10
Velocity (m s–1)
15
Figure 2.20 U-shaped power curves of three species of flying bird. Note that in all
cases slower and faster flight speeds incur a higher energy cost (i.e. more muscle
power is required). Reprinted by permission from Tobalske, B.W., Hedrick, T.L. Dial,
K.P., and Biewener, A.A. (2003) Comparative power curves in bird flight. Nature 421,
363–6; and Dial, K.P., Biewener, A.A., Tobalske, B.W., and Warrick, D.R. (1997)
Mechanical power output of bird flight. Nature 390, 67–70.
energy whenever practicable, to adopt optimal flying
speeds. In fact it has proven very difficult to demonstrate that birds fly at an optimal speed in real
life, perhaps because birds incorporate more information (about their momentum, their motivation, the
weather etc.) into their decision-making than we
have taken into account when making our prediction.
The ability of birds to assimilate external information has an impact upon collision avoidance during
flight, see Box 2.6.
Flight path: Flight can have a display or information
exchange function during foraging, territoriality or
courtship. page 101 and 123.
Box 2.6 Collision avoidance
How do birds avoid collisions?
I am always amazed at the ability of a hunting Sparrowhawk
Accipiter nisus to dart in and out of a hedgerow chasing its
passerine prey, or of a feeding hummingbird to flit from
flowerhead to flowerhead as little more than a blur—at
such speeds how on earth do birds avoid collisions with one
another and with objects in their environment?
We know that insects use the motion of images across the
eye (something called pattern velocity) to provide information
about their own movement relative to their surroundings.
Experiments involving honey bees have demonstrated that
pattern velocity is used to maintain course, to control speed
and altitude, and to gauge distance travelled. From these
experiments we also know that bees are particularly attuned
to react to nasal-to-temporal pattern velocity; more simply
they modify their flight behaviour by monitoring the speed at
which objects appear to pass them laterally as they fly
through the environment. This is something that you will be
familiar with if you drive; you will notice that a sign that
seems to take an age to reach as you look forwards seems to
whizz by if you try to read it as it passes. By assessing changes
in the apparent speeds of several signs you would be able to
determine your rate of acceleration or deceleration and perhaps adjust your speed accordingly.
Roslyn Dakin and her colleagues have carried out some
elegant experiments involving trained hummingbirds to
test the hypothesis that birds utilize fore-aft pattern velocity
during flight to avoid collisions. They trained Anna’s
Hummingbirds Calypte anna to fly along a tube to a food
source. During the flights they projected moving and/or
static patterns onto the walls of the tube and monitored
the behaviour of the flying bird. In one experiment for
example they projected patterns of vertical bars onto the
walls of the tube, one side they kept static and the other
they moved forwards or backwards away from the feeder.
Bees under a similar treatment would be expected to follow a curved flight path, but the hummingbirds were able
to maintain their direction of flight straight down the middle of the tube—this demonstrates that birds, unlike bees,
do not steer by balancing nasal-to-temporal pattern
velocity. Further experiments revealed that in fact hummingbirds pay more heed to pattern velocity in the vertical
axis—to the changing apparent height of objects as they
move towards them. It is possible that this allows birds to
use apparent expansion in the size of the objects they
approach to judge speed and distance and to react
accordingly (imagine running towards two identical horizontal beams, one a few metres ahead of you and one
further away—the close one would appear to grow at a
faster rate). So rather than relying upon pattern velocity to
avoid collisions, birds utilize information about objects in
their environment.
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Optic Tectum
OPT
LM
The eye
nBOR
Tectofugal
Pathway
nRt
WULST
Thalamofugal
Pathway
Accessory
Optic System
Figure 2.21 Key neuronal elements of the avian visual system including the tectofugal pathway (brightness, colour, pattern, and simple
motion); the thalamofugal pathway (spatial orientation, motion perception, and binocular vision; and the accessory optic system (ability to
follow an object whilst keeping the head stationary). Abbreviations are explained in the main text. Adapted from Wylie, D.R., GutiérrezIbàñez, C., and Iwaniuk, A.N. (2015) Integrating brain, behaviour and phylogeny to understand the evolution of sensory systems in birds.
Frontiers in Neuroscience 9(281).
Through experiments with pigeons, the neurons that process information about object expansion have been identified within the nucleus rotundus, an area of the thalamus
which is known to be part of the tectofugal pathway, one of
three main neuronal pathways comprising the visual system
of birds (Figure 2.21). The tectofugal pathway is the major
visual pathway in birds, accounting for 90 per cent of retinal
projections (the neuronal processes emanating from the retina), and it is involved in the assessment of brightness, recognition of colour, pattern discrimination, and both simple
and complex motion. The thalamofugal pathway (comprising
the principal optic nuclei of the thalamus and the wulst) is
thought to be involved in spatial orientation, motion perception, and binocular vision. The Accessory Optic System (AOS)
comprising the LM (or nucleus lentiformis mesencephalic)
and the nBOR (nucleus of the basal optic route) is involved
in the processing of the optic-flow information generated by
self-motion. Integration of all of these pathways (and others)
is essential for flight. The LM of the AOS is known to be
important in the optokinetic response (OKR), the ability of an
organism to follow the movement of an object with the eyes
whilst keeping the head stationary. The OKR is essential to a
hovering animal like a hummingbird and so we might expect
them to have a particularly well developed LM, and
compared with other birds they do (Figure 2.22).
Collisions do happen
But in spite of the adaptations enabling birds to avoid high
speed aerial collisions, they do happen and often with
catastrophic effects. It has been estimated that each year
hundreds of millions of birds die as a result of collisions with
man-made static objects: fences, buildings, power-lines,
wind turbines etc. Some of these we can perhaps understand—when a bird hits your window you assume that it
simply didn’t see the glass. But how is it that birds don’t see
Hummingbirds
Kestrel
Spinebill
Kingfisher
Grouse
Hawk
Nightjar
Owls
Swifts
Pigeon
Songbirds
Coot
Shorebird
Egret
Duck
Frogmouth
Cockatiel
0.0
0.1
0.2
LM % Brain
0.3
Figure 2.22 The LM (nucleus lentiformis mesencephalic) of the
brain, which is involved in the ability of an organism to follow the
movement of an object with their eyes while the head remains
stationary, is more developed (expressed as percentage of volume)
in hovering birds such as hummingbirds, kestrels, and kingfishers.
Adapted from Wylie, D.R., Gutiérrez-Ibàñez, C., and Iwaniuk,
A.N. (2015) Integrating brain, behaviour and phylogeny to
understand the evolution of sensory systems in birds. Frontiers in
Neuroscience 9(281).
a pylon or wind turbine projecting tens of metres above the
surrounding vegetation? Collisions with such static objects
have been estimated to be the most significant non-natural
cause of mortality amongst large soaring birds like Eagles,
Vultures, Cranes, and Storks and as a result collision mitigation is a pressing conservation issue. In his excellent book
The Sensory Ecology of Birds, Graham Martin proposes a
possible explanation. Considering the plight and flight of the
continued
43
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ESSENTIAL ORNITHOLOGY
Box 2.6 Continued
Griffon Vulture Gyps fulvus he suggests that two interacting
factors come together to explain the inability of these birds
to avoid what to humans seem to be obvious obstacles. First,
unlike the new world Vultures that use their sense of smell to
locate their food, old world Vultures rely upon their vision. As
a result, soaring birds spend a lot of their time looking down.
As Figure 2.23 illustrates, the eyes of a Griffon Vulture are
positioned such that it has relatively large ‘blind spots’
above and below the head, and a Vulture’s forward vision
has a lower acuity than it’s lateral vision. It seems likely
therefore that they collide with things simply because they
can’t see them! But, perhaps there is slightly more to it
A
60°
B
than this. Martin also suggests that it is possible that birds
frequently fly at, or beyond, the limits of their perceptual
ability by which he means that they may not be in a position
to process all of the high speed visual information they
receive as they move through their environment and that as
a result they often extrapolate or predict what is in front of
them rather than actually seeing it—it may be that because
they don’t expect a fixed position obstacle in the open sky
they simply fail to notice it until it is too late.
Mitigation
What can be done to minimize collision risk? It may be possible for us to position turbines etc. in places that birds are
less likely to encounter them. But where there is a risk of
collisions efforts should be made to prevent them. It could be
possible to manipulate the environment around an obstacle
to divert birds away from it. Planting trees in front of power
lines might ‘force’ birds to lift above them. Putting flags,
discs or balls on the lines to increase their visibility has been
shown to reduce collision incidence in some cases (but it is
likely that if the birds don’t see a line because they are flying
beyond their perceptual ability they probably won’t see a
disc either!). In the case of turbines, it may be possible to
minimize collision risk by siting wind farms in areas less frequently used by birds, for example away from known migration bottlenecks or the flightpaths used by birds moving to
and from a breeding colony. Alternatively, because an immobile turbine probably poses less of a risk than the active turbine (simply because the sweeping blades decrease the area
of ‘safe’ space through which to fly), operating the turbine
only during those periods during which collision is less likely
might be beneficial. Currently there do not seem to be any
really good solutions to the collision problem, but as increasing numbers of wind farms (and other large fixed structures)
are being built, this is a fast moving field and hopefully
major breakthroughs will be made in the near future.
References
Figure 2.23 Flying old world vultures need to scan the ground
below them for carrion. They also need to keep a look-out
side-ways for other vultures who they might be able to follow
towards food. As they fly they pitch their heads through 60o as
shown in figure A. As a consequence they have fairly large blind
spots above and in front of them (shaded blue in figures A and B).
Adapted from Martin, G.R. (2017) The Sensory Ecology of Birds.
Oxford University Press, Oxford.
Dakin, R., Fellows, T.K., and Douglas, L.A. (2016) Visual guidance of forward flight in hummingbirds reveals control
based on image features instead of pattern velocity.
Proceedings of the National Academy of Science 113(31),
8849–54.
Martin, G.R. (2017) The Sensory Ecology of Birds. Oxford
University Press, Oxford.
Wylie, D.R., Gutiérrez-Ibàñez, C., and Iwaniuk, A.N. (2015)
Integrating brain, behaviour and phylogeny to understand
the evolution of sensory systems in birds. Frontiers in
Neuroscience 9(281).
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2.8 The evolution of flight
and flightlessness
Flight path: evolution of birds from dinosaurs, page 6.
Just as the question of the evolution of birds from
dinosaurs has generated controversy (see chapter 1)
so has the question of the evolution of avian
flight itself. So how and when did flight evolve?
The rich dinosaur, paravian, and avian fossil record
that we discussed in the previous chapter helps
us to go some way towards answering this question
(Figure 2.24).
One school of thought suggests that flight
evolved initially as gliding flight and then through
subsequent modification as powered flight, when
animals climbed trees (or cliffs etc.) and used flight
either to slow their fall to earth or to extend their
leap from one high place to another, the tree-down
or arboreal hypothesis. A second school of thought
suggests that flight evolved as a means by which
running animals could increase their stability during an extended leap perhaps to escape a pursuing
predator or to capture fleeing prey (the ground-up
or cursorial hypothesis). The third proposal, the
wing assisted incline running (WAIR) hypothesis
suggests that wings were initially used to propel
animals forward as they ran up a slope that would
otherwise be too steep to climb. Finally it may be
that flapping (and subsequently flapping flight)
evolved as a means of increasing the height gained
during a vertical leap. So what evidence is there to
support these ideas?
Evidence in support of the arboreal hypothesis
comes from a variety of sources; the fossil remains
of many early birds seem better suited to gliding
than to powered flight; many of the dinosaur ancestors of birds were able to climb; the evolution of
flight in mammals (bats) is thought to have been
‘tree-down’; there is a link between climbing and
gliding in a wide range of vertebrate taxa; using
gravity to provide the initial power for flight is easier and more efficient than fighting against it to take
off from the ground; the flight stroke needed to prolong a glide is far simpler than that required to lift a
bird from the ground; and perhaps most significantly a number of the fossil precursors of modern
45
birds had an anatomy and feather types that would
have facilitated gliding but perhaps not sustained
flapping flight. However, it is also the case that
most (but not all) of the ancestral and early birds
had hind legs that are more like those of running
dinosaurs than climbing animals and so the arboreal
hypothesis alone seems to be insufficient.
Key reference
Dececchi, T.A., Larsson, C.E., and Habib, M.B. (2016)
The wings before the bird: an evaluation of flappingbased locomotory hypotheses in bird antecedents.
PeerJ 4, 2159.
So if the early birds and their ancestors were running animals, what support is there for the cursorial,
WAIR, and vertical leap hypotheses? All of these
behaviours, to initiate take off, can be seen amongst
modern birds and so all seem plausible; wildfowl
run across the surface of a lake whilst flapping,
passerines leap into the air and then flap, and
partridges have been observed to use WAIR to propel themselves up slopes that are otherwise too
steep to climb. Alexander Dececchi and his colleagues have used biomechanical modelling techniques taking into account wing and body size,
anatomy, and inferred locomotory ability (running
speed for example) in an attempt to establish the
possibility that non-avian theropods had the ability
to take off and fly in the manner of modern birds—
and to determine the most likely hypothesis for the
evolution of flapping flight. They found that whilst
a small number of paravians like Microraptor would
have been capable of powered flight, most of the
winged ancestors of birds would not have been.
They did not find particular support for any one of
the cursorial, WAIR, or vertical leap hypotheses
over the others; although WAIR did receive the
least support it could not be ruled out entirely in the
case of small-bodied, large-winged animals like
Archaeopteryx. Dececchi’s analyses do however suggest that flapping flight appeared independently
several times in the dinosaur/bird lineage and so
perhaps a single explanation for the evolution of
flight will always be insufficient. It may seem
somewhat paradoxical but from the fossil record
(chapter 1) and Dececchi’s work it appears that
pennaceous-feathered wings and/or tails first
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ESSENTIAL ORNITHOLOGY
Psittacosaurus
Could not fly
Dilong
Could not fly
Filaments
Protofeathers
Pennaceous feathers
Bat-like skin membrane
Ornithomimus
Probably could not fly
Caudipteryx
Could not fly
Yi
Plausible glider
Protofeathers;
could not fly
Microrptor
Plausible glider/incipient
flapping flight
Dinosaurs
Theropods
Maniraptoriforms
Had wings, but
probably could not fly
Zhenyuanlong
Probably could not fly
Pennaraptorans
Had wings; Possible
incipient flight
Paravians
Had wings; Possible
incipient flight
Anchiornis
Plausible glider/incipient
flapping flight
Archaeopteryx
Incipient or more advanced
flapping flight
Avians (birds)
Had wings; capable
of powered flight
Modern bird
Flapping flight
Figure 2.24 Feathers and wings evolved in some early dinosaurs, but flight came later and it is likely that only birds were capable of full
powered flight. From Brusatte, S.L. (2017) A mesozoic aviary: Biomechanical models are key to understanding how dinosaurs experimented with
different ways of flying. Science 355(6327), 792–4. Reprinted with permission from AAAS.
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evolved amongst the flightless theropod dinosaurs.
It is highly likely therefore that their initial function
was not related to locomotion. From fossil evidence
we know that the feathers of these wings were
highly pigmented, so perhaps they had a display
role in courtship or aggression. Or perhaps they
were used as a shield against the elements during
the care of young.
It was once presumed that flightless birds had
evolved from birds that had themselves never
evolved the ability to fly. We know today that this is
not the case and that extant flightless forms are in
fact derived from flying ancestors. If flight was sufficiently advantageous to the ancestors of modern
birds why then should the ability to fly have been
lost? Well, there are situations where flight is no
longer advantageous. The evolution of flightlessness is common for example amongst those species
of terrestrial birds inhabiting isolated islands. In
such habitats, predators are often absent and so
escape flight is not required, nor is it likely that
47
either flight in search of food or flight off the island,
for whatever reason, is particularly important.
Amongst some marine birds the need to fly may be
secondary to the need to swim and in fact wings
may even be a hindrance under water, so they have
been reduced (and as a result some strong swimmers are weak fliers), or even changed completely
through the course of evolution in the case of the
penguins, to become flippers.
Summary
Feathers have a range of functions (insulation,
display etc.) but are crucial to flight and have to be
constantly maintained and regularly replaced by
the process of moult. Flight is energetically costly,
but birds possess anatomical, physiological, and
behavioural adaptations to optimize their efficiency.
Flightlessness in modern birds has evolved as the
loss of flight rather than being the precursor of the
ability to fly.
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C H A PT ER 3
Movement: migration and navigation
‘The stork in the sky knows the time to migrate.’
The book of the Prophet Jeremiah, chapter 8, verse 7
The quotation that opens this chapter demonstrates
that the human appreciation of migration is not a
new phenomenon. The prophet uses migration as a
metaphor to put across a point to his ‘audience’.
This will only work if that audience understand the
substance of that metaphor.
In this chapter I will assume that the reader is
more than a little aware of the phenomenon of
migration but perhaps less aware of its detail.
I want therefore to consider some fundamental
points about migration. Why does it happen? How
is it controlled? How are the bodies of birds adapted
to facilitate migration? What are the consequences
of this behaviour both for the birds themselves, and
in terms of their management and conservation?
I also want to consider other movements of birds
that whilst not strictly migrations per se, do have a
lot in common with them. Finally, I want to think
about the mechanisms that birds use to navigate
during migration, and to extend that discussion
to consider the navigation of birds during their
daily lives.
Chapter overview
3.1
3.2
3.3
3.4
3.5
The ecology of migration
Genes and migration
Physiology and migration
The weather and migration
Navigation
Concept
Categories of movement
It is possible to recognize two distinct categories of
bird movements. The first includes those movements
that are concerned with a proximate response to an
actual resource shortage: foraging trips, commuting or
ranging between patches, and dispersal from a natal
area to an available local area to establish a home
range. These movements conclude when the need for
the resource involved is satisfied.
The second category of movements are true
migrations, triggered by internal rhythms or by a
forecast of resource shortage. They are characterized by
the physiological suppression of the proximate response
to resource need and their conclusion is a result of
physiological changes resulting from the movement
itself.
If they know nothing else about birds, most people
will be able to tell you that some of them migrate.
They might not get the detail right, but they will be
able to tell you that birds fly south (or north depending on your hemisphere of residence) to avoid bad
weather. The general phenomenon of migration,
the periodic mass movements of species along
established routes, fills us with awe. In fact the level
of interest in these long distance movements is such
that in 2004 and 2005 millions of people followed
with rapt attention the progress of a handful of
Tasmanian Shy Albatrosses Thalassarche caute as
they undertook a journey of around 10,000 km
Essential Ornithology. Second Edition. Graham Scott, Oxford University Press (2020). © Graham Scott (2020).
DOI: 10.1093/oso/9780198804741.003.0003
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across the open waters of the Southern Ocean to
and from South Africa. Tracking the birds was possible because they had been fitted with electronic
satellite tracking devices and because their daily
progress is mapped on an open-access internet site.
The project, The Big Bird Race, was an innovative
collaboration between the business community (in
this case the bookmaker Ladbrokes), the Tasmanian
State Government, the scientists of The Conservation
Foundation and, in some senses most importantly,
by publicity-generating private individuals such as
the model and actress Jerry Hall (who sponsored
the 2004 winning bird ‘Aphrodite’) and the publisher Nicholas Coleridge, a direct descendent of
Samuel Taylor Coleridge author of Rime of the
Ancient Mariner, the classic poem in which the fate
of an Albatross is somewhat prophetically linked to
the fate of man. The bets placed on The Big Bird Race
Box 3.1 Albatrosses in crisis
The Diomedeidae, the family to which the albatrosses
belong, has been described as the world’s most threatened
bird family. In 2017 the IUCN Red List categorized all 22
species as being under threat of extinction at some level.
Three of the species (Tristan Albatross Diomedea dabbenena,
Amsterdam Albatross Diomedea amsterdamensis, and
Waved Albatross Phoebastria albatrus, are all critically
endangered and therefore at high risk of extinction. A further 12 species are listed as being threatened, vulnerable or
endangered, and the remainder are classed as being near
threatened. In spite of the excellent work of ornithologists
and conservation organisations, 12 species still have a
declining population trend. For two species the trend is
unknown, four species are thought to be stable, and thankfully four are on the increase (but not yet secure).
Despite their enigmatic status as lonely wanderers of the
oceans, we know surprisingly little about the biology of
these long-lived seabirds away from their breeding grounds
because historically they have been very difficult to study. For
example, despite more than 20,000 Wandering Albatross
Diomedea exulans being ringed/banded during one 29-year
study, only 81 of them were ever recaptured or found away
from their nest site. Through the use of increasingly sophisticated satellite tracking technology we are beginning to
uncover the migratory and dispersive strategies and feeding behaviours of individuals and of populations of birds.
Members of the British Antarctic Survey have, for example,
recently determined that in the case of adult Grey-headed
Albatrosses Thalassarche chrystostoma (Figure 3.1), three
discrete movement strategies seem to be apparent. Some
birds stay in their breeding range in the South Atlantic on
and around South Georgia. Others make regular return
migrations from here to a specific area of the southwest
49
Indian Ocean. Interestingly this area also supports a resident
(breeding) population of Grey-headed Albatross, but one
that is relatively sedentary. Finally, some South Georgian
birds make one or more trips around the world between
breeding attempts. Some of these birds fly close to 1000 km
per day and the fastest recorded circumnavigation took just
46 days (in theory the fastest non-stop circumnavigation
would take 30 days). Satellite tracking has also revealed
that in addition to annual migrations individual Wandering
Albatross may make foraging trips of between 3,600 km and
15,000 km over up to 33 days when their mates are incubating eggs. Once the chicks have hatched the trips shorten to
around 300 km over three days.
It is crucial that the movement patterns of these seabirds
are established so that effective conservation strategies can
be developed. Unlike many birds, the albatrosses are not
endangered because their breeding habitats are threatened,
they are dying out largely because they are the accidental
bycatch of human fishing activities. Specifically hundreds of
thousands of seabirds fall victim to one fishing technique,
longlining, each year. During longlining operations, thousands
of baited hooks on a line up to 130 km long are dragged
behind a boat. Seabirds in general and albatrosses in particular,
attempt to take this bait, are hooked, and drown. Mitigation
strategies have been put in place around South Georgia,
including a partial closure of the Patagonian toothfish
Dissostichus eleginoides longline fishery and as a result
albatross bycatch in the area has been reduced to a minimal
level. However, recent surveys of the South Georgia albatross
population carried out by Sally Poncet and her colleagues
have reported that between 2004 and 2015 populations of
continued
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Box 3.1 Continued
Figure 3.1 Grey-headed Albatross (© Ian Robinson).
Wandering and Grey-headed Albatross have declined by
18 per cent and 43 per cent respectively.
The Grey-headed Albatross migration study suggests that
for this species at least, only birds staging in the southwest
Indian Ocean are likely to come into direct contact with
intensive longlining and so perhaps it is in this area that
mitigation efforts should be concentrated. The good news is
that some mitigation is possible: by minimizing discards
from fishing boats so that birds are not attracted to the
area, by setting the lines at night when most seabirds are
not foraging, or by weighting the lines to sink the bait
below the birds’ reach, it is possible to minimize the
impact that longlining has. Of course this will only happen
if boat owners accept and implement these mitigation
methods. Towards this end the governments of 13 countries have already become signatories to The Agreement
for the Conservation of Albatrosses and Petrels (ACAP). In
doing so they have agreed to take specific measures to
ensure that their national fishing fleets reduce the impact
raised vital funds towards the ‘Save the Albatross
Campaign’ administered by BirdLife International,
and the race itself brought to the attention of the
public the plight of Albatrosses and of seabirds in
general (see Box 3.1).
Not all bird migrations are of the globe-trotting
scale of the albatrosses. Another Tasmanian-breeding
of longline fisheries and to improve the conservation status of the birds concerned. In light of estimates that
between a third and a half of all longlining is being carried
out by illegal pirate fishing boats, with no specific national
allegiance, the pressure for change must be maintained lest
the albatross become a weight around our collective neck.
References
Croxall, J.P. (2008) The role of science and advocacy in the
conservation of Southern Ocean albatrosses at sea. Bird
Conservation International 18, 13–29.
Croxall, J.P., Silk, J.R.D., Phillips, R.A., et al. (2005) Global
circumnavigations: Tracking year-round ranges of nonbreeding albatrosses. Science 307, 249–250.
Poncet, S., Wolfaardt, A.C., Black, A., et al. (2017) Recent
trends in numbers of wandering (Diomedea exulans),
black-browed (Thalassarche melanophris) and greyheaded (T. chrysostoma) albatrosses breeding at South
Georgia. Polar Biology 40, 1347–58.
bird, the Swift Parrot Lathamus discolour also undertakes an annual migration. This species breeds in
western Tasmania and feeds largely on the blossom
and nectar of the seasonal flowers of Eucalyptus species. As the breeding season draws to a close, the
flowers become less common and the birds range
into eastern Tasmania before making a migration
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northwards across the 300 km Bass Strait into southern Australia. Throughout the southern winter the
parrots range across southern Australia in search of
food before re-crossing the straits in time to breed
the following year.
Concept
The Red List
Since 1964 the International Union for the
Conservation of Nature (IUCN) has maintained a list
of endangered species. This Red List, as it is known,
provides the public and policy-makers with an annual
assessment of the risk of extinction of thousands
of species. Risk is categorized at several levels taking
into account population size, population trends, and
geographical distribution.
3.1 The ecology of migration
Why do birds migrate? In the northern hemisphere
we tend to think of migrating birds leaving our
shores to winter in a place that offers a more benign
climate and guaranteed food resources. Similarly
we think of the birds that winter with us as doing so
to avoid even more harsh conditions at their breeding sites. So we could argue that birds migrate to
avoid cold weather. We should remember however
that not all migrations are a response to colder winter conditions. In the tropics many species migrate
in response to the seasonal patterns of rainfall and
drought. But in the case of both tropical and temperate bird species it would appear that migration
is at least in part an evolutionary response to predictable climate variability. Migration must therefore also be in part a response to seasonal variations
in food resources that accompany these climate
fluctuations. But it has also been suggested that
migrations may have evolved in response to seasonal changes in the inter- and/or intraspecific
dominance relationships between birds—the idea
being that at some times of the year the level of
competition faced by some birds is such that they
migrate to lessen it. You may notice that my language in the preceding paragraph has been quite
negative, but perhaps we shouldn’t see migration
just as a drastic measure taken to avoid hardship.
We could equally well think of it as a strategy
adopted by birds to allow them to take advantage
of a seasonally available opportunity. Think of it
51
this way—should we think of a temperate migrant
such at the Sedge Warbler Acrocephalus schoenobaenus or the Yellow Warbler Dendroica petechina as a
temperate bird that tolerates the heat and humidity
of the tropics to avoid the northern winter? Or, as a
tropical bird that takes advantage of the extended
foraging permitted by the longer temperate days?
Whatever the reasons for migration, however, one
thing is clear, migration must ‘pay’ because if it did
not birds would not do it. Migration is costly in
energy terms and in terms of risk, many species pass
through geographical bottlenecks as they migrate
and at these times they are particularly vulnerable to
predators including man (it has been estimated that
only 60 per cent of the wildfowl that migrate south
through the USA in fall each year return to breed
the following spring). At least one species of bird of
prey, Eleonora’s Falcon Falco eleanorae, takes advantage of the seasonal glut of migrating prey by timing
its breeding to coincide with the autumn passage
of passerine migrants out of Europe across the
Mediterranean Sea into North Africa. Equally however, if migration does pay why do some species
stay put? Well for each species a balance is probably
struck and we can go some way to understanding
this balance if we compare key aspects of the life histories of generalized tropical residents, temperate
residents, and migrants (Table 3.1).
Key reference
Ketterson, E.D. and Nolan, V. Jr. (1983) The evolution
of differential bird migration. Current Ornithology 1,
357–402.
In their study of the Dark-eyed Junco Junco hyemalis,
Ketterson and Nolan have compared the migration
behaviour of males and females. They have shown
that each sex responds in a slightly different way to
the selective pressures acting during migration,
Table 3.1 Comparison of key life history traits of generalized
migrant and resident species
Trait
Temperate
resident
Migrant
Tropical
resident
Productivity
High
Moderate
Low
Adult survival
Low
Moderate
High
Juvenile survival
Low
Moderate
Moderate/High
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with the results that this species exhibits a differential migration. Dark-eyed Juncos breed throughout the northern USA and Canada and populations
winter throughout the USA and in southern
Canada. But within a population the sexes migrate
different distances. Females migrate further south
than males. In this case a longer migration is an
advantage, females have a higher rate of over-winter
survival than males. If migrating a little further
south is such an advantage, why do males risk
dying by travelling less far? Why don’t they overwinter in the same place as the females? The answer
to this question relates to the fact that for males a
second selective pressure exerts a significant influence. Birds that undertake a shorter migration, and
survive the winter, have less far to return to their
summer breeding grounds. Once there, a strong correlation exists between early arrival on territory
and increased productivity. Simply put, the first
birds back get the best spots and raise the most
young. So there is an advantage to male juncos in
not flying too far south that outweighs the risk of
dying during the winter.
Concept
Migration strategies
Migrating birds adopt a number of migration strategies.
Some species make single, long haul flights, others a
series of short hops, refuelling en route. Some species
are funnelled through migration bottlenecks and others
migrate across a broad front. The males and females of
some species migrate separately, or migrate to different
destinations (often referred to as differential migration).
Different breeding populations of a species often use
different wintering areas and may leap-frog over one
another to reach them.
3.2 Genes and migration
During the migratory period passerine birds exhibit
a behavioural change. At night they become restless. This migratory restlessness offers researchers a
means by which levels of motivation to migrate
might be measured and compared.
Captive birds can be housed, singly, in funnel
cages such as that shown in Figure 3.2. The floor of
the cage is an inkpad, the roof of the cage is a wire
screen through which the bird has sight of the night
sky. A non-migrating bird will be inactive at night
and will stand on the pad. But during migration,
Opaque
Circular Screen
Wire Screen Top
Blotting-paper
Funnel
2-Quart
Pan
Ink pad
Rubber
Tubing
Figure 3.2 A migratory bird held in a funnel cage. The bird’s
footprints on the side of the funnel indicate its motivation to migrate
and preferred direction of flight. From Able, K.P. (2004) Birds on the
move: Flight and Migration. Illustration by Robert Gillmor, © Cornell
Lab of Ornithology. In Handbook of Bird Biology. Podulka, S.,
Rohrbaugh, R.W. Jr, and Bonney, R. (eds) The Cornell Lab of
Ornithology, Ithaca.
when the bird becomes restless, it will flutter against
the sloping sides of the funnel. Evidence of this
activity is recorded on the funnel wall by the inky
footprints left by the bird. From this relatively simple arrangement two important pieces of information can be gained: the number of footprints equates
to the level of restlessness of the bird, or the strength
of its drive to migrate, and their position on the funnel wall indicates the direction in which the bird
was driven to fly.
Key reference
Schwabl, H. (1983) Ausprägung und bedetung des teilzugverhaltens einer südwestdeutschen population der
amsel Turdus merula. Journal of Ornithology 124, 101–6.
As a result of observations made of birds in funnel
cages, and of the migratory behaviours of wild
birds, it is well established that individuals of a species can differ from one another in terms of their
migratory behaviour. From these observations it has
been assumed that there is a genetic component to
the control of migration. For example when Schwabl
tested in funnel cages the offspring of blackbirds
Turdus merula from German populations known to
be migratory or resident, the offspring of migrants
demonstrated migratory restlessness but those of
residents did not. Presumably these birds had
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inherited their migratory tendencies from their
parents. Before we look in more detail at the link
between genes and migration, it is important however to recognize the role that environment may also
play. In Britain, the Herring Gull Larus argentatus is a
sedentary species, while the closely related, Lesser
Black-backed Gull Larus fuscus, is migratory. When
Harris cross-fostered the young of these species (i.e.
placed young fuscus in argentatus nests and vice
versa) he found that the young Lesser Black-backed
Gulls raised by Herring Gulls migrated normally—
presumably having inherited their migratory
behaviour from their genetic parents. However,
Herring Gulls raised by Lesser Black-backed Gulls
also migrated, although not as far as their foster parents. These birds had not inherited a migratory
behaviour pattern and so must have been responding to an external environmental cue—possibly the
movement of their foster parents. This demonstrates
that whilst genes are clearly important, environmental factors do have a part to play.
Key reference
Harris, M.P. (1970) Abnormal migration and hybridisation of Larus argentatus and L. fuscus after inter species fostering experiments. Ibis 112, 488–98.
Number of Thirty-Minute Periods per Night with
Migratory Restlessness
The most thoroughly investigated case of the role of
genes in bird migration is that of the Blackcap Sylvia
53
atricapilla, an old world warbler found throughout
Europe and on several North Atlantic islands (the
Azores, Madeira, the Canary Islands, and the Cape
Verde Islands). Peter Berthold and colleagues have
carried out extensive field and laboratory studies of
this bird, and no discussion of the genetics of migration could be complete without consideration of
their work.
Blackcaps demonstrate a range of migratory
behaviours. Populations in northern and eastern
Europe are migrants, most of them spending the
northern winter months around the Mediterranean
or in North Africa. Those of southwest Europe,
the Azores, the Canaries, and Madeira are partial
migrants (some migrate but others remain on their
breeding territories all year round). Populations
of birds found on the Cape Verde Islands are
wholly resident and never migrate. Berthold and
co-workers have compared migratory restlessness
levels of birds from these populations and, as would
be expected, have found that birds from Germany
(migrants) have higher levels of restlessness than
partial migrants from the Canary Islands (Figure 3.3).
When hybrids are formed between these two populations the resultant offspring show an intermediate
level of restlessness, demonstrating that there is a
genetic basis for their migratory behaviour.
Other work carried out by Berthold and his team
has demonstrated the genetic basis for migratory
10
Southern Germany Population
Obligate Migrants
8
S. Germany × Canary
Islands Hybrids
6
4
2
Canary Islands Population
Partial Migrants
0
0
50
100
Number of Days After Migratory Restlessness Began
150
Figure 3.3 Comparison of differing levels of migratory restlessness exhibited by German and Canary Island Blackcaps and exhibited by hybrids
between them. From Berthold, P. and Querner, V. (1981) Genetic basis of migratory behaviour in European warblers. Science 212, 77–9, reprinted
with permission from AAAS.
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ESSENTIAL ORNITHOLOGY
orientation—the compass bearing followed by
actively migrating birds. Blackcaps breeding in central Europe and migrating to Africa could fly due
south and perhaps by doing so minimize their
migratory distance. But if they did, they would also
maximize the time that they spent airborne over the
Mediterranean Sea. This sea passage would be
arduous indeed and few birds would survive it
without significant physiological cost. Instead, eastern birds migrate initially in a south-eastern direction, following a route around the eastern edge of
the Mediterranean and into north-east Africa. Birds
from the west, on the other hand, set off in a southwesterly direction and make the crossing into Africa
via the narrow Straits of Gibraltar. Berthold found
that hybrids between members of these two populations demonstrate a mixed strategy (Figure 3.4),
some flying south-east and some south-west, but
some flying due south. From these observations we
can deduce that the potential for an initially southbound migration has been present in Blackcaps
from central Europe, but that it has been strongly
N
E
W
SW German
birds
Austrian
birds
S
Hybrids
Figure 3.4 Directions of migration of Austrian Blackcaps (inner
circle, white triangles), south-west German Blackcaps (inner circle,
shaded triangles), and of hybrids between them (outer circle, shaded
triangles). From Scott, G.W. (2005) Essential Animal Behavior.
Blackwell Science, Cambridge. Adapted with permission of Springer,
from Helbig, A.J. (1991) Inheritance of migratory direction in a bird
species: a cross breeding experiment with SE- and SW- migrating
Blackcaps (Sylvia atricapilla). Behavioural Ecology and Sociobiology,
42, 9–12.
selected against, and is not expressed in natural
populations.
We are used perhaps to thinking about natural
selection as an evolutionary force that has its effect
over long, perhaps very long, periods of time.
However, from experiments with captive birds it is
clear that the results of selective pressures can be
seen remarkably quickly. In fact Berthold has shown
experimentally that in just three generations of selection for migration a captive population of partially
migrant Blackcaps can become completely migratory, and in just six generations members of the same
population could all be made to behave as residents.
Presumably this is exactly what has happened to the
resident Blackcaps of the Cape Verde Islands, and
to the now-resident populations of the typically
migratory Dark-eyed Junco found on the island of
Guadalupe 250 km off the Californian coast. The loss
of migratory behaviour is a common phenomenon
amongst species that have colonized remote islands.
Flight path: changing environmental pressures can
result in rapid evolutionary change. page 11.
The Blackcap does offer us another example of the
evolutionary flexibility of migratory behaviour. The
British breeding population is a migratory one
which spends the winter months in southern Spain
and North Africa, but in the closing decades of the
twentieth century bird watchers in Britain started to
record Blackcaps during the winter months. It was
assumed that this was because the British climate
had warmed and people had begun to maintain
gardens more suited to the needs of over-wintering
birds. The British public were also providing food
for birds in increasing amounts (by 2000 some 60
per cent of UK households were feeding wild birds
in winter). Initially it was thought that these winter
birds were members of the British breeding population that had chosen for whatever reason not to
migrate. However, as the winter Blackcap population grew, evidence initially from ringing recoveries
and latterly from stable isotope analyses (see Box 3.2
for an explanation of this technique), and from the
tracking of individual birds using geo-locators, has
revealed that they are migrants. In fact they are members of a population of birds breeding in north-west
Europe (Belgium, the Netherlands, and Germany)
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Box 3.2 Stable isotopes and genetic variation as tools to unravel migration
Ringing studies allow us to pin-point exactly where birds go.
But they depend upon our ability to capture a bird at one
location and then recapture it at a later date and in another
place (perhaps thousands of kilometres away). Recapture
rates are very low for the majority of migratory species, perhaps as few as one in a hundred thousand ringed passerines
will be re-trapped in this way. Therefore the detailed information that we have about the breeding and wintering locations of specific populations of birds, and of the staging
posts that they habitually visit during migration has until
recently been quite limited. As technology has developed, a
range of methods which enable the tracking of individual
birds are providing us with fascinating insights into large
scale migratory movements and small scale daily habitat
use. Unfortunately the current costs involved and the limitations of the equipment (size and power principally) means
that even this technology fails to fill as many of the gaps in
our knowledge as we might like.
Chemistry however, may provide us with an answer to at
least some of the questions that we have. You may recall
that chemical elements such as carbon (C) each have a specific atomic number, which equates to the number of protons
found in the nucleus of one atom of that element—so carbon for example has 12 protons and the atomic number 12.
But whilst the number of protons in a carbon atom is constant, the number of neutrons is not. So carbon can exist in
various forms or isotopes. Examples are carbon-12 (C12),
carbon-13 (C13), and carbon-14 (C14). Atoms of these isotopes all have 12 protons, but a C12 atom has 12 neutrons,
C13 has 13, and C14 14. During photosynthesis, plants fix
atmospheric carbon and the ratio of C12 to C13 that is fixed in
this way can be characteristic of particular vegetation communities. This particular ratio can be detected in the carbon
containing tissues of birds that have grown while they were
feeding on plants, or on animals that had fed on plants, in an
area dominated by that vegetation community type. So if we
trap a bird in one area of known C12:C13 ratio and find that
its feathers exhibit a different ratio we can be sure that it
grew them elsewhere. In fact the distributions of these
plants results in the existence of a latitudinal gradient of the
isotope C13. A latitudinal gradient of the hydrogen isotope
deuterium also exists (related to a latitudinal gradient in
annual rainfall), and gradients or variations in the isotopes
of other elements also exist. By comparing information from
the isotopes of a range of elements in bird tissues with those
from the environments through which a bird might have
travelled, we might be able to pin-point the areas that a bird
has actually visited more precisely.
But does the theory work? Well the answer to this question is yes it would appear that it does. As an example consider the work of Chamberlain and co-workers. They have
collected feather samples from Willow Warblers Phylloscopus
trochilus of two recently diverged (in evolutionary terms),
but discrete sub-species P. trochilus trochilus and P. trochilus
acredula. Willow Warblers (Figure 3.5) are common throughout Europe, but the birds that they studied come from an
interesting Swedish population where the ranges of the two
sub-species come into contact. Acredula breed in the north
of the country, trochilius breed in the south, and the breeding ranges of the birds overlap slightly at 62°N latitude.
Limited evidence from ringing recoveries suggests that the
populations of the two sub-species winter in different areas
of sub-Saharan Africa (see Figure 3.6). If this is the case, one
might expect tissues produced during the winter to vary in
terms of their isotope ratios in a way that would reflect variation in the environmental isotope ratios in these different
regions. Willow Warblers undergo a complete moult during
the winter and when feathers from birds that had returned
to Sweden after migration were analysed, it was found that
the makeup of the feathers of the two different sub-species
varied significantly in terms of their carbon and nitrogen
isotopes. What is more, the researchers found a sharp
change in their data in samples collected on either side of
Figure 3.5 Willow Warbler Phylloscopus trochilus trochilus
(© Ian Robinson).
continued
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Box 3.2 Continued
the 62°N line of demarcation between the breeding populations. The evidence of the chemistry therefore supports the
evidence of ringing studies and the technique could be
important in making the links between far distant habitats
that are essential to specific populations of migrating birds.
Max Lundberg and his colleagues have used wholegenome sequencing to compare the genetic profiles of
P. trochilus trochilus and P. trochilus acredula and correlated
the differences that they have found with the migratory
phenotypes of the two sub-species. Their analysis has
revealed that although their genotypes are almost the same
(which we would expect given their close evolutionary relationship and recent divergence) they differ in three key areas
of chromosomes 1, 3, and 5. The variation found in chromosome 3 does not seem to be related to migratory strategy,
trochilus
acredula
that was previously assumed to migrate south-west
to winter around the western Mediterranean. We
now know that in fact the Blackcap population of
north-west Europe exhibits at least two migratory
strategies, and whilst the majority of birds do
migrate south-west, an increasing number migrate
rather it correlates with differences in breeding altitude and
latitude and involves a gene (RYR2 ) known to be involved in
heart muscle activity and to be under selection in high altitude species. The variations in chromosomes 1 and 5 do correlate with migratory strategy and involve genes that are
known to be involved in metabolic processes. The authors
speculate that this genetic variation may be related to different adaptations for fuel use associated with the different
migratory strategies of the two sub-species.
Reference
Lundberg, M., Liedvogel, M., Larson, K., et al. (2017) Genetic
differences between willow warbler migratory phenotypes are few and cluster in large haplotype blocks.
Evolution Letters 1(3), 155–68.
Figure 3.6 The distribution of Swedish breeding
populations of P.t. trochilus (dotted pattern) and P t.
acredula (striped pattern) and the contact zone between
them (black area). Arrows indicate the presumed migratory
route of both sub-species and the sites of recoveries of
ringed birds in Africa are marked. From Chamberlain, C.P.,
Bensch, S., Feng, X., et al. (2000) Stable isotopes examined
across a migratory divide in Scandinavian willow warblers
(P. trochilus trochilus and P. trochilus acredula) reflect their
African winter quarters. Proceedings of the Royal Society B:
Biological Sciences 267, 43–9.
north-west. Before the conditions changed, any
central European birds that migrated to Britain
would not have survived the winter months. As
conditions became more favourable though, birds
tthat migrated to Britain and survived were at an
advantage compared with those that wintered
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further south because their return trip was a shorter
one and so they tend to arrive back on the breeding
grounds first. As a result these birds have access to
the best territories and have better breeding success.
They also tend to mate assortatively (pairs of
birds tend to migrate to the same area) and there is
evidence that the north-west and south-west migrating populations are differentiating genetically and morphologically. Because the offspring of
these birds share their parents migratory orientation
(remember there is a genetic component to this
novel migratory behaviour), the population will
continue to increase unless conditions in Britain
change again and birds are no longer able to survive
the winter months.
Key references
Bearhop, S., Fiedler, W., Furness, R.W., et al. (2005)
Assortative mating as a mechanism for rapid evolution
of a migratory divide. Science 310, 502–4.
Heimer, D., Salewski, V., Fiedler, W., et al. (2018) First
tracks of individual Blackcaps suggest a complex migration pattern. Journal of Ornithology 159(1), 205–10.
Rolshausen, G., Segelbacher, G., Hobson, K.A., and
Schaefer, H.M. (2009) Contemporary evolution of reproductive isolation and phenotypic divergence in sympatry
along a migratory divide. Current Biology 19, 2097–101.
3.3 Physiology and migration
Whilst it is certain that there is a genetic component
to the control of migration, it is important to remember that genes operate in environments; using the
word environment here in its traditional ecological
sense and also in the sense that the expression of the
gene or the activity of its protein product will be
effected by the internal or physiological environment of the body, and the social environment of the
bird concerned. The control of migration must
therefore integrate behaviours conducted over a
range of timescales and a range of strategies. In
terms of timing, the onset of migration needs to be
managed at the seasonal/annual scale and on a
day-to-day basis during the migration period itself.
For example, usually diurnal species often need to
switch their behaviour patterns to become mobile at
night; and before/after migratory flights birds often
exhibit a shift in diet or hyperphagia. Some migrants
undertake a single long haul flight, others migrate
57
via a series of shorter hops with periods of refuelling
along the way. The migration facilitating behaviours (and life-cycle consequences) of these different migratory strategies have a significant impact
upon individuals and populations.
Concept
Hyperphagia
Birds that are about to undertake an endurance flight
as part of their migration, or have just completed
such a flight, typically exhibit a heightened motivation
to feed. This ‘over eating’ is termed hyperphagia, a
behaviour that is often also associated with a dietary
switch as birds increase the rate at which they store fat,
the main fuel for migration.
3.3.1 Seasonality and coordination of migration
In my hometown in northern England the autumn
migration is heralded by the sudden departure of
the Swifts Apus apus. One day flocks of screaming
swifts can be seen chasing one another up and
down our streets and then seemingly all at once
they are gone. The conditions for their epic flight to
southern Africa are right and in one coordinated
movement they leave. Synchronized autumnal
migration is a commonly observed phenomenon,
and one that requires some explanation given that
other life-cycle milestones are less synchronous for
some species. For example some young Yellowgreen Vireos Vireo flavoviridis are hatched early in
the breeding season while others are hatched some
weeks later and yet, as a population, they typically
embark upon their autumn migration at roughly
the same time. Prior to migration all young vireos
must fledge (leave the nest), undergo a partial
moult, and store the fat that they will need to fuel
their migratory journey. From the research of John
Styrsky and his colleagues it seems that individual
vireos vary the relative timing of each of these steps
according to their hatch date. Under experimental
conditions they found that whilst the earlier hatched
birds might take as many as 145 days before they
begin their post-juvenile moult, the latest hatched
birds (hatched as many as seven weeks later) begin
their moult after just 70 days. This of course results
in the birds being relatively synchronous in the timing of their moult (and it turns out in the deposition
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of fat and the initiation of migratory restlessness).
The birds involved in this experiment had all been
collected from the wild when just a few days (six to
eight) old and then raised in standard conditions. So
whatever it was that triggered the accelerated development of the late birds must have had its effect during those first few days of life. It seems likely that the
birds even at this early stage were sensitive to photoperiod and took their developmental cue from the
day length that they experienced immediately after
hatching—a phenomenon described as a calendar
effect. Remarkably in this study day lengths across
the hatching period varied by just 33 minutes.
Key references
Falsone, K., Jenni-Eiermann, S., and Jenni, L. (2009) Corticosterone in migrating songbirds during endurance
flight. Hormones and Behaviour 56, 548–56.
Styrsky, J., Berthold, P., and Robinson, M.D. (2004)
Endogenous control of migration and calendar effects
in an intratropical migrant, the yellow-green vireo.
Animal Behaviour 67, 1141–9.
3.3.2 Hormones and the control of migration
It is highly likely that hormones are key to the control of life-cycle steps such as the timing of moult
and the onset of migration and there is some evidence that the seasonality of migration is linked to
the production by the adipose tissue of hormones
such as adiponectin and visfatin. Testosterone has
been implicated in the onset of pre-migratory fuelling and restlessness, and at the smaller scale
levels of the hormone melatonin have been implicated in the timing of nocturnal migratory activity.
But currently the hormone that is most studied
and therefore perhaps best understood in the context of the control of migration is the glucocorticoid corticosterone. In their studies of migrating
European Robins Erithacus rubeclua and Pied
Flycatchers Ficedula hypoleuca, Karen Falsone and
her colleagues found that baseline corticosterone
levels in birds that were captured during their
natural migratory flight were higher than those of
birds that were resting. They suggest that the hormone has a role to play in the management of
energy supply during endurance flying, and in
particular in the regulation of use during migration. This is because when fat reserves are
exhausted corticosterone levels increase, facilitating a shift to protein metabolism and subsequently
a shift to landing behaviour and feeding (refuelling) as is discussed in Box 3.3.
Box 3.3 Putting on fat for migration
To elucidate the role of corticosterone in the control of premigratory fattening and the onset of migratory flights, Cas
Eikenaar and colleagues compared the hormone levels and
migratory behaviours of two sub-species of Northern
Wheatear Oenanthe oenanthe at a shared stop-over site;
the North Sea island of Helgoland off the coast of Germany.
In spring birds of the sub-species O.o. oenanthe (Figure 3.7)
which breeds in northern Europe have a relatively short
Figure 3.7 Northern Wheatear Oenanthe
oenanthe oenanthe breaking its migration for
just a few hours on the English Yorkshire coast
(© Will Scott).
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onwards journey to their breeding grounds or next stop-over
(a sea crossing of 50–250 km); but O.o. leucorhoa, which
breeds in Iceland, Greenland, the Faroe Islands, and Canada
has a far longer journey to make (a sea crossing of 1,000–
2,500 km). The researchers hypothesized that if corticosterone promotes refuelling, leucorhoa should have higher
levels than oenanthe, and that the rate at which birds feed
(store fat) should be positively correlated with hormone
levels. They found however that although leucorhoa do put
on more weight at a faster rate than oenanthe, they in fact
had lower levels of corticosterone and that their rate of fat
deposition was negatively related with hormone levels. So in
this species at least it would appear that corticosterone does
not promote refuelling.
So what does it do? In a second experiment Eikenaar and
co-workers studied Wheatears on Helgoland during the autumn
migration (without distinguishing the two sub-species) to
test the hypothesis that rather than promoting refuelling,
levels of corticosterone are important in triggering the shift
in behaviour from refuelling to migratory flight.
Their results supported their hypothesis (Figure 3.8). They
also found that hormone levels were positively correlated
with the date in the migration season and the occurrence of
winds that are conducive to migration, both of which are of
course also positively correlated with the motivation of a
bird to migrate. It would appear therefore that in this species
at least corticosterone is involved in the control of shift from
pre-migratory feeding to migratory flight.
Reference
Eikenaar, C., Fritzsch, A., and Bairlein, F. (2013) Corticosterone
and migratory fuelling in Northern wheatears facing
different barrier crossings. General and Comparative
Endocrinology 186, 181–6.
(B)
departure time (min after sunset)
(A)
59
corticost erone (ng ml–1)
12
10
8
6
4
0
departing
staying
350
300
250
200
150
100
50
0
1 2 3 4 5 6 7 8 9 10 11 12
Cortieosterone (ng ml–1)
Figure 3.8 Wheatear with higher levels of corticosterone are more likely to initiate their migratory flight than those with lower levels (A);
and corticosterone levels are negatively correlated with departure time after sunset (B). From Eikenaar, C., Müller, F., Leutgeb, C., et al. (2017)
Corticosterone and timing of migratory departure in a songbird. Proceedings of the Royal Society B 284, 1–6.
3.3.3 Fuelling migration
Fat is stored in often extensive reserves across the
body of a bird, but principally under the skin, in the
muscles, and in the peritoneal cavity. As a fuel fat is
highly efficient, potentially yielding more than
seven times as much energy as an equivalent mass
of protein or carbohydrate. However, stored fat is
not instantly available for energy release and at the
onset of an endurance flight a limited amount of
protein or carbohydrate metabolism is essential.
When fat reserves are depleted a switch back to protein metabolism will be necessary if a refuelling
stop cannot be made. Shifts from fat to protein
metabolism also take place when birds become
dehydrated during migratory flights because protein releases around six times as much water as fat
per calorie of energy produced. On average birds
increase their body fat from around 5 per cent of
their total mass when not migrating to 25–35 per
cent during migration. These increases in stored fat
inevitably lead to increased body mass and in the
extreme case of the Ruby Throated Hummingbird
Archilochus colubris, a doubling of mass from 3 g to 6 g
is needed if this tiny bird is to successfully make
an 800 km crossing of the open water of the Gulf of
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ESSENTIAL ORNITHOLOGY
Mexico as part of its annual migratory journey.
There is of course an upper limit to the extra fat that
a bird can carry if it is to continue to fly efficiently
and birds have adapted to cope with this limitation
in a number of ways. Some species strategically balance their lean muscle to fat ratio to ensure the optimal mass for long distance flights, and we will look
at this in more detail a little later. Other species take
advantage of the fact that their migratory routes
pass through sites that are ideal as refuelling stations. They store just enough fuel to make the ‘hop’
from one of these staging posts or stop-overs to the
next. In some species the same sites are used by the
same individuals year after year. After migration, or
during a stop-over during migration, birds need to
rapidly restore their reserves but because there may
be a lag-time before they are able to feed again, they
often continue to metabolize residual fat reserves
for a short period. Although as Box 3.4 illustrates,
modern agricultural practices may be negatively
impacting stop-over feeding behaviour.
Flight path: Foraging behaviour is flexible and
responds to changing physiological needs. page 125.
Box 3.4 Pesticides can hamper migratory refuelling
In the mid 1990s a new family of pesticides appeared on the
market. These neonicotinoids were originally thought to be
less likely to harm vertebrates because their ability to bind to
vertebrate neuro-receptors was less strong than their ability
to bind to the receptors of the invertebrates they were
designed to target. Unfortunately scientists are beginning to
realize that the indiscriminate nature of the effect of these
pesticides is having a devastating impact upon essential pollinators like bees, and is having a direct impact upon birds.
Birds can be exposed to neonicotinoids directly (during
spraying) or by ingestion of contaminated soils and seeds.
Even relatively low dosage exposure is known to impact
negatively upon condition, survival, and behaviour, and
recently Margaret Eng and her colleagues have demonstrated an impact upon bird migration.
The researchers captured White-crowned Sparrows
Zonotrichia leucophyrs (Figure 3.9) during their spring
migration, recorded their weight and the amount of fat that
they were carrying, and then exposed them to very low sublethal oral doses of the neonicotinoid imidacloprid. Some
birds were exposed to a low dose, some to a higher dose,
and some to a control substance (sunflower oil). The doses
Figure 3.9 White-crowned Sparrow Zonotrichia leucophyrs (© Peter Dunn).
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involved were typical of those that birds might encounter
naturally as they migrated through recently treated agricultural land. The researchers held the birds overnight and then
re-weighed them and fitted them with a tracking device
before releasing them back into the wild. Comparisons of
the birds’ weights showed that during the first six hours
after being exposed to the pesticide they lost fat and weight,
and the effect was more pronounced in those birds that
received higher doses (Figure 3.10). They also found that
birds that had received the highest doses consumed far less
food in captivity than the birds that received no pesticide or
a low dose.
Monitoring of the birds post-release revealed that the
birds that had not been exposed to the pesticide tended to
spend a shorter period at the migratory stop-over site, most
(A)
of them resuming their northwards journey very soon after
release. Weather permitting, the median time to departure
was just 12 hours and all of these birds had departed within
four days. Birds that had been exposed to the chemical
delayed their departure (low dose median three days, high
dose four days, with some birds waiting as long as nine days).
It is likely that these extended stop-overs are a consequence
of the birds having lower fat stores and a reduced level of
feeding and therefore refuelling after exposure. Although it is
known from laboratory studies that birds exposed to similar
doses do make a full recovery, and, from this study that once
the birds did set off on their migratory flight, direction and
duration was as would be expected, the delay and even short
term loss of condition that these birds suffer is likely to have
individual fitness and population level effects.
(B)
0
% Change Body Fat
% Change Body Mass
50
–0.5
Control
Low
25
0
–25
High
Control
Low
Treatment
High
Control
Low
Treatment
High
Treatment
(D)
30
4
Food Construption
% Change Lean Mass
(C)
0
–0.4
20
10
0
Control
Low
Treatment
High
Figure 3.10 The effect of the neonicotinoid imidacloprid on migrating White-crowned Sparrows. Compared to control birds, treated birds
lost body mass (A), and fat (B) and had a reduced appetite (D) they also suffered a loss in lean mass (C) although not a statistically
significant one. From Eng, M.L., Stutchbury, B.J.M., and Morrisey, C.A. (2019) A neonicotinoid insecticide reduces fuelling and delays
migration in songbirds. Science 365, 1177–80. Reprinted with permission from AAAS.
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3.3.4 Long haul flights
Not all migratory routes allow refuelling. For
example, the geographical distribution of sightings of Bar-tailed Godwits Limosa lapponica of the
race baueri suggested to Robert Gill and colleagues
that these birds were likely to make the annual trip
from their New Zealand wintering areas to their
Alaskan breeding grounds in a series of short
hops, refuelling en route, but that the return trip
was probably completed as a single trans-Pacific
flight. Using theoretical models that incorporated
information about the known flight metabolism of
godwits and the weather systems prevalent along
their presumed migration routes, Gill and his colleagues proposed that the birds would be capable
of making this 11,000 km trip without refuelling. In
2007 their proposal was validated when a satellitetagged female godwit made the trip north to
Alaska via China in two ‘hops’, one of 10,200 km
and a second of 5,000 km. It then went on to make
the 11,500 km return trip in just eight days (and
remember that unlike a seabird, a godwit cannot
rest at sea).
To achieve these astonishing long haul trips, the
birds metabolize a large fat reserve (migrating birds
may carry 41 per cent of their mass as fat), and have
evolved a migratory strategy that takes advantage of
the fact that the dominant atmospheric pressure systems across the Pacific during the migration season
reliably generate favourable winds. But it is likely that
as in the case of other godwits and other species of
bird, that some protein metabolism is also necessary—
with the effect that body condition may suffer.
Key references
Gill, R.E. Jr, Piersma, T., Hufferod, G., et al. (2005)
Crossing the ultimate ecological barrier: evidence for
an 11,000-km-long non-stop flight from Alaska to New
Zealand and Eastern Australia by bar-tailed godwits.
The Condor 107, 1–20.
Landys-Ciannelli, M.M., Piersma, T., and Jukeman, J.
(2003) Strategic size changes of internal organs and
muscle tissue in the bar-tailed godwit during fat storage
on a spring stopover site. Functional Ecology 17, 151–9.
Bar-tailed Godwits of the race Limosa lapponica
tamyrensis may not undertake as impressive a
long haul migration as their baueri ‘cousins’, but
they do make a 9,000 km migration between
breeding grounds on the Russian Taymyr peninsular and the mudflats of west Africa, and in particular those of Mauritania and Guinea Bissau.
However, these birds do not make the trip as a
single flight. Instead they divide the journey into
two approximately equal flights each lasting
around 60 hours. Between these two flights they
spend a month refuelling on the rich mudflats of
the Dutch Wadden Sea.
When Landys-Ciannelli and co-workers examined the bodies of Bar-tailed Godwits at various
points during the refuelling period, they found the
amount of fat that the birds carried increased with
time (from around 10 per cent to 30 percent of total
body mass); exactly what one would expect if, during refuelling, birds are replacing fat used up on
the first leg of the journey and then laying down a
store for use on the second. They also found some
extremely interesting changes in muscle mass suggesting that the birds may be varying the mass that
they carry in a strategic way. The mass of the muscles associated with flight varied in line with fat
load. Birds had a lower muscle mass when they
arrived at the stop-over site than they did when
they left—so we can assume that some flight muscle
is lost during flight and presumably birds build up
their flight machinery so as to be as prepared as
possible for the coming journey. Variations were
also found in the mass of the stomach, kidneys,
liver, and intestines, i.e. in the organs associated
with digestion. Newly arrived birds arrived with
low mass and very quickly gained mass in all of
these components of the digestive system. We
would expect them to do so given that they are
about to engage in a bout of prolonged hyperphagia. But unlike the continuing weight gain observed
in fat stores and in flight muscles, this weight gain
peaked during the early part of the refuelling
period—mass remained constant during the middle period, and then as departure neared mass fell
again as the digestive system atrophied. In this way
the birds seem to manage their ‘baggage-allowance’
they do not carry extra mass associated with a
redundant function (godwits cannot feed on the
wing) and must therefore ‘save fuel’.
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Flight path: Birds strategically manage their mass to
maximize flying efficiency. page 30.
3.4 The weather and migration
Local weather conditions, and the broad scale
weather patterns that they predict, have important
consequences for migrating birds. The majority of
them prefer to set off under fine anticyclonic conditions with little or no cloud cover and favourable
tail winds. At night when most passerines and other
smaller birds are on the move, clear skies make
celestial navigation possible. During the day, clear
skies enable the development of thermals and orographic uplift that enable larger soaring birds like
raptors and storks to travel huge distances with little energy expenditure. But as you are no doubt
aware the weather is not a constant and in the face
of changing conditions birds must alter their behaviour to maximize their chances of success. When
birds make the ‘wrong’ decision things can end terribly as Norman Elkins describes in his excellent
book Weather and Bird Migration. In the book
Elkins provides an account of an extreme fall (‘fall’
being the term used to describe a mass grounding
of migrating birds) that occurred in south-east
England on a single day in 1965. High pressure over
Scandinavia had created the ideal conditions for
the initiation of migration, but as they crossed the
North Sea the migrating birds encountered a warm
front associated with a small but intense low pressure system. Encountering cloud, rain, and
unfavourable winds, the birds were forced away
from their usual southwards route. Thousands of
dead birds were washed up along the English coast,
presumably their energy reserves had run out as
they struggled against the wind. Enormous numbers
of birds did make landfall however—one recorder
estimated more than 30,000 displaced migrants along
just 4 km of the coastline and half a million along a
40 km stretch. Reports of the day even suggest that
such was the shortage of trees in some towns that
birds fluttered onto the shoulders of people!
Radar studies have revealed that when the
weather is less than optimal for migration birds
choose not to set off on their migratory flight, or if
63
they have started they pause. To birdwatchers this
is particularly noticeable at migratory bottlenecks
or ahead of major geographical barriers, such as the
Gulf of Mexico. Then, when a window of opportunity
arises and weather conditions are favourable they
depart en masse. For a number of years the only
insights we had into the effects of weather on migrating birds came from these large-scale observations of birds at particular locations and often in
the face of unusual or extreme weather phenomena.
But recent advances in technology have allowed an
unprecedented level of insight into the day-to-day
decision-making of individual birds. Raymond
Klaassen and his colleagues have studied the annual
migrations of Montagu’s Harriers Circus pygargus
migrating to and from their breeding grounds in
the Netherlands and their winter quarters in subSaharan Africa. These harriers adopt a mixed flying style during migration, using flapping flight
when they have to but taking advantage of thermals and soaring when they can. Because the birds
were fitted with GPS-loggers, Klaassen was able to
record their position several times per hour during
the day and several times each night. For some
birds data was collected every few seconds which
provided highly detailed information about flying
behaviour. Their results revealed that the harriers
are a diurnal migrant, resting at night, and that
they alternate flying and foraging throughout the
day even when crossing the Sahara (suggesting
that it is a less harsh environment than might have
been assumed). The importance of weather was
confirmed because the birds flew for longer and
flew further on days when they benefitted from
stronger tailwinds. As might be expected the harriers were also recorded as resting more on days
with strong headwinds, presumably they were
waiting for the wind to change rather than ‘wasting’ energy flying into it.
Key references
Elkins, N. (1983) Weather and Bird Migration. T. &
A.D. Poyser, Calton.
Klaassen, R.H.G., Schlairch, A.E., Bouten, W., and
Koks, B.J. (2017) Migrating Montagu’s harriers frequently interrupt daily flights in both Europe and Africa.
Journal of Avian Biology 48, 180–90.
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ESSENTIAL ORNITHOLOGY
Box 3.5 Impacts of light ‘pollution’ on migration
There are numerous examples of migrating birds being drawn
off course and congregating around artificial light sources
such as offshore installations (oil and gas platforms, wind
farms, and larger passenger ferries for example). Birds are
often killed when they collide with these structures and may
starve when grounded around them. It is likely that millions of
migrating birds are killed when they collide with illuminated
city buildings each year. There is a tendency to assume that
this kind of direct impact of artificial light on migrants is confined to nights when the conditions for migration are poor
because conditions are overcast. I have personal experience of
grounded birds around a fogbound lighthouse on a Scottish
island but anecdotal observations can do only so much to
advance our understanding of this potential problem.
The scale of the potential problem has been demonstrated by James McLaren and his co-workers who have
used data from weather surveillance radar to show that
birds migrating through northeastern USA are attracted to
the sky-glow above major urban areas. They have also established that as a result these birds are more likely to make
migratory stop-overs in sub-optimal habitat which will
almost certainly have an impact upon their fitness. Carrying
out experimental manipulations of the light levels experienced by birds during their migrations is particularly challenging, but if we are to understand the detail of the problem
(A)
and if necessary mitigate the effect of light pollution on
migrating birds, they are essential.
Benjamin Van Doren and his colleagues have taken
advantage of a unique ‘natural experiment’ to assess directly
the impact of bright city lights on the behaviour of birds
migrating over New York City (Figure 3.11). Their work
focused on the impact of the iconic light installation of The
National September 11 Memorial and Museum’s Tribute in
Light. The Tribute in Light consists of 88 searchlights
arranged close to the World Trade Centre, together they
produce two vertical beams of intense light that are visible
from a distance of some 60 miles. Van Doren combined
weather surveillance radar data together with acoustic and
visual monitoring of birds to compare the numbers and
behaviours of migrant birds in the sky above the Tribute in
Light on nights during peak migration when the tribute was
illuminated and not illuminated. When the searchlights were
switched on, the team found that even on nights with a clear
sky, very large numbers of birds congregated around the
beams, circling and calling, suggesting that they were disorientated. Over a period of seven nights across seven years
the team estimated that 1.1 million birds were directly
affected. This result is significant because it is possible that
as a result of being attracted to the light and then being
‘held’ around it (although the team’s data modelling
Tribute in Light
(B)
Sept 12, 2015 02:12
New York
off
Tribute
in Light
0 km1 km 2 km
(C)
500 birds
with 0.5 km
Sept 12, 2015 02:32
New York
Individual
migratory
birds
on
Tribute
in Light
15,700 birds
0 km1 km 2 km
with 0.5 km
Low
Number of birds
High
Figure 3.11 Migrating birds are attracted to the bright lights of the city. From Van Doren B.M., Horton, K.G., Dokter, A.M., et al. (2017)
High-intensity urban light installation dramatically alters nocturnal bird migration. Proceedings of the National Academy of Science 114(42),
11175–80.
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suggests that in this case at least birds possibly moved on
after around 30 minutes), birds may be more likely to collide
with buildings, be more susceptible to predation, become
exhausted, or be required to alter their stop-over behaviour.
When the beams were switched off these birds very quickly
dispersed and their calling rates decreased. This would suggest that by working with stakeholders it may be possible to
3.5 Navigation
We tend to think of migrants as having special status in terms of their navigational abilities. There is
something awe inspiring about the fact that an 8 cm
long passerine can return with pin-point accuracy
to its breeding area having first flown across the
best part of two continents to get there. But surely
the ability of a bird to relocate its nest again and
again during the course of the foraging day, or to
accurately relocate a cached seed in a complex habitat is equally amazing. At both scales these movements require the individual to navigate.
At the local scale there is evidence that birds
make use of visual landmarks, a class of navigation
involving spatial memory and referred to as piloting. The early evidence for this came from experiments in which homing pigeons were fitted with
frosted contact lenses prior to being released some
distance from their home loft. These birds, by the
means that we will discuss below, are able to return
to the general vicinity of the loft. But being unable
to see it they simply land and wait to be carried in.
Experiments involving a range of vertebrates have
shown that specific areas of cells in one region of the
brain, the hippocampus, are essential to tasks involving spatial memory. In rats a class of hippocampal
cells termed place cells have been shown to become
active in response to the animals encountering a specific landmark, or to groups of landmarks that have a
specific relationship to one another and to the spatial
position of the test animal. In pigeons hippocampal
lesions (which destroy these cells) disrupt the ability
of the birds to home even short distances over familiar ground. Such birds do set off in the right direction
so the hippocampus is not it would appear related to
compass sense, but they get lost en route, presumably
having lost their map sense. If the lesioned birds are
confined to their lofts for a sufficient period they will
65
mitigate the impact of light sources by managing their use at
times of peak migration.
Reference
McLaren, J.D., Buler, J.J., Schreckengost, T., et al. (2018)
Artificial light at night confounds broad-scale habitat use
by migrating birds. Ecology Letters 21(3), 356–64.
eventually regain their ability to home to it, but they
will never learn to home to a new loft. The hippocampal cells are clearly therefore involved in both
the acquisition and storage/retrieval of spatial information (see also Box 3.6).
But is the hippocampus involved in navigation
during migration? There are hippocampal differences between migratory and non-migratory bird
species (some migrants have larger hippocampi,
some have hippocampi that have more neurons
per unit volume), and differences are apparent
between species with different migratory strategies.
For example Semipalmated Sandpipers Calidris
pusilla and Spotted Sandpipers Actitis macularia
have similar numbers of hippocampal neurons, but
the Spotted Sandpiper has a larger hippocampal
formation and a greater number of hippocampal
microglia. These differences are correlated with
differences in migratory behaviour. Semipalmated
Sandpipers have a longer migration that crosses
large expanses of open water whereas the migratory journey of the Spotted Sandpipers is a shorter
and a visually more complex land-based route,
leading to a suggestion that the hippocampus has a
role in navigation at both the local and landscape
level where landmark recognition and learning are
important. There is currently however no concrete
evidence that the hippocampus has an important
role in navigation at the larger geographical scale.
Key reference
Bingman, V.P. and MacDougall-Shackleton, S.A. (2017)
The avian hippocampus and the hypothetical maps
used by navigating migratory birds (with some reflection on compasses and migratory restlessness). Journal
of Comparative Physiology A 203, 465–74.
Navigation at the larger scale, involving the types
of orientations and movements characteristic of
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ESSENTIAL ORNITHOLOGY
Box 3.6 Finding stored food
Important evidence for the key role of the hippocampus in
spatial memory comes from comparative studies of the foraging behaviour of passerine birds. The members of some
passerine species are well known for their ability to hide and
then retrieve seeds. This caching behaviour is obviously to
the advantage of the birds concerned. Caching allows them
to take advantage of a greater proportion of a food resource
than might be possible without storage. It may also provide
them with the food they need to live through the lean times,
but only of course if they can remember where they hid it.
David Sherry has shown experimentally that captive Blackcapped Chickadees Parus atricapillus can do just this. He provided birds with an opportunity to store sunflower seeds in
70 holes drilled into posts in an aviary. When the birds had
cached four or five seeds they were ushered out of the aviary
and Sherry cleaned it, removed the seeds and then covered
every one of the holes with an identical Velcro flap before
allowing the birds to return. In the wild chickadees are constantly on the move, lifting bark, turning leaves, and probing
crevices—opening Velcro flaps would be second nature to
them. So when they got hungry would the birds remember
where the seeds had been hidden and open the right stores?
Yes they did. They spent almost ten times as much time
exploring the holes in which they had stored seeds compared
to the sites they had not used. They were also far more likely
to visit a previous cache than an unused site. Taken together
these observations strongly suggest that the birds do remember where they have hidden food. Further work in the field
has shown that the birds only use each cache once, put just
one item of food into each cache and can remember where
they have hidden a seed for almost a month.
The role of the hippocampus in this context has been established via a range of studies but I think that one in particular
is worthy of some consideration, providing as it does an excellent example of the comparative approach in biology. Sue
Healy and co-workers have compared the foraging behaviour
and related brain structure of two species of European Parid
closely related to the Black-capped Chickadee. Their work
involved the Blue Tit Cyanistes caeruleus and the Marsh Tit
Parus palustris. Marsh Tits, like the chickadee, are avid food
storers. Individual birds are known to store up to 100 seeds in
a morning, and across the course of a typical winter will store,
and perhaps more importantly retrieve, literally thousands of
items of food. Blue Tits on the other hand do not store food
and given this fundamental difference in the foraging ecologies of the two species we might hypothesize that they will
have different spatial memory abilities and adaptations.
Specifically Healy and her co-workers have asked the question
do they have differently developed hippocampi?
In an attempt to answer this question the researchers have
compared the hippocampal volumes of birds of both species.
Consider first the data in Figure 3.12, which relates to juvenile birds of both species. The data show that when hippocampus size is expressed relative to the size of the telencephalon
(an area of the brain not related to spatial memory and therefore not expected to vary between these species) bigger
brained juvenile Marsh Tits do have a bigger hippocampus,
but so do bigger brained juvenile Blue Tits and size for size
there is no difference between them. This might seem to be a
disappointing result, but look at the figure again and this
time pay particular attention to the data collected from adult
birds. The hippocampus volume of the adult Blue Tits is no
different to that of either juvenile Blue Tits or juvenile Marsh
Tits, but that of the adult Marsh Tits is appreciably larger than
all of these. So why is there a difference in adults but not
juveniles? It seems that the juvenile marsh tits had not yet
had the opportunity to store food whereas the adult birds
had. In effect the juvenile Marsh Tits were behaving ecologically more like a typical Blue Ttit. It would appear therefore
that a larger hippocampus is related to spatial memory, but
that hippocampal enlargement is a response to food storing
behaviour rather than a prerequisite for it.
Reference
Sherry, D.F. (1984) Food storage by black-capped chickadees: Memory of the location and contents of caches.
Animal Behaviour 32, 451–64.
30
Hippocampal volume (mm3 )
66
Juvenile marsh tits
Juvenile blue tits
Adult marsh tits
Adult bule tits
20
10
0
0
100
200
300
400
500
Telencephalon volume (mm3 )
Figure 3.12 Adult Marsh Tits who have had experience of food
storing have a more developed hippocampus than do inexperienced
juvenile Marsh Tits or adult/juvenile non-storing Blue Tits. From
Healey, S.D., Clayton, N.S., and Krebs, J.R. (1994) Development of
hippocampal specialisation in two species of tit (Parus spp).
Behavioural Brain Research 81, 23–8. With permission from Elsevier.
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67
The Hague,
The Netherlands
Natural
wintering area
of Hague
Starlings
Recoveries of
adult Hague
Starlings released in
Switzerland
Switzerland
Recoveries of juvenille
Hague Starlings
released in
Switzerland
Figure 3.13 Recoveries of migrating juvenile (filled circles) and adult (open circles) European Starlings Sturnus vulgaris following their
translocation from the Netherlands to Switzerland. Adult birds compensated for their new start point, juveniles did not. Re-drawn from data in
Perdeck, A.C. (1958) Two types of orientation in migrating Starlings Sturnus vulgaris L. and Chaffinches Fringilla coelebs L., as revealed by
displacement activities. Ardea 46, 1–37.
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ESSENTIAL ORNITHOLOGY
migrations seem likely to involve two processes: a
compass orientation—often termed vector navigation and, a goal orientation which is often termed
true navigation. The distinction between these is
possibly best explained by reference to an example,
and in this case no discussion of the topic could be
complete without reference to the classic example
afforded by the work of Perdeck in the 1950s.
Perdeck captured more than 10,000 Starlings
Sturnus vulgaris, a mixture of adults and juveniles, in
the Netherlands at the onset of the autumn migration. Typically these birds would have undertaken a
relatively short south-westerly migration to winter
in the southern half of the United Kingdom and
along the northern coasts of Belgium and France.
The birds were marked so that their movements
could be tracked, and then transported almost 400
miles to the south-east prior to release in Switzerland.
During the following winter around one third of
these birds were relocated, having completed their
migration. But where had they gone? In fact as can
be seen from Figure 3.13, two types of movement
had taken place. Some of the birds had flown in a
north-westerly direction towards their traditional
wintering grounds, a few had even made it there.
Others had found novel wintering grounds in southern France and on the Iberian peninsula. The birds
had separated into two discrete populations according
to age; the juveniles had headed south-west while
the adults had flown north-west. Remember that
juveniles would not have previously migrated and
had no experience upon which to draw. Remember
also that earlier in this chapter we saw that the initial
migratory orientation is innate. So it would seem
that these birds were able to set off in the right direction using a compass sense, but lacking a map sense
they had no way of knowing that they were going to
the wrong place. This is an example of vector-based
navigation.
The adult birds on the other hand had presumably migrated to and from the traditional wintering
area at least once before, and in doing so had established a map sense which allowed them in some
way to establish a link between their current location and their ultimate goal. Translocated to
Switzerland they demonstrated true navigation and
were able to undertake a journey across unfamiliar
country to reach a familiar goal.
It seems likely that during their first migration
young birds learn their route and the locations of
their breeding and non-breeding areas with reference to cues from the environments around them.
With this acquired information they are then able to
develop their mental map and then to use it during
subsequent journeys. Several cues seem to be
important and it seems likely that when they are
available they are used in combination.
3.5.1 Navigational cues
The sun and the stars
Birds navigate by day and by night and use celestial
cues to enable them to do so. By day the sun is the
dominant cue and at night it is replaced by the stars.
That the sun can be used as a navigational cue was
first demonstrated by Kramer in the 1950s. In a
series of influential experiments he first established
the preferred orientation of starlings exhibiting
migratory restlessness (through the use of funnel
cages). He then positioned mirrors around the cages
in order to shift (from the point of view of the birds)
the position of the sun by 90° and found that the
orientation of the birds changed to compensate for
this. Further experiments have established that
the specific cue used is in fact the position of the
sun relative to the horizon, or more precisely the
position of an imaginary line from the sun to the
horizon referred to as the azimuth.
Of course the sun is not a stationary body. The
azimuth moves during the course of the day and so
birds using it for navigation must use a bi-coordinate
system that takes account of both solar position
and time. Clock shifted starlings, that is birds that
have been conditioned in captivity to be out of
‘sync’ with natural day time have been used in
experiments to demonstrate this. If starlings are
conditioned so as to be clock shifted by six hours
(so that at noon they ‘think’ that it is in fact 6 am)
they will demonstrate a 90° shift in their orientation. By this I mean that when tested against the
natural position of the sun at 6 am they will fly in
an inappropriate direction for the real time of day.
Because the azimuth moves by 15° per hour they
demonstrate the 90° shift and fly in a direction
more appropriate to a flight undertaken at noon.
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So it would appear that these birds do cross reference the position of the sun and time when direction finding.
At night the sun is no longer available and in its
place the stars are used instead. Experiments
involving funnel cages in a planetarium (so that
the star map experienced by the birds can be
manipulated) have shown that young birds
observe the apparent rotation of the pattern of
stars above them as the earth rotates beneath
them. In this way they learn the position of the
centre of the map, which in the northern hemisphere is Polaris, the North Star. This means that
once they have learned this they are able to correctly determine north as long as they can see that
star and some of those around it. With this information northern hemisphere migrants can fly
south (away from the star) in the autumn and
north (towards it) in the spring. But what happens
when clouds obscure their view? There is some
evidence that suggests that birds may choose not
to migrate on cloudy nights. Blackcaps Sylvia atricapilla and Red-backed Shrikes Lanius collurio
have both been observed to show migratory restlessness on cloudless nights but not under an
(A)
N
W
(B)
E
(D)
E
S
Days 5 and 8
The magnetic field
Homing pigeons have no problems finding their
lofts on sunny days when they are made to fly with
a bar magnet attached to them, but they lose the
ability to home when carrying the magnet on a
cloudy day. The magnet will cause a localized disruption of the magnetic field experienced by the
bird and so it seems likely that geomagnetism is
important in orientation (presumably the pigeons
are unaffected on sunny days because they are able
to utilize their sun compass).
The magnetic poles of the earth maintain a predictable magnetic field across the surface of the
planet with a south to north orientation. At the
poles the field dips towards the surface of the earth
at an angle of 90° and at the equator the angle is 0°.
Birds have been shown experimentally to be able
to detect this field, or more precisely to detect the
angle of dip of the field as it varies with latitude.
E
S
Days 1, 2, and 4
N
5
8
W
overcast sky. However, there is also considerable
evidence that birds make use of a range of other
cues to compensate for the ‘loss’ of the sun or the
stars because birds are able to orientate appropriately in the absence of a visible sky.
N
1
2
4
W
Control
(C)
69
N
10
10+
W
E
S
Day 10 and later
Figure 3.14 Migratory direction preferences of Silvereyes
prior to (control) and following exposure to a strong magnetic
pulse. It is clear that over time the disruptive effect of the
pulse wears off. From Scott, G.W. (2005) Essential Animal
Behavior. Blackwell Scientific, Cambridge.
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ESSENTIAL ORNITHOLOGY
This should in theory allow them to establish the
directions north and south, and to position themselves on the surface of the earth. Current evidence
suggests that birds may use the magnetic field in
two ways; as a compass to determine direction, and
as the basis of a map. Considering the compass
first, Wolfgang Wiltschko has shown that a strong
magnetic pulse is enough to disrupt the migratory
orientation of Silvereyes Zosterops l. lateralis. As
Figure 3.14 shows these birds usually follow a
southerly route from their non-breeding range on
the Australian mainland to their Tasmanian breeding grounds. A magnetic pulse disorientates them
for some days, but the data do suggest that they are
able to either recover from the disruption, or to at
least accommodate its effect after 10 days or so.
Such a disruption may be possible under natural
conditions as a result of a solar storm for example.
Ian Henshaw and colleagues have carried out
elegant experiments to investigate the use of a magnetic map by Thrush Nightingale Luscinia luscinia
on their migratory route from Sweden to southern
Egypt. These birds would typically pause before
crossing the Sahara and through hyperphagic
fuelling behaviour significantly increase their
body mass prior to the arduous desert crossing. The
researchers found that by altering the magnetic
field parameters experienced by birds to mimic
those experienced during migration they were able
to induce levels of hyperphagia and mass gain typical of birds about to cross the Sahara in birds that
were actually still in Sweden. These results suggest
that the birds were using magnetic field information as a map to determine their location and altering their behaviour accordingly.
So how do birds ‘read’ magnetic fields to determine compass direction and map position? Although
the details are not fully elucidated it seems likely that
two discrete mechanisms may be involved. It is
known that the sites of activity in the brain when
birds do respond to changes in magnetic fields are in
the visual system and that they can only be recorded
if the retina is intact and operational and if the bird is
exposed to particular wavelengths of light (specifically they appear to need light at the blue end of the
spectrum). Recent research by Anja Günther and her
co-workers suggests that in the European Robin
Erithacus rubecula at least, the magnetic compass sense
might be related to up-regulation (increased availability) of mRNA coding the protein Cryptochrome
4 (Cry4) in double-cone cells of the retina. Their
research recorded a significant increase in Cry4 activity during the migration season. Cryptochromes are
light sensitive proteins that form radical pairs, the
free electrons of which have different but correlated
spins as a result of photo-excitation. It seems likely
that through their interaction with the magnetic field
these radicals enable birds to perceive it in some
way. The magnetic map sense however seems likely
to be related to an as yet unidentified and undiscovered iron-based receptor located somewhere in
the neural architecture of the optical system.
Key references
Günther, A., Einwich, A., Sjulstok, E., et al. (2018) Doublecone localisation and seasonal expression pattern
suggest a role in magnetoreception for European Robin
Cryptochrome 4. Current Biology 28(2), 211–23.
Henshaw, I., Fransson, T., Jakobsson, S., et al. (2008)
Food intake and fuel deposition in a migratory bird is
affected by multiple and single-step changes in the
magnetic field. The Journal of Experimental Biology
211, 649–53.
Heyers, D., Elbers, D., Bulte, M., et al. (2017) The magnetic map sense and its use in fine-tuning the migration programme of birds. Journal of Comparative Physiology A 203(6–7), 491–7.
Following your nose
There is something special about the smell of seabird guano on a warm summer’s day. I appreciate
that it may not be to everyone’s tastes, but it is one
of my favourite smells, and it is an important smell
because research suggests that it helps seabirds to
relocate their colonies and even their individual
nests. Data have been available for some time that
suggest that homing pigeons learn the smell around
their loft and use it, among other cues, to relocate
home when they have been displaced by their
owners for racing purposes. Now Enrica Pollonara
and her colleagues have carried out experiments on
Scopoli’s Shearwaters Calonectris diomedea breeding
on a small island colony off the coast of Italy. The
researchers captured incubating shearwaters (taking
care to protect their eggs) and moved them to a release
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point some 400 km away (and 100 km offshore). Prior
to release, the birds were assigned to one of three
experimental groups and fitted with a data logger
that enabled the researchers to determine the route
they took back to their nest when they were eventually
recaptured. Some birds were simply tagged, relocated,
and released—these control birds were free to
behave normally. The other birds were subjected to
one of two experimental manipulations: some had
magnets attached to their heads to disrupt their
ability to use the earth’s magnetic field to navigate
by, and others were rendered anosmic. This means
that their ability to smell was temporarily removed
(the effect would last for just a few weeks).
71
As would be expected all of the control birds
were recaptured at the colony, back on their nests,
within a few days. Similarly all of the birds that
had magnets fixed to them were able to find their
way home suggesting that even if the magnetic
sense is important in the navigation of this species
there are other cues that can be used to excellent
effect. But compare their quite direct routes
home with flightpaths of the anosmic birds in
Figure 3.15. Without their sense of smell the birds
seem to be initially ‘lost’—wandering back and
forth around the release site before heading to an
adjacent coastline. Then the birds fly back and
forth along the coast until eventually something
(A)
(B)
(C)
(D)
Figure 3.15 The flight lines of Scopoli’s Shearwaters that had been displaced from their colony. Control birds (A) and birds fitted with magnets
to disrupt their ability to read the earth’s magnetic field (B) made relatively direct flights home. In comparison anosmic birds did not (C and D).
From Pollonara, E., Luschi, P., Guilford, T., et al. (2015) Olfaction and topography, but not magnetic cues, control navigation in a pelagic seabird:
displacements with shearwaters in the Mediterranean Sea. Scientific Reports 5, Article number 16486, 10.
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ESSENTIAL ORNITHOLOGY
changes and their flight becomes much more
direct. Still hugging the coast they fly back to the
island and their colony. The researchers interpret
this as suggesting that without smell the birds
cannot find their colony in a featureless sea. Once
they find the coast however, they are probably
able to use visual landmarks to navigate by and
although the route may be circuitous they do
eventually make it home.
Summary
Migration allows birds to make the most of the
resources available to them. It has a genetic component but is a response to environmental cues.
Migrating birds face numerous hazards and conservation of migrants relies upon efforts made in a
number of countries. Birds use a wide range of
navigational cues to facilitate their movements and
in some cases have excellent spatial memories.
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C H A PT ER 4
Eggs, nests, and chicks
‘The avian egg is a miracle of natural engineering’
Noble S. Proctor and Patrick J. Lynch (1993)
Eggs, particularly perhaps those of domestic fowl,
are something that we are probably all very familiar
with, but just how much do we know about them?
In this chapter I want to consider the egg from its
conception, through laying and incubation to hatching; and to think about chicks.
Chapter overview
4.1
4.2
4.3
4.4
4.5
4.6
4.7
4.8
Sex and the gonads of birds
The egg
Clutch size
Egg shell colouration and patterning
Nests
Incubation
Hatching
Chicks
4.1 Sex and the gonads of birds
Birds reproduce sexually; a male and a female copulate, sperm are transferred, an egg is fertilized
(internally) and assuming that all goes well a new
bird is the eventual result. Genetically this new
individual will be a combination of its parents having inherited half of its genetic material from each
of them.
As humans one of the chromosomes we inherit
from our father determines our sex. Human sex
chromosomes come in two types, labelled X and
Y. Our fathers (like all male mammals) have paired
sex chromosomes consisting of one X chromosome
and one Y chromosome and when their germ cells
divide at meiosis they produce gametes (sperm)
that have either an X or a Y. Male mammals are therefore described as the heterogametic sex. But our
mothers (and other female mammals) are homogametic, i.e. they have a pair of X sex chromosomes
and so their gametes are all the same (X). This of
course means that the sex chromosome that we
inherit from our mother will always be an X
chromosome, but from our father we may inherit
either an X or a Y. If our paternal sex chromosome is
a Y then we are male, if it’s an X we are female. Birds
too have one heterogametic sex and so sex is determined in the same way, but with two notable differences. The first is a difference in terminology—instead
of X and Y chromosomes birds have W and Z
chromosomes. The second difference is perhaps
biologically more significant; whereas in mammals
sex is determined by the material inherited from
male parents, in birds it is determined by the material
coming from the female because it is the female that
is the heterogametic sex having a ZW pair of sex
chromosomes (males have two Z chromosomes).
Chromosomes consist of a double helix of DNA,
specific sections of which act as templates for the
production of proteins. These protein coding sections are what we refer to as genes. Each individual
gene always codes for the same protein or part of a
protein (some are the product of a number of genes
working together) and so the expression of a particular gene will always affect the same character of
the organism’s behaviour, physiology, development, etc. The observable effects of the expression
of genes are an organism’s phenotype, but we
Essential Ornithology. Second Edition. Graham Scott, Oxford University Press (2020). © Graham Scott (2020).
DOI: 10.1093/oso/9780198804741.003.0004
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ESSENTIAL ORNITHOLOGY
Ovary
Infundibulum
Magnum
region
Ovum and
albumen
Ovum and
shell membranes
Isthmus
region
Uterus
region
Large intestine
Vestigial right oviduct
Vagina
region
Cloaca
Figure 4.1 The oviduct and the formation of eggs. After its release from the ovary, the egg typically takes 24 hours to develop fully: Spending
around 30 minutes in the upper area of the oviduct (the infundibulum); around 3 hours in the magnum region where it is coated with albumen; an
hour in the isthmus region where shell membranes are deposited; and, spending up to 24 hours in the uterus where the hard outer shell and
associated pigmentation is laid down. From Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology: Avian Structure and Function. Yale
University Press, New Haven.
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should not think of phenotype (be it behaviours
observed, physiological characteristics or plumage
colour) as being solely determined by genotype.
Phenotypes also depend upon the environment in
which they are expressed, something that we will
return to later in this chapter.
The genes found on the Z and W chromosomes are
referred to as being sex-linked. For example, only a
female bird can have any of the genes that are found
solely on the W chromosome, so these genes are
linked to being female. We are only beginning to
understand the specific details of the impact of sexlinked genes upon the development and life of the
individual but in chapter 5 we will consider one
exciting example of the clear link between a sexlinked gene and sex specific development, bird song.
of the female and ejaculates directly into her. In the
passerines the male cloaca does swell and protrude
during the breeding season and this may serve to
increase the efficiency of sperm transfer. In a similar
way some species of duck and members of a small
number of other families develop a penis-like
protuberance that is involved in copulation.
After transfer, sperm swim from the area of the
female cloaca towards the top of the oviduct, to the
infundibulum and ovary, where the mature ovum is
fertilized (Figure 4.1). In some species females have
special storage organs around the junction of the
vagina and uterus where sperm may be retained in a
viable state for some days or even weeks prior to
their release which is timed to coincide with ovulation. The significance of this is discussed in chapter 5.
Flight path: Development and control of bird song.
Flight path: sperm storage and breeding strategies.
page 105.
page 95.
Although the details have yet to be determined, it can
be assumed that the basic genetic difference between
male and female birds also in some way determines
the differentiation of their tissues into gonads that are
either male (testes) or female (ovaries). Males have a
pair of internal testes which produce sperm. These
are enlarged during the breeding season but shrink
away to almost nothing during the rest of the year.
Females of most bird species have only one developed ovary (usually the left one), although there are
exceptions and the females of some species of bird of
prey do have two ovaries (although they may not
both be functional). As in the case of the male testes,
the female ovary is far larger during the breeding season than it is during the rest of the year. Presumably
this seasonal development of gonad tissue is of
benefit to birds that have to carefully balance their
body mass to maximize their flight efficiency.
Flight path: seasonal modification of tissue mass,
flight efficiency, and migration. page 62.
Birds on the whole do not possess an external sex
organ such as the mammalian penis and copulation
is usually a very brief affair lasting just seconds,
although it can last for 25 minutes in the case of the
Aquatic Warbler Acrocephalus paludicola. Both males
and females have a cloaca, and during copulation
the male places the opening of his cloaca over that
75
4.2 The egg
In their excellent Manual of Ornithology Nobel
Proctor and Patrick Lynch refer to the egg of a bird
as ‘. . . a miracle of natural engineering. Light
and strong, it provides everything a developing
bird embryo needs.’ And this quote does I think
sum up an egg perfectly.
Key reference
Proctor, N.S. and Lynch, P.J. (1993) Manual of
Ornithology: Avian Structure and Function. Yale
University Press, New Haven.
Essentially the egg is a zygote, a fertilized ovum,
sitting in a relatively huge store of nutrients and
encased in a protective shell. But as Figure 4.2 illustrates, there is rather more to it than that.
Flight path: Yolk volume correlates with chick
developmental strategy. page 96.
At the centre of the egg is the yolk, rich in fats, proteins, and other nutrients. The yolk may comprise as
much as 70 per cent of the content of an egg in the
case of the Brown Kiwi Apteryx australis, or as little
as 20 per cent in the case of small passerines. When
we crack open an egg to cook it the yolk appears to
be a relatively uniform yellow body but in fact if
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ESSENTIAL ORNITHOLOGY
Germinal spot
(blastodisc)
Yellow yolk
White yolk
Shell
Outer shell membrane
Inner shell membrane
Dense albumen
Chalaza
Air space
Chalaza
Light (thin)
albumen
Figure 4.2 The internal anatomy of a generalized bird’s egg. From Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology: Avian Structure
and Function. Yale University Press, New Haven.
prepared properly its real structure can be seen and
it is revealed as being a series of alternating layers
of nutrient-rich yellow and less rich white yolk.
These layers are built up over a period of days as
the yolk is formed and the difference in their colour
is an indication of differences in nutrient availability (layers laid down at night are less nutrient-rich).
So, just as we can age a tree by its growth rings, we
can determine yolk age (or at least measure the time
taken for its development) by counting the layers
within it. The developing embryo (beginning as a
group of germ cells termed the blastula) sits on top
of the yolk. Specifically it sits on top of a column of
white yolk and because white yolk is less dense
than yellow yolk this column ensures that as the
egg rotates, the embryo (and the white yolk under
it) floats to retain its position above the yolk mass
rather than underneath it. The yolk is contained
within the vitelline membrane to maintain its integrity and is held in place by the chalazae, gelatinous
albumen structures which allow the aforementioned yolk rotation but limit its movement otherwise. To facilitate the uptake of nutrients from the
yolk and to permit the exchange of gases with the
environment, the developing embryo produces two
extra-embryonic membranes. One of these, the yolk
sack, is a vascularized sheath surrounding the yolk
and acting as a kind of external stomach, allowing
the embryo to absorb nutrients directly from the yolk.
Shortly before hatching the yolk sack is absorbed
into the body of the chick and it may serve as a
nutrient reserve to enhance its chances of survival
during the first few days after leaving the egg.
As embryonic development progresses, the chick
absorbs the calcium needed for bone growth from
the shell of the egg, thereby weakening it and presumably increasing the ease with which the chick
will be able to crack it when the time comes.
The second membrane, the chorioallantois, develops on the inner surface of the egg shell, eventually
covering most of it. This highly vascularized membrane provides for the transport of oxygen into, and
carbon dioxide and excess water vapour out of the
embryo. These gases enter and leave the chorioallantois and the egg via pores in the outer shell.
The yolk is surrounded by the albumen, commonly referred to as the white of the egg because of
the transformation that it undergoes on cooking;
changing as it does from an almost transparent gel
to a white solid. If you fry an egg sunny side up
you will notice that there are two layers of albumen, a dense inner layer in contact with the yolk
and a less dense outer layer. Consisting of around
90 per cent water and 10 per cent protein, the
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albumen is the water reserve for the developing
chick. The albumen layer also acts as a physical
cushion, protecting the embryo from sudden jolts
as the egg moves, and as an insulating membrane
reducing the cooling of the yolk and embryo when
incubation is interrupted.
The outer shell of an avian egg is composed of a
number of discrete layers, the most obvious being
the hard outer layer of calcium carbonate crystals
arranged in a lattice of flexible collagen fibres. This
gives the shell the strength that it needs to bear
the weight of an incubating parent, the resilience
required as it is jostled against other eggs in the clutch,
and against its surroundings (remember that not all
eggs are laid into a comfortable nest, some such as
those of cliff nesting seabirds are laid directly onto
unyielding rock). Beneath this outer layer are two
flexible inner membranes to which the brittle outer
layer adheres, further contributing to the overall
stability of the shell. The innermost shell membrane
is in direct physical contact with the vascularized
chorioallantoic membrane through which embryonic
respiration takes place. To facilitate the transport of
gases into and out of the egg, the shell has permanently
open pores allowing the inner membranes of the egg to
communicate directly with the external environment.
Most birds lay eggs at the rate of one per day for
a fixed period (depending upon clutch size, the
determination of which is discussed later in Box 4.1).
There are of course exceptions—some birds lay
every other day, and as an extreme the Masked
Booby Sula dactylatra lays the two eggs in its clutch
six or seven days apart. The reason for the inter
egg interval probably relates in part to the time it
takes for an egg to be produced (see Figure 4.1) and
the need on the part of female birds to maintain
flying efficiency, carrying one almost fully formed
egg is probably a sufficient burden in the context
of aerodynamics.
Key reference
Bolund, E., Schielzeth, H., and Forstmeier, W. (2009)
Compensatory investment in zebra finches: females
lay larger eggs when paired to sexually unattractive
males. Proceedings of the Royal Society of London:B
276, 707–15.
Female birds do it seems have some control over the
size and quality of the eggs that they lay. Elisabeth
77
Bolund and her colleagues have demonstrated that
when they are paired with a low quality mate,
female Zebra Finches increase the volume of the
eggs that they lay and increase the carotenoid content of their yolks. In essence they lay better eggs.
This is presumably an attempt by them to offset the
poor genetic quality (low attractiveness) of their
mate by giving their offspring a bit of a head start.
4.3 Clutch size
Female albatrosses invariably lay a single egg whilst
the clutch of a Blue Tit Cyanistes caeruleus can have
as many as 17 eggs in it. There is clearly therefore
considerable variability in clutch size. Females of
some species are extremely limited in terms of the
variation in clutch size that they can achieve (e.g.
female Spotted Sandpiper Actitis macularis always
lay four eggs, the implications of which are discussed in chapter 5). On the other hand the females
of many species are able to vary the number of eggs
that they lay between nesting attempts/seasons. In
these cases the question ‘how big should a clutch
be?’ is one that has been a focus of considerable
interest to ornithologists.
General patterns of variation in clutch size have
been described and interpretation of these does
allow the formulation of some apparently straightforward explanations for the phenomenon. For
example the clutches, and therefore broods, of altricial species (whose young are highly dependent
upon their parents) tend to be smaller than those of
precocial species (with young that are quite independent). It seems clear that in these cases the ability of the parents to feed, brood, and protect the
chicks is a key determinant of clutch size. It has also
been noted that species utilizing open nests have
smaller broods than those with a more secure cavity
nest. Presumably the increased protection from predation afforded by a cavity nest is important, but it
is also possible that open nest broods are smaller to
enable faster fledging and so minimize predation
by cutting short the risky period during which
chicks are in the nest. There must also be a heritable
component to clutch size, after all artificial selection
for increasing ‘clutch size’ has allowed humans to
develop varieties of domestic fowl that are able to
lay an egg a day almost all year round.
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Early observations of clutch size took the view
that the number of eggs laid by a female should be
the same as the maximum number of young that
could be successfully reared during a breeding
attempt, after all to produce more eggs than this
would be a waste of resources, to produce fewer
would be a waste of opportunity. Field-based observations suggest that in fact clutches are most often
slightly smaller than would be expected. This disparity between theoretical and actual clutch size
can be explained if, rather than considering a single
breeding season, the prediction is made that the optimal clutch size will be the one that allows a female
to maximize her productivity over her lifetime. In
effect by producing slightly fewer eggs in any one
clutch, females are ensuring that they will have
the reserves/survivorship potential to lay further
clutches in future.
Goran Högstedt, who noted that the clutches laid
by individual females of the Swedish Black-billed
Magpie Pica pica population that he studied, varied
in size between five and eight eggs, provides evidence for this kind of subtle brood manipulation. To
test the idea that these females somehow ‘knew’
what the optimal number of eggs to lay was, he
manipulated brood sizes over three breeding seasons. Some broods were not manipulated and these
females were allowed to rear all of the chicks that
they hatched. Some females had their brood size
reduced, and the newly hatched chicks that were
removed from them were used to increase the
broods of others. The data presented in Figure 4.3
show that in all cases the optimum clutch size (the
one resulting in the most chicks still alive at the point
of fledging) was the same as that laid by the female.
Through further work Högstedt was able to show
that the main factor determining clutch size was, in
this population, territory quality and that at some
level females were able to relate territory quality to
clutch size and consistently lay the optimum clutch.
Figure 4.3 also highlights some of the consequences
of not laying the optimal clutch; lay too many or too
few eggs and productivity will decline. This story
will be returned to in chapter 5 when we consider
Magpie parenting behaviour.
A number of hypotheses have been proposed to
explain the evolution of clutch size in species that
Initial clutch size laid
5
Number of young fledged
78
8
4
3
7
2
6
1
5
4
5
6
7
Experimental brood size
8
Figure 4.3 Experimental manipulation of brood size demonstrates
that female Magpies Pica pica consistently lay that number of eggs
that their territory can support. From Högstedt, G. (1980) Evolution of
clutch size in birds: adaptive variation in relation to territory quality.
Science 206, 1148–50. Reprinted with permission from AAAS.
have a capacity to lay varying numbers of eggs during a single breeding attempt. Initially it was suggested that clutch size was determined by food
availability (Ashmole’s hypothesis), the idea being that
females with access to less food during the breeding
season would be restricted in the number of eggs
that they could lay, or that they would be able to rear
fewer young (or both). Numerous studies have provided support for this resource availability hypothesis
demonstrating that increased food availability
during the breeding season is directly related to
increased productivity, and/or that seasonal food
shortages during the period prior to breeding results
in increased adult mortality. Increased adult mortality in turn leads to reduced competition during the
subsequent breeding season and a relative increase
in available resources enabling larger clutches.
However, there are other potential explanations for
variation in clutch size. For example, a number of
hypotheses have been proposed suggesting that
variable predation risk (nest, fledging, and adult
predation) can explain variable clutch size. These
predation risk hypotheses suggest that the likelihood of
adult or young birds/eggs being predated both
have an impact upon optimal clutch size. This is
because larger broods require adult birds to visit
them more often to provide food to developing
chicks and as a result both adults and nests might be
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more conspicuous to predators. Therefore, in areas
of high predation risk, optimal clutch sizes should
be smaller to minimize visit rates and thereby minimize the chances that adult birds or eggs/nestlings
will be killed and eaten.
But how to tease apart the relative importance of
these hypotheses? Ornithologists typically adopt
one of two approaches to a question like this one.
In some cases they carry out an experiment to test
predictions of the hypotheses in the case of one or
a small number of study species. Alternatively
they determine the significance of complimentary
or competing hypotheses through an interrogation
of a large comparative data set. An example of the
former is the work undertaken by Kristen Dillon
and Courtney Conway who have conducted an
elegant experiment involving a population of Redfaced Warblers Cardellina rubifrons inhabiting the
mountain ranges of Arizona. The researchers
observed that across their range the clutches of
these birds varied from five eggs at lower elevations to three or four eggs at higher elevations.
Based upon their knowledge of the species and the
area, they hypothesized that invertebrate food
available to the warblers might decrease with altitude but also that levels of predation risk might
increase. So in this case both the resource availability
hypothesis and the predation risk hypothesis might
influence clutch size.
To test the relative effects of resource (food) availability and perceived predation risk upon clutch
size, Dillon and Conway designed an experiment
that enabled them to manipulate both in a controlled way and counted the numbers of eggs laid
by birds subjected to each experimental condition.
To vary food availability they simply provided
some birds with additional food in the form of trays
of wax moth larvae placed close to their nests. To vary
perceived predation risk a caged Cliff Chipmunk
Tamias dorsalis was placed in the territory of some
birds for a short period each day. In total four
experimental treatments were applied: a control
condition (no manipulation); increased food availability; increased predation risk; and, increased
food availability plus increased predation risk.
Their results revealed that increased food availability during breeding did not result in a change in
clutch size compared to the control treatment. So in
79
this case they found no direct support for the
resource availability hypothesis but it is important to
bear in mind that because these warblers are
migrants it is possible that resource availability
prior to breeding does have some effect. However,
the clutches of birds exposed to the caged chipmunk were on average smaller than those of birds
that were not subjected to an increased perceived
predation risk (and the same size as the clutches of
birds exposed to the chipmunk and given extra
food). So in this case at least it would appear that
the predation risk hypothesis best explains the
observed variation in clutch size (Figure 4.4).
Key references
Martin, T.E. (2014) A conceptual framework for
clutch-size evolution in songbirds. The American
Naturalist 183, 313–24.
Harmáčková, L. and Remeš, V. (2017) The evolution of
clutch size in Australian songbirds in relation to
climate, predation and nestling development. Emu
Austral Ornithology 117(4), 333–43.
̌ ová and Vladimír Remeš have
Lenka Harmáck
adopted a different approach to understanding the
factors driving the evolution of clutch size. They
have explored a data set containing life history information of 313 species of Australian Passeriforme
songbirds and used it to test a number of hypotheses
including the resource availability hypothesis and the
linkage between resources, seasonality and latitude,
and the predation risk hypothesis and an extension of it
(Martin’s hypothesis) that they describe as the fledgling development gradient. Martin’s hypothesis suggests that whereas increased predator risk should
result in smaller clutch sizes (as described previously) in those cases where nest predation is highest,
young birds should fledge early to minimize risk
(and as a result will leave the nest at an under developed state being less heavy and with only part grown
primary feathers). This means that adult birds must
compensate by expending more energy provisioning
mobile, dependent fledglings that are themselves at
risk of predation. As a result, the interaction of juvenile mortality, level of fledgling development, and
resource availability determines clutch size. In
essence species with young that spend longer in the
nest should lay bigger clutches (when adult body
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ESSENTIAL ORNITHOLOGY
Control
Chipmunk
Supplemental Food
Supp.Food + Chipmunk
4
Clutch Size
5
3
10
5
0
10
5
0
10
5
0
10
5
0
Figure 4.4 Female Red-faced Warblers provided with extra food lay clutches that are similar in size to control birds. Birds that have an increased
perception of predator risk lay smaller clutches. Dashed lines indicate average clutch sizes. From Dillon, K.G. and Conway, C.J. (2018) Nest
predation risk explains variation in avian clutch size. Behavioural Ecology 29(2), 301–11, by permission of Oxford University Press.
size is taken into account). From the results of their
̌
analysis, Harmácková
and Remeš conclude that in
Australia at least, although clutch size does generally
increase with latitude (something that has also been
observed in the northern hemisphere), they did not
find any evidence to support the resource availability
hypothesis, nor did they find evidence to support the
predation risk hypothesis. However, they did find some
evidence to support Martin’s hypothesis suggesting
that some interaction of local resource availability
and age-specific predation risk may explain the relative clutch sizes of Australian songbirds, but exactly
what factors exert the most influence on clutch size
may vary across the globe.
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4.4 Egg shell colouration and patterning
4.4.1 Camouflage
Eggs are quite simply beautiful objects. Their form is
particularly pleasing to the human eye for some reason, and the diversity of their colours and patterns is
quite amazing. There are two components to egg
shell colour–the base colour (usually white, pale
brown, or pale blue, but deep reds, blacks, and
greens are also found), and the pattern (streaks, spots
or blotches in a range of colours that are usually, but
not always, darker than that of the base). The natural
beauty of eggs sparked a frenzy of egg collecting and
their study (oology) during the Victorian period.
Over the period of their academic study a host of
explanations as to the significance of their colour and
pattern have been proposed. These are very well
summarized by Underwood and Sealy in their contribution to the monograph Avian Incubation.
As a student I was told that the colour of an egg was
an adaptation to facilitate camouflage. This, it was
explained, was why white eggs were laid by cavity
nesting birds and why patterned eggs were laid by
birds that had open nests (with the colour and pattern matching the habitat around the nest). There
may be some truth to this in that some eggs are
camouflaged—personally I have often had great
difficulty in locating the nests and greenish/brown
mottled eggs of Oystercatcher Haematopus ostralageus despite their being laid on open ground in
nothing more elaborate than a scrape (Figure 4.5).
In my local Oystercatcher population the eggs are
‘lost’ amongst the gravel mix of the upper shore on
which they are laid.
However, not all eggs that are laid in the open
are camouflaged and not all cavity nesters lay white
eggs. So whilst this explanation might explain the
colouration of a proportion of eggs, it is insufficient
as an explanation of the colouration of all eggs. The
camouflage explanation for egg colour is one of a
Key reference
Underwood, T.J. and Sealy, S.G. (2002) Adaptive
significance of egg colouration. In Avian Incubation.
Deeming, D.C. (ed.) Oxford University Press, Oxford.
Figure 4.5 Although obvious when pointed out, this Oystercatcher nest containing a clutch of three eggs was particularly difficult to locate on
the shore (© Graham Scott).
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family of explanations that ascribe a signal function
to the appearance of the egg (the cryptic pattern is
effectively a dishonest signal to a predator). Others
in this family of explanations include the evolution
of patterns to facilitate egg recognition by incubating parents and/or the evolution of patterns to
signal female quality (presumably to male birds).
4.4.2 Egg mimicry
In an attempt to stay one step ahead of the competition some brood parasites such as the Cuckoo
Cuculus canorus lay eggs that accurately mimic those
of their host, thereby making their discrimination
and rejection harder. At the population level, female
Cuckoos lay eggs of a range of colours and patterns
but each individual female lays only one type and
preferentially parasitizes only one or a small number
of the wide range of hosts available. Those that she
chooses are the ones with eggs most similar to her
own. This host specificity is thought to be genetically
controlled and sex-linked to the W chromosome.
There is experimental evidence to support the utility
of this egg mimicry in that in a range of host/parasite pairs, hosts have been found to reject a higher
proportion of non-mimetic than mimetic eggs.
4.4.3 Egg recognition
Recognition of one’s eggs is likely to be important
in two key situations: when trying to find them in a
crowded colony; and, when trying to separate them
from others laid alongside them within a clutch. In
the former case it is important that incubating birds
are able to discriminate between their own eggs and
those of their neighbours in a colony. In many colonies the eggs of open nesting birds are laid in very
close proximity to one another and although birds
returning to incubate are likely to gain information
from a variety of cues relating to nest position in the
colony and perhaps directly from their partner, if it
is in attendance at the nest, the ability to recognize
one’s own eggs is clearly important. It has been
shown experimentally that Guillemot are able to
discriminate between their own egg and those of
their neighbours on a crowded cliff ledge because
they recognize the colour and blotch pattern of their
own particular egg.
Egg recognition is also important in the reduction
of the impact of brood parasitism, the behaviour by
which a female lays her eggs in the nest of another
bird. Brood parasitism can occur between individuals of the same species (when it is more usually
referred to as egg dumping), but is probably better
known as an interspecies activity. Brood parasitism
in the traditional (interspecific) sense is a comparatively rare breeding strategy found in less than
1 per cent of bird species but having evolved in a
broad range of taxa, notably the cowbirds Icteridae,
whydahs Viduidae, honeyguides Indicatoridae,
and the cuckoos Cuculidae. It is also exhibited in a
number of species that have precocial young (quite
independent at hatching), often as part of a wider
reproductive strategy that does involve incubation
of own young. So for example brood parasitism
amongst the various species of duck Anatidae is
widespread and with one exception all of the species involved do most commonly rear their own
young. The exception in this case is the Blackheaded Duck Heteronetta atricapilla which is an
obligate brood parasite (i.e. it never rears its own
young) and has been recorded laying its eggs in the
nests of 18 different species including gulls, ibises,
herons, coots, rails, and even birds of prey.
Flight path: Brood parasitism is just one of a wide
range of reproductive strategies, page 97.
Egg dumping is common, for example, amongst
some species of colonially nesting African weaver
birds Ploceidae, females of which occasionally lay
an egg in the nest of one of their neighbours. This
might be to their advantage as both an insurance of
their output against the risk that their own nest will
suffer predation and as a means by which they can
increase their total productivity. Of course from the
viewpoint of the recipient of the dumped egg,
investment in the incubation and rearing of the
young of another pair is not an advantage, it reduces
the investment that can be made in one’s own
young. Weaver egg patterns are very diverse, perhaps as an adaptation to increase the ability of
females to recognize their own eggs and enable
them to remove those of their competitors. Some
weaver bird species are the hosts of the Diederik
Cuckoo Chrysococcyx caprius, a brood parasite in the
traditional interspecific sense of the term, laying its
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Box 4.1 When does it pay hosts to accept brood parasites?
predation rates (as do unparasitized eggs) and the most
likely predator in this case is the cowbird.
Hoover and Scott interpret their findings as follows: When
they reject a cowbird egg, warblers induce a high price—a
visit from the cowbird and predation of their clutch. It therefore pays them to accept the egg in a scenario that is somewhat like a mafia protection racket! By predating warbler
nests the cowbirds act as ‘farmers’ inducing the laying of
second clutches which provide new parasitism opportunities.
(A)
Nest predation (%)
80
60
40
20
0
(B)
Warbler offspring/nest
Natural selection seems to favour those host birds able to
recognize and eject the eggs of brood parasites. Numerous
examples of the ‘arms-race’ between the egg mimicry ability
of the parasite and egg recognition abilities of the host have
been described. But it seems that there may be instances
when the parasite can get the upper hand and it will pay the
host to accept the cost of rearing the cuckoo in the nest.
Jeffery Hoover and Scott Robinson have carried out an
elegant series of experiments involving the relationship
between Brown-headed Cowbirds Molothrus ater and their
Prothonatory Warbler Protonotaria citrea hosts. In this system, unlike that of other brood parasites, hosts raise the
alien chick alongside their own brood—paying an energetic
cost and producing weaker chicks as a result.
The researchers wanted to investigate two interesting
hypotheses: That the cowbirds may ‘farm’ their hosts, i.e.
induce parasitism opportunities; and, that the warbler hosts
may be ‘intimidated’ into accepting parasitism by the consequences of not doing so. In essence they suspected the parasites of mafia-like behaviour—punishing those warblers
that ejected their eggs by returning to destroy their clutches.
To test their ideas Hoover and Robinson established a
nest-box breeding population of warblers in an area frequented by cowbirds and carefully monitored nesting
attempt outcomes. They noted parasitism rates and manipulated parasitized nests. Some they allowed to develop naturally but from some they removed the cowbird egg. Some,
but not all, of these manipulated nests then had their
entrance hole reduced to permit warbler access whilst
excluding cowbirds.
Look carefully at the results of the experiment (Figure 4.6).
Treatments 3, 4, and 5 show that in ideal conditions (no
parasitism or egg removed but no possibility of a return to
the nest by the cowbird) a Prothonatory Warbler pair might
expect to raise three or four chicks per breeding attempt,
and that these nests were rarely predated. Treatment 3 also
reveals a cost to the warblers of accepting the parasite in
that warbler productivity is lower in these nests than in the
nests of treatments 4 and 5. The cost paid by accepting the
parasite (about one chick) is however far lower than that
paid by birds that reject the egg (treatment 1)—who on
average raise only one of their chicks. These nests suffer high
1
2
3
4
Treatment category
5
1
4
2
3
Treatment category
5
5
4
3
2
1
0
Figure 4.6 The figures show predation rates (A) and warbler
success (B) in each of five experimental treatments. Under treatment
1 cowbird eggs were removed and cowbirds were allowed
subsequent access to the nest. Treatments 2 and 5 include all nests
that were not parasitized (in 2 cowbird access would be possible, in
5 it would not). Under treatment 3 the cowbird egg was accepted
by the warblers, and cowbirds always had access to the nest. Under
treatment 4 the cowbird egg was removed and access to cowbirds
subsequently denied. From Hoover, J.P. and Scott, K. (2007)
Retaliatory mafia behaviour by a parasitic cowbird favours host
acceptance of parasitic eggs. Proceedings of the National Academy
of Science 194(11), 4479–83. Copyright (2007) National Academy
of Sciences, USA.
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eggs in the nest of another species and leaving its
young to be raised by these unwitting foster parents. It is possible therefore that egg recognition by
weavers is also a strategy to minimize the effect of
this behaviour. Cruz and Wiley provided compelling evidence to support this argument when they
reported that a population of Village Weaver Ploceus
cucullatus, introduced to the Caribbean island of
Hispaniola, lost most of their egg recognition ability
during the 200 years of brood parasite-free existence that they enjoyed prior to the establishment of
a population of Shiny Cowbird Molothrus bonariensis. After just 16 years of coexistence with this brood
parasite the discriminatory ability of the weavers
had almost completely returned.
Key reference
Cruz, A. and Wiley, J.W. (1989) The decline of an
adaptation in the absence of presumed selection
pressure. Evolution 43, 55–62.
4.4.4 Signals of quality
Egg colouration may also be a signal used by males
to judge the quality of a female and of her offspring.
Juan Moreno and co-workers have shown that the
eggs of a Spanish population of Pied Flycatcher
Ficedula hypoleuca vary in the intensity of their bluegreen colouration (measured in terms of the intensity
of their reflectance of light in the blue-green region of
the visible spectrum); eggs are similar within a
clutch, but variation between clutches is marked.
The blue-green colouration of the eggs of this species
is a result of the deposition in the matrix of the shell
of the pigment biliverdin. This pigment has antioxidant properties and is positively correlated with
immunocompetence in adult birds. It is likely that
only healthy females will have a sufficient surplus of
biliverdin to produce really blue-green eggs. Egg
colour could therefore be a signal of female health
status or quality, but what evidence is there that
males actually take note? To explore this question the
researchers made observations of male provisioning
rates at nests of known egg colour type (they also
cross-fostered clutches to ensure males really were
responding to egg colour and not to laying female
behaviour or other cues). They found that males made
more provisioning visits to the nests containing the
most colourful eggs so they did invest more in the
chicks of healthy females (presumably these females
produce healthy chicks). Thus it is possible that egg
colour was used as a cue by males.
Key references
Moreno, J., Morales, J., Merino, S., et al. (2006) More
colourful eggs induce a higher relative paternal
investment in the pied flycatcher Ficedula hypoleuca:
a cross fostering experiment. Journal of Avian Biology
37(6), 555–60.
Martínez-de la Puente J., Merino, S., Moreno, J., et al.
(2007) Are eggshell spottiness and colour indicators of
health and condition in blue tits Cyanistes caeruleus?
Journal of Avian Biology 38, 377–84.
On the other hand José Martínez-de la Puente
and co-workers have demonstrated a correlation
between egg shell patterning and a measure of low
female quality in the Blue Tit Cyanistes caeruleus.
Blue Tit eggs are white with red-brown spots that
are the result of the incorporation of protoporphyrins in the matrix of the shell. The presence of these
pigments in the shell seems to be a consequence
of elevated protoporphyrin levels in the laying
female. These pigments are oxidants rather than
anti-oxidants and at elevated levels they can indicate and even cause poor health in the adult bird.
Specifically the researchers have shown that
females in poor body condition, indicated by their
having a higher cellular level of a protein HSP70
which is known to be linked to stress, laid spottier
eggs. So perhaps increased patterning is a means by
which females can rid their bodies of excess protoporphyrins and improve their own health status.
There is no evidence currently that male Blue Tits
respond either positively or negatively to this
potential signal.
4.4.5 Pigments and shell quality
An alternative explanation of the significance of
protoporphyrin pigments in passerine egg shells has
been proposed by Andrew Gosler and co-workers.
Their study involved working with the eggs of a
population of Great Tits Parus major, which like
Blue Tits have a white egg patterned with brown
spots. Birds in their study population (at Wytham
Woods near Oxford, UK) laid rounder, spottier eggs
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(A)
85
(B)
Figure 4.7 A Great Tit clutch (A) and eggs from five clutches to illustrate their variability (B). The eggs shown here in ‘columns’ are from five
separate clutches and the ‘rows’ are the first (top), middle, and last (bottom) eggs of the laying sequence in each of them (© Andrew Gosler).
if their territories were low in calcium, and more
elliptical, less spotty eggs if their territories were
high in calcium (Figure 4.7).
Key reference
Gosler, A., Higham, J.P., and Reynolds, S.J. (2005) Why
are birds’ eggs speckled? Ecology Letters 8 1105–1113.
The significance of these observations seems to be
that the brown spots are coincident with thinner
(less calcium rich) areas of the shell, and spottier
eggs therefore had generally thinner shells. A thinner shell is a weaker shell and this might explain the
recorded difference in egg shape because a rounder
egg is stronger than an elliptical one. This difference
in shell quality can be easily explained. Female
birds must obtain calcium from their environment
and in a calcium-poor environment they will produce poorer eggs. But what about the spots? Being
coincident with thinner areas of shell it is presumed
that they play an important structural role and act
as strengthening agents.
Of course it is possible that the potential health
status signal and egg shell strengthening roles of
protoporphyrins are not mutually exclusive—birds
low in calcium might be in generally poor condition, producing poor quality eggs.
4.5 Nests
Nests are the places and structures where eggs are
laid and incubated. The most simple nest of all is
really no more than a ‘nest-site’—a suitable patch of
largely unmodified bare ground/wood onto which
an egg is placed. Many species of wader for example
lay their eggs directly into a shallow depression or
scrape on the ground (see Figure 4.5). Similarly cliff
nesting auks such as Guillemot Uria aalge and
Razorbill Alca torda lay their eggs directly onto what
seem to be the narrowest of rock ledges. The housekeeping in establishing these simple nests may
involve the rearranging or removal of materials, but
no real construction takes place. However, when we
think of a nest we are more likely to imagine a
clutch of eggs nestling in a cup that has been built
by a bird from a range of suitable materials. You
probably have a mental image now of a cup with a
strong outer casing woven from twigs and strong,
thick grasses within which nestles a smaller cup
lined with soft down feathers? This is one kind of
nest, but in fact the variety of nests, nest locations,
and nesting materials is so enormous that it is
beyond the scope of an introductory text such as
this and I would recommend that the interested
reader consult Mike Hansell’s excellent book Bird
Nests and Construction Behaviour. Nests are placed
within cavities or burrows; stuck to vertical surfaces
with mud, faeces, and saliva (Figure 4.8); they float
‘tethered’ to emergent vegetation; they hang over
water; they are placed in vegetation at ground level,
in shrubs and in tree-tops (Figure 4.9). Some are so
small that females straddle them rather than sitting
on them when incubating eggs and others are so
large that their weight can bring down the tree in
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ESSENTIAL ORNITHOLOGY
Figure 4.8 The mud nest of the Red-rumped Swallow Hirundo
daurica (© Robin Arundale).
Figure 4.9 The intricately woven nest of a weaver bird (Ploceidae)
(© Graham Scott).
which they have been built (the huge colony nests
of some social species of African weaver bird for
example).
Key references
Hansell, M. (2000) Bird Nests and Construction
Behaviour. Cambridge University Press, Cambridge.
Deeming, D.C. and Reynolds, S.J. (eds) (2015) Nests,
Eggs and Incubation: New ideas about avian
reproduction. Oxford University Press, Oxford.
The primary function of a nest is to provide a safe
place in which eggs can be laid and incubated and
where, in the case of altricial species, chicks can be
safely reared. Nests tend to be quite messy places
and so nest hygiene is important (Box 4.2). In
order for the embryo inside to develop, eggs must
be kept warm. In fact the eggs of most species
require a fairly constant temperature of around
38ºC (100ºF) and above ambient humidity (to prevent water loss from the egg through the porous
shell). Relatively few birds experience such temperatures in their environment and for those that
do environmental temperatures are likely to fluctuate to too great an extent to make ambient incubation a possibility. Australasian megapodes do of
course practice environmental incubation, burying their eggs under mounds of earth and organic
matter, which as it decays releases the steady heat
that they require. The majority of species however
practice direct incubation with parent birds ‘sitting’ on the eggs until they hatch. In many cases
both sexes share incubation duties, but there are
numerous examples of female only incubation
and more rarely examples of male only incubation. Birds are able to influence incubation temperature and humidity in a number of ways. They
may simply choose a nest site that is likely to provide the conditions required (or make it easier
to achieve them). As an example, in their edited
volume, Charles Deeming and Jim Reynolds
describe the fact that Palestine Sunbirds Cinnyris
osea typically position their nests so that the opening faces away from the prevailing wind in order
to prevent cooling of the eggs, and in shade (rather
than full sun) to minimize fluctuations in ambient
temperature. Birds are also able to vary the materials that they use when constructing their nests to
accommodate local conditions. In a comparative
study Vanya Rohwer and James Law have analysed the properties of the nests of Yellow Warblers
breeding in two different parts of their Canadian
range. They found that those birds breeding in
Manitoba built larger, less porous nests with more
insulation than those built by birds breeding in
Ontario. This is significant because the Manitoba
climate is colder and windier than that of Ontario
(which is wetter), and so in Manitoba nests that
are windproof and well insulated are best, whereas
in Ontario too much insulation would hamper
drying.
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Box 4.2 Nest hygiene
Many birds attempt to maintain nest hygiene by defecating
over the lip of the nest, although this can make nests conspicuous and perhaps for this reason the chicks of many passerines
produce discrete faecal pellets that are collected and ingested
or carried away for disposal by the parent birds. This copraphagy
may seem unpleasant to us, but it has been shown to make a
significant contribution to the nutrition of some breeding birds.
To further maintain nest health some species regularly add fragrant green vegetation to their nests It has been suggested
that the volatile chemicals given off by these plants may act as
insecticides or arthropod deterrents and by including them
birds may be able to limit the harmful effects of nest parasites.
For example, Adèle Mennerat and her co-workers have shown
that Blue Tit chicks raised in nests with aromatic plant fragments have higher blood haemocrit levels than those raised in
nests without added vegetation. Haemocrit levels are related
to the oxygen-carrying capacity of the blood and are an indicator of general health, so it does seem that there is a benefit to
the addition of this material to the nest in that it may in some
way enable birds to better withstand parasite attack.
In Mexico City House Sparrows Passer domesticus and House
Finches Carpodacus mexicanus have found a novel way to
utilize nicotine and other chemicals from the tobacco plant to
maintain nest health. Farmers use the same chemicals to protect
poulty from ectoparasites. On the streets of Mexico City birds
have a ready supply of pre-packaged repellent in the form of
cigarette butts. Constantino Macías Garcia and his colleagues
explored the relationship between the amount of material from
cigarette butts in the nests of birds and the numbers of
ectoparasites in those nests. They found that nests with more
cigarette material had lower ectoparasite loads (Figure 4.10),
but also that material from butts that had been smoked
appeared to be more effective than unsmoked material, perhaps because burning releases higher levels of the pesticide.
Furthermore, in a subsequent experiment the researchers demonstrated that house finches actively add butts to nests when
the researchers had added extra live ticks suggesting that the
incorporation of the pesticide is a response to an actual parasite
load and that the birds are in effect ‘self medicating’.
References
Mennerat, A., Perret, P., Bourgault, P., et al. (2009) Aromatic
plants in nests of blue tits: positive effects on nestlings.
Animal Behaviour 77, 569–74.
Suàrez-Rodríguez, M. and Macìas Garcia, C. (2017) An
experimental demonstration that house finches add cigarette butts in response to ectoparasites. Journal of Avian
Biology 48(10), 1316–21.
no. ectoparasites in the nests
100
75
50
25
0
5
10
weight of cellulose from cigarette butts (g)
Key reference
Rohwer, C.G. and Law, J.S.Y. (2010) Geographic
variation in nests of yellow warblers breeding in
Churchill, Manitoba, and Elgin, Ontario. The Condor
112(3), 596–604.
Flight path: Reproductive strategies vary between
species. page 97.
15
Figure 4.10 House Sparrow (black circles) and House Finch
(grey circles) nests that include more material from cigarette
butts typically contain fewer ectoparasites. From SuàrezRodríguez, M., López-Rull, I., and Macìas Garcia, C. (2013)
Incorporation of cigarette butts into nests reduces nest ectoparasite load in urban birds: new ingredients for an old recipe?
Biology Letters 9(1), 20120931.
4.6 Incubation
Incubation periods vary greatly—the eggs of some
species of African weaver bird (Ploecidae) hatch in
just nine days, whereas those of some penguin species take 65 days, and those of kiwis can take an
amazing 85 days to hatch.
A few days before the onset of incubation physiological changes occur in the parent bird. Levels of
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ESSENTIAL ORNITHOLOGY
the hormone prolactin circulating in the blood
stream increase and at the same time levels of circulating testosterone decrease. This hormone shift is
thought to be a trigger for the onset of incubation
and parenting behaviours and for a reduction in the
performance of behaviours related to territoriality
and courtship. All of these behaviours will be further discussed in chapter 5, but at this stage I do
want to briefly describe the development in the
incubating bird of a specialized ‘organ’ to facilitate
the transfer of body heat to the egg. Feathers on
the lower breast and belly are lost (they drop out or
are pulled out, and may then be used in nest insulation) and the bare skin beneath them swells with
fluid. The blood vessels beneath this skin dilate
thereby increasing blood flow to this region. This
brood patch as it is termed (Figure 4.11) is concealed
by the contour feathers in a non-incubating bird,
but as it settles onto the nest, the feathers are drawn
back such that the hot skin of the patch makes direct
contact with the eggs. The brood patch is a temporary feature of incubating birds and once the eggs
have hatched and the developing brood no longer
need to be warmed it shrinks away and the feathers
regrow when the bird next moults.
By adjusting the position of eggs in the nest
(Figure 4.12) and by raising and lowering their
body over the eggs, birds can control their temperature and in extremes of heat some species of open
nesting bird stand above the eggs to give a parasol
Figure 4.11 The unfeathered belly skin of this female European
Goldfinch Carduelis carduelis is stretched taught and heavily
vascularized to create a brood patch (© Chris Redfern).
Figure 4.12 This Oystercatcher has just adjusted the position of her eggs and is settling down to continue their incubation (© Graham Scott).
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Box 4.3 Birds, eggs, and agricultural chemicals
The second half of the twentieth century began with a global
expansion in and intensification of agriculture. This involved a
worldwide increase in the application of new pesticides and
herbicides, designed to boost crop yields by decreasing populations of crop pests and competitors. There are even pesticides
designed to directly target bird species in soft fruit growing
areas. However from the ornithologists perspective perhaps the
most notorious of these chemicals were not those intended to
control birds but those which had an indirect impact upon them.
During the 1950s and 60s marked declines in numbers of
birds of prey were recorded throughout the countries of the
developed world. Adult birds were found to have died for no
apparent reason (they were not the victim of trauma for
example), and clutches of eggs were found broken and/or
abandoned. In 1970 Derek Ratcliffe published a keystone
paper in the Journal of Applied Ecology in which he demonstrated that the main cause of the population declines was
breakage of eggs in the nest, a phenomenon that he showed
to have arisen quite suddenly in the mid/late 1940s. After
making measurements of shells laid during the period of the
decline, and comparing them with collected eggs from earlier
in the century, he proved that the increase in egg breakage
coincided with a sudden change in the quality of egg shells, in
simple terms the shells of the eggs had become thinner
2.30
2.20
2.10
Eggshell index
Weight (mg)
L(mm) x B(mm)
2.00
1.90
1.80
1.70
1.60
1.50
1.40
1.30
1.20
1.10
1.00
0.90
1900
1910
1920
1930
1940
1950
1960
1970
Year
Figure 4.13 Note that eggshell thickness for UK Peregrine Falco peregrinus remained fairly constant during the period 1900–1945 but
that during the post-war years (1945–1970) shells became considerably thinner on average. This was coincident with increased use of DDT.
Adapted from Ratcliffe, D. (1970) Changes attributable to pesticide in egg breakage frequency and eggshell thickness in some British birds.
The Journal of Applied Ecology 7, 67–115.
continued
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Box 4.3 Continued
(Figure 4.13). Ratcliffe’s paper did more than just demonstrate
the incidence of thinning. It also provided correlational evidence
to support the idea that the most likely cause of the thinning
was an accumulation in the birds concerned of residues of
organochlorine pesticides such as DDT which had come into
widespread use in the period 1946–1950. Subsequent experimental work has confirmed that the breakdown products of
organochlorines (DDE from DDT, HEOD from dieldrin and
aldrin, and PCBs) do all impact upon the calcium metabolism
of birds thereby directly causing egg shell thinning.
Having identified organochlorine pesticides as a main
factor in the decline of bird populations, many governments
legislated against the general use of organochlorines and
against the use of DDT, aldrin and dieldrin in particular (they
were banned in the UK in 1986 for example). But has it done
any good? Well thankfully it has. Take for example the case
of the Merlin Falco columbarius a small raptor common
throughout North America and northern Europe. It is a bird
that is known to have suffered egg shell thinning and
reduced breeding success throughout its range. Ian Newton
and colleagues have shown that in the case of the British
Merlin population legislation has probably saved them from
the brink of extinction. By the 1980s their numbers had
fallen to just 500 or so pairs in the whole of the British Isles,
just ten years later the population had more than doubled to
an estimated 1300–1500 pairs. This increase coincided with
both a fall in the detectable levels of organochlorines, such
as DDE, in eggs from failed broods and an increase in an
index of egg shell quality approaching the pre-1946 level
(Figure 4.14).
So have we as a society learned a valuable lesson from
this potentially disastrous episode? The answer to that question is a qualified yes. It took decades to recognize the issue
relating to organochlorine use, decades for positive remedial
action to be taken and only now, decades later, are we seeing the full benefit of those actions (and it should be remembered that high levels of these chemicals in the environment
are still having their effect in a number of parts of the world).
But as a society we continue to rely upon the introduction
of chemicals into the environment to solve our agricultural
problems and all too often we come to realize their negative
environmental impacts only in the face of a catastrophe.
Take for example the sudden and dramatic demise of the
worlds vultures during the opening years of the twenty-first
century. Populations of some vulture species declined
massively between 1990 and 2000; numbers of Oriental
1.3
1.2
Shell index
90
1.1
1.0
0.9
1960
1970
1980
Year
1990
2000
Figure 4.14 Shell index (thickness) values for UK Merlin Falco
columbarius have increased during the post-DDT era, almost
returning to pre-DDT levels (index c. 1.25). Reproduced from
Newton, I., Dale, L., and Little, B. (1999) Trends in organochlorine
and mercurial compounds in the eggs of British Merlins Falco
columbarius. Bird Study 46, 356–62, with permission of BTO.
White-backed Vulture (Gyps bengalensis) on the Indian subcontinent fell by a staggering 95 per cent for example. Initial
speculations suggested an epidemic specific to vultures
might be to blame, but very quickly diagnostic tests revealed
that a pollutant was the causal agent. Specifically, in 2004
Lindsay Oaks and co-workers demonstrated that the antiinflammatory drug Diclofenac was causing renal failure in
the birds. This drug was in widespread use in the treatment
of domestic livestock. When treatment was unsuccessful
livestock carcasses were simply left to be scavenged by the
vultures; the birds ingested the drug and died as a result. By
2006, just two years later, India had announced its intention
to ban the use of Diclofenac in an attempt to halt the decline
of vulture populations and hopefully protect these birds from
extinction. In the years that have followed vulture friendly
drugs such as Meloxicam have been developed as alternatives to Diclofenac and captive breeding programmes of the
most affected vulture species have been established in an
attempt to boost populations. It would appear therefore that
although we have not yet learned to avoid such mistakes
completely, we have learned to identify them and respond to
them positively more quickly.
Reference
Oaks, J.L., Gilbert, M., Virani, M.Z., et al. (2004) Diclofenac
residues as the cause of vulture population decline in
Pakistan. Nature 427, 630–33.
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E G G S, N E S T S, A N D C H I C K S
effect—if this is insufficient they make a trip to a
local water supply, wet their breast feathers and
then return to drip cooling water directly onto the
eggs. In heavy rain birds spend less time away from
their nests than on dry days, presumably to keep
their eggs dry and prevent chilling. You will recall
that at the time of laying, the embryo within the egg
is little more than a cluster of cells on the surface of
the yolk (Figure 4.1). As incubation progresses these
cells repeatedly divide and differentiate and the
embryo becomes recognisably a bird.
4.7 Hatching
You will recall from Figure 4.2 that within the egg
there is an air space. This is particularly significant
during the period immediately prior to hatching.
Once it has fully developed, the chick begins to push
with its beak against the membrane of the air space.
This marks the beginning of hatching—a process
that is thought to be triggered when the chick has
quite simply outgrown its space. Specifically the
onset of hatching coincides with increased hypoxia
and hypercapnia, i.e. the chick is simply not able to
take up enough oxygen, or expel enough carbon
dioxide via the chorioallantoic respiratory system,
and in effect it needs to hatch before it suffocates. To
assist it the chick has two temporary anatomical
features related to hatching. One is an overly developed hatching muscle (more properly termed the
complexus muscle) at the back of the head and neck
that provides the extra strength needed to break out
of the shell. The other is the egg tooth, a sharp process at the tip of the upper mandible of the beak that
is used to pierce the air space membrane. Once the
air space is broken into, the chick begins to use it
lungs to breath air directly. The chick uses the egg
tooth to scrape the inner surface of the shell and by
a combination of scraping and pushing it eventually makes a tiny hole. By repeating this process,
and at the same time rotating the egg, the chick
eventually weakens the shell sufficiently to cut off
the cap and break out.
Interestingly the protoporphyrin pigments of
brown speckled eggs that were discussed in an earlier section of this chapter may be important in
hatching too. If you remember there is a suggestion
that these pigments play a strengthening role in
91
thinner areas of shell. In fact the qualities of the
pigment/shell matrix that strengthen it against
forces from outside of the egg may in fact operate
in reverse against forces from within—effectively
making it easier for the chick to break the shell. In
the Great Tit it has been noted that maximum areas
of pigmentation coincide with the shoulder of the
egg—the area first breached by the chick.
The process of hatching (or pipping as it is sometimes called) can take anything from a few hours in
the case of a small passerine, to a few days in the
case of some of the larger birds. Often the chick completes the process unaided but there are examples of
a helpful parent assisting in the final stages of the
break out. Having hatched, parental assistance is
almost always essential. Newly hatched chicks are
exhausted, wet, and extremely vulnerable to
predators. As a minimum parents brood chicks until
they dry, but the extent of the care that they provide
beyond that will vary from species to species.
4.8 Chicks
Newly hatched chicks demonstrate a range of levels
of development. At one extreme the chicks of
Australasian megapodes (Megapodiidae), hatching
from eggs that have been incubated for a prolonged
period in a mound of compost or fermenting vegetation, require no parental care. They hatch feathered
and are able to fly almost at once. They are also able
to thermoregulate and to forage for themselves. Such
chicks are classed as being superprecocial. At the
other extreme are the newly hatched chicks of the
passerines (Box 4.4). Hatching blind, naked, and
helpless these altricial chicks rely entirely upon their
parents for warmth, food, and protection. Interestingly
it has been suggested that such helplessness is only
possible because passerines have evolved the ability
to construct a complex nest which protects chicks
from predators and from inclement weather.
Between these two extremes there are various
grades of precocial/altricial development. In his
review of the subject Starck suggests that eight
different classes of chick can be recognized: the
superprecocial, three grades of precocial chick,
semiprecocial and semialtricial, and two grades of
altricial development which differ principally in
therate of their growth.
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ESSENTIAL ORNITHOLOGY
According to Starck’s classification precocial chicks
are mobile and sighted upon hatching and require
varying degrees of parental care. For example the
chicks of ducks and pheasants follow their parents
and are protected by them. They are initially downcovered and so must be brooded by a parent to survive cold/wet weather, but like megapodes’ chicks
they are able to feed themselves from hatching. The
precocial chicks of coots and rails are very similar to
those of pheasants but they are initially unable to
find their own food and so must be fed by their
parents (who place food in front of hungry chick
and demonstrate pecking behaviour to them).
The semiprecocial chicks of most gulls and terns
are down-covered and fed/brooded by their parents at the nest (Figure 4.15). However, when threatened they will leave the nest that is typically quite
exposed, and run/swim for cover, returning to the
nest when it is safe to do so. Interestingly, but perhaps not surprisingly, the young of cliff nesting
Kittiwakes Rissa tridactyla differ from those of their
gull cousins in that when danger threatens them
they do not flee the nest (a bad thing to do if you
live on a cliff face!). Instead they crouch in the nest
cup and as a result of their cryptic plumage can be
(A)
(B)
Key reference
Starck, J.M. (1993) Evolution of avian ontogenies. In
Current Ornithology Power, D.M. (ed.) Plenum Press,
New York.
Figure 4.15 (A) These newly hatched semiprecocial Arctic Tern Sterna paradisaea chicks will stay in their nest for only a few days (© Ian Grier).
(B) In contrast, these altricial Cormorant Phalacrocorax carbo chicks will be nestbound for several weeks (© Les Hatton and Shirley Millar).
Box 4.4 Speed is of the essence but there is a price to pay
Typically during the early summer I am able to assign the
passerine birds that I catch as part of my data collection to
one of two age classes. Juvenile birds (those that have
hatched and fledged during the preceding weeks) typically
have very loose and fluffy body feathers whereas the body
feathers of adult birds (birds at least one calendar year old)
tend to be more substantial. In essence these juvenile
feathers could be thought of as being less good quality.
Given that I stressed the importance of good quality feathers in chapter 2, the question that you may be asking
yourself is why should this be the case? What explains this
difference in the structure of these feathers? This is exactly
the question that Lea Callan and her colleagues at Cornell
University and the US Geological Survey, Montana set out
to answer.
Specifically the researchers tested the hypothesis that
loosely textured juvenile feathers are the result of a trade-off
that takes place during the nestling phase between growth
rate and risk of predation. Essentially they asked the question: do some juvenile birds have loosely textured feathers
because the risk of being predated whilst in the nest is a
greater potential fitness cost of fledging with them, and
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E G G S, N E S T S, A N D C H I C K S
suffering an associated cost of say, poorer thermoregulation
or reduced flight efficiency, for example.
To test their hypothesis the research team studied 123
altricial species and measured the quality (the number of
barbules per centimetre of rachis) of the flank feathers of
adult birds and of juvenile birds a few days after they had
left the nest. In some species juvenile feathers were very
different to those of adult birds, and in other species the
feathers of the two age categories were not easily
distinguishable from one another.
It might have been expected that birds in warmer places
would have had lower quality (more open) feathers because
the pressure to retain body heat is lower. Or perhaps those
species that do not undergo a post-juvenile moult and so do
not replace their feathers prior to migration would have
(A)
more adult-like feathers. But the analysis did not support
either of these ideas. What the team did determine was that
species that spend a longer time in the nest grew more
adult-like feathers compared to those that fledge at an earlier stage (Figure 4.16A). For 67 of the species that were
included in the analysis, the researchers had access to information about relative nest predation rates and when that
data was included in the analyses it was found that species
suffering the lowest rates of nestling predation grew the
most adult-like feathers (Figure 4.16B). These results confirm
that increased nestling predation risk is an important selective pressure that drives rapid chick growth and early fledging, but at a cost. Faster growth results in less good feather
quality, but presumably the fitness benefits of early fledging
outweigh this cost.
(B)
juv ad
juv ad
1.0
0.8
0.7
0.6
0.9
0.8
0.7
juv ad 0.6
juv ad
b
1.0
Feather structure
Feather structure
0.9
Feather structure
a
1.0
0.9
0.8
0.7
0.6
0.5
0.5
0.00
10
15
20
25
30
Time in the nest (days)
0.02
0.04
0.06
Daily rates of nestling predation
–0.03
–0.01
0.01
0.03
Daily rates of nestling predation
controlling for time in the nest
Figure 4.16 (A) The feathers of nestlings that spend longer in the nest are higher quality in both tropical and temperate species, and
those of tropical species are on average of lower quality than those of temperate species. Figure 4.16(B) The indirect (a) and direct (b) effects
of nest predation risk on feather quality. (a) shows the indirect effect because predation risk is strongly correlated with time spent in the
nest. (b) shows a direct effect because even taking into account the effect of time in the nest, those species at high risk of predation still
grow less adult-like feathers. From Callan, L.M., La Sorte, F.A., Martin, T.E., and Rohwer, V.G. (2019) Higher nest predation favours rapid
fledging at the cost of plumage quality in nestling birds. The American Naturalist 193(5), 717–24.
quite difficult to see. These chicks would be classed
as being semialtricial.
Summary
Eggs permit the external development of young,
allowing female birds to maximize output without
compromising flight. Females routinely lay optimally sized clutches although clutch size, location
of nest, and incubation vary greatly from species to
species. In some cases birds do not care for their
own young and such egg dumpers/cuckolds are
involved in an evolutionary arms race with their
hosts. Some chicks are independent soon after
hatching, others depend upon the care of their parents for some time. As eggs and chicks, young birds
are particularly vulnerable to predation and to the
consequences of pollution.
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C H A PT ER 5
Reproduction
‘The dunnock’s sex life is an arrangement of huge complexity.’
Mark Cocker (2005)
In chapter 4 I outlined the basic sequence of events
from the laying of an egg to the hatching of a chick.
In chapter 5 I want to explore the diverse mating
systems exhibited by birds in more detail and to
consider behaviours such as courtship and territoriality that precede egg laying, and those that follow
hatching during the raising of chicks to independence.
Chapter overview
5.1
5.2
5.3
5.4
5.5
Males and females are different
Mating systems
Courtship and mate choice
Song
Raising a family
5.1 Males and females are different
Males and females are different. I made the point in
chapter 4 that the gonads of males and females differ, and of course associated with that difference
their gametes, the products of the gonads, also
differ. Male gonads produce millions of sperm (the
male gamete) at each ejaculation even though only
a small number need reach the egg (the female gamete) to ensure successful fertilization and most of
the sperm produced are destroyed or ejected by
the female. This may seem to be a wasteful process,
but it is necessary for a number of reasons. As
we will see later in this chapter the males of some
species compete with one another to monopolize
opportunities to mate (pre-copulatory competition),
but in other species females are promiscuous and
post-copulatory competition (competition between
sperm after insemination, see Box 5.1) becomes more
important. In birds at least it also appears that there
is an advantage associated with a higher number of
sperm reaching the site of fertilization. Although in
mammals penetration of the egg by many sperm
(polyspermy) is damaging to the ovum, research
conducted by Nicola Hemmings and Tim Birkhead
on Zebra Finch Taeniopygia guttata and domestic
fowl has demonstrated that in birds a level of polyspermy is advantageous. Their results suggest that
penetration by too few sperm results in reduced
embryonic survival. They have also shown that if
fewer sperm are inseminated a greater proportion
than expected reach the ovum. This suggests that
some mechanism exists which allows females to
regulate the numbers of sperm that are destroyed,
ejected, or ‘allowed’ to proceed. Why are birds and
mammals different? Hemmings and Birkhead suggest that the answer to that question might be
related to the fact that while a mammalian egg is
typically fertilizable for up to 24 hours, a typical
avian egg has a window for fertilization of just 15
minutes and so perhaps polyspermy is necessary to
ensure a sufficient number of sperm reach the ovum
in good time.
Key reference
Hemmings, N. and Birkhead, T.R. (2015) Polyspermy
in birds: sperm numbers and embryo survival.
Proceedings of the Royal Society B: Biological Sciences
282, 20151682.
Essential Ornithology. Second Edition. Graham Scott, Oxford University Press (2020). © Graham Scott (2020).
DOI: 10.1093/oso/9780198804741.003.0005
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Box 5.1 Sperm competition
the existence of within-female competition between the
sperm of different males and the potential consequences of
extra-pair copulations (EPCs). The results of some of these
experiments are summarized in Figure 5.2.
The first experiment (Figure 5.2A) was designed to simulate a situation in which a single female mates with two
males, switching rapidly between them but mating with
each in turn. In this case the result was that the second male
(and last to mate with the female) fathered the majority of
the eggs that were laid. The second experiment (Figure 5.2B)
simulates the situation in which a female that mates regularly with her mate (the first male) is involved in just one
extra-pair copulation with the second male (significantly this
EPC is the last copulation in the mating sequence). Again the
figure shows that even this single mating by the second
male results in his fathering the majority of the eggs that are
laid. Taken together these two experiments demonstrate
sperm competition and a significant feature of this system—
last male precedence.
The third experiment (Figure 5.2C) demonstrates the
effectiveness of a well known male strategy presumed to
reduce the impact of EPCs and last male precedence—
retaliatory copulation. In this experiment each male copulates with the female once, but these copulations follow one
another almost immediately (simulating the situation in
which a male might observe his mate copulating with a rival
The realization that a female bird might mate with more
than one male during a reproductive cycle has resulted in a
dramatic shift in the way in which ornithologists perceive
competition between males to pass on their genes. Prior to
this paradigm shift pre-copulatory competitive behaviour
was presumed to be the means by which male precedence
was determined. However we now know that sperm competition, a post-copulatory phenomenon, is widespread and
highly significant.
We saw in chapter 4 that at copulation sperm are transferred from the male to the female and that they must then
travel through the oviduct to the infundibulum in order to
fertilize the egg. Not all of the transferred sperm make this
journey. Some of them enter sperm storage tubules at the
junction of the uterus and vagina (see Figure 4.1, chapter 4)
where they can remain viable for periods of many days.
Sperm from these tubules can be released to fertilize eggs
produced over several days without the need for further
copulation. Tim Birkhead and his co-workers at the University
of Sheffield have established that in the case of the Zebra
Finch Taeniopygia guttata around 10 per cent of eggs laid
13 days after the last copulation have been fertilized
(Figure 5.1).
Birkhead and his colleagues have also investigated the
effect of multiple male matings upon the paternity of eggs
laid by a female. Their work has demonstrated very clearly
100
% Eggs fertile
80
60
40
20
0
0
2
4
6
8
10
12
14
16 >16
Days after last possible copulation with fertile made
Figure 5.1 Egg fertilization levels decline with time following a copulation event but stored sperm may remain viable for up to 13 days.
From Birkhead T.R. and Møller A.P. (1992) Sperm competition in birds: evolutionary causes and consequences. Academic Press, Copyright
Elsevier, Netherlands. Data from Birkhead, T.R., Pellat, J.E., and Hunter, F.M. (1988) Extra-pair copulation and sperm competition in the zebra
finch. Nature 334, 60–2.
continued
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Box 5.1 Continued
Experiment:
A
B
C
Probability of fertilization
1.0
1st Male
0.5
2nd Male
0
p<0.001
p<0.001
NS
Figure 5.2 The outcomes of experiments (A, B, and C) to investigate sperm competition in the Zebra Finch expressed as the proportion of
eggs fertilized by each of two competing males (see text for explanations of individual experiments). From Birkhead, T.R. and Møller,
A.P. (1992).
or might infer a recent copulation having witnessed his
female return from the territory of a rival). In this case the
data presented demonstrate that retaliatory copulation is an
It is also significant that following ejaculation, stores
of sperm can be quickly replenished and so males are
in theory capable of multiple matings and could
potentially sire large numbers of offspring during a
period of reproductive activity. Sperm are therefore
often thought of as being relatively inexpensive to
produce and each individual sperm is in itself probably not a particularly significant investment on the
part of the male. Eggs on the other hand are relatively
large and they are relatively expensive to produce.
Eggs are also in finite supply and so each of them has
significant value to the female, representing as it does
one of a very limited number of reproductive opportunities available to her. This fundamental difference
in gamete size is termed anisogamy and it is important because the reproductive strategies of birds (and
other animals) are largely a consequence of it.
Flight path: the relationship between the genetic
make-up of the sexes and their behaviour, page 73.
effective means by which a male might reduce the impact of
an EPC because both males fathered a similar proportion of
the eggs that were laid.
Concept
Anisogamy
Males and females have different sized gametes.
Those of males (sperm) are small, mobile, and relatively
inexpensive. Those of females (eggs) are relatively large,
immobile, and expensive.
In basic terms we presume that all individuals seek
to maximize their own reproductive output by
which we mean that they seek to pass on as many
copies of their own genes as possible. We can therefore assume that individuals of both sexes behave
in a way that will maximize their reproductive success in terms of both the quantity of offspring produced and/or the quality of those offspring. As a
result of anisogamy it is the case that males and
females can probably maximize their reproductive
output in different ways. Because a male can mate
repeatedly, taking advantage of his easily replenished store of cheap sperm, we might reasonably
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REPRODUCTION
assume that males can most easily increase their
output by fathering as many young as possible.
Females on the other hand cannot usually adopt the
same strategy. They are constrained by a limited
supply of eggs, and by the fact that there is a delay
between successive ovulations. For a female therefore the most effective way to maximize reproductive output is for her to maximize the quality of her
young. Females should therefore be expected to be
choosy about their mates, seeking to maximize the
quality of the contribution made by the male parent
in terms of either the quality of his genetic material
or of the resources that he is able to provide.
One further consequence of the differences between
male and female birds is that although actual sex
ratios may be close to 1:1 (i.e. there are the same numbers of males and females of a species present in a
population), operational sex ratios may depart from
this significantly. This is because once a female bird
has successfully mated she is likely to be unavailable
for mating with another male because of the time she
spends laying her fertilized egg and then in the majority of cases because she will then invest time and
energy in the successful incubation and rearing of her
eggs and chicks. During this period of time the male
is not similarly constrained and may be free to seek
another mate. As a breeding season progresses therefore the operational sex ratio of the population will
skew towards the relatively numerous males and
away from the available females. In effect, females
can be thought of as being the rarer sex. Charles
Darwin recognized that anisogamy is one of the phenomena underpinning the process of sexual selection,
an important evolutionary force, by which the members of the rarer sex can be choosy about their mates,
and those of the more common sex will be forced to
compete at some level for access to mates.
necessary to consider both the social basis of the
relationship between parent birds (do they work
together to raise young or does one partner desert
the other for example) and the genetic relationships
between offspring and social parents (i.e. the birds
which rear them but are not necessarily their biological parents). Table 5.1 provides a brief description of the main avian mating systems, many of
which are described in more detail in section 5.3.
The fidelity unto death of a pair of birds has often
been presumed as being a given truth. On the basis of
this commitment pairs of birds are often used as a
symbol of fidelity in human society (St Valentine’s
day has bird associations for example). However, the
advent of genetic paternity analysis has revealed that
in fact socially monogamous birds are often quite
promiscuous. A brood of apparent full siblings might
in fact be sired by several males. Why should this be?
Remember that male birds can maximize their reproductive output by fertilizing as many eggs as possible, and during that period of time when a female is
incubating her eggs, her male partner will often seek
matings with other females presumably to increase
the number of offspring that he sires. Females on
the other hand are limited in their ability to increase
the number of offspring that they produce and so
would be expected to focus on the production of
Table 5.1 Avian mating systems
System
Main features of system
Social
monogamy
One male and one female cooperate to raise a brood
of young. Genetic monogamy describes the situation
in which these birds are both the genetic parents of
the chicks being raised.
Polygyny
A male bird sires the offspring of a female and then
deserts her (temporarily or permanently) to seek
other females with which to mate. Deserted females
raise young alone or with reduced help from a
returning mate.
Polyandry
A female bird abandons her eggs to be raised by her
male partner (this male is not always the genetic
parent of the brood that he will raise). Deserting
females may seek to mate with further males in the
same breeding season.
Polygynandry
A group of males and females cooperate to rear
young. The resulting broods are produced by several
females and sired by several males.
5.2 Mating systems
Although some species of socially monogamous
(one male and one female) birds may be genetically
monogamous i.e. no extra-pair copulations (EPCs),
more than 85 per cent of those species that have been
subjected to DNA paternity studies have been found
to be sexually polygamous (multiple males and or
females contributing genetic material to a single
brood). So when thinking about mating systems it is
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ESSENTIAL ORNITHOLOGY
fewer higher quality offspring. It has been suggested
that females could seek EPCs for a number of reasons.
Perhaps they need to increase the chance that their
mate will be able to fertilize their egg, or that their
mate will be healthy. They may choose to mate
with males who have features that are more attractive
to ensure that their sons will also be attractive. Anders
Møller has provided evidence in support of this sexy
sons hypothesis by demonstrating that female Barn
Swallows Hirundo rustica find males who have long
tail streamers particularly attractive and are more
likely to attempt to secure EPCs with long-tailed
males if their own mate has a shorter tail. More
recently however advances in molecular ecology and
genetics have enabled us to investigate the incidence
and consequences of genetic compatibility and
incompatibility in birds. For example, research carried out by Katharina Foerster and her colleagues
has shown that the extra-pair offspring of Blue
Tits Cyanistes caeruleus are more heterozygous than
within-pair offspring and that they exhibit higher
levels of fitness. This suggests that female Blue Tits
who have genetically similar mates seek out EPCs
to increase the genetic diversity of their offspring.
In contrast however Adrianne Hajdasz and her colleagues have demonstrated that female American
Redstarts Setophaga ruticilla paired with a genetically
similar mate were no more likely to seek EPCs, but
that when they did, their offspring were more genetically similar to one another than when they only
mated with their social partner. It may be that in this
species mating in a way that reduces genetic diversity
may be advantageous because the population is a
highly out-bred one with high levels of immigration
and the potential for considerable variation. In such a
population out-breeding may risk the loss of genes
and gene complexes that are adapted to local conditions. These apparently contradictory situations (Blue
Tits minimizing in-breeding and American Redstarts
minimizing out-breeding) suggest that different
populations (relatively closed versus relatively open)
require different strategies to optimize out-breeding.
Key reference
Foerster, K., Delhey, K.J., Lifeld, J.T., and Kempenaers, B.
(2003) Females increase offspring heterozygosity and
fitness through extra-pair matings. Nature 425, 714–17.
Hajdasz, A., McKellar, A.E., Ratcliffe, L.M., et al. (2019)
Extra-pair offspring are less heterozygous than within-pair
offspring in American redstarts Setophaga ruticilla.
Journal of Avian Biology 50: doi:10.1111/jav.02084
Møller, A.P. (1988) Female choice for male sexual tail
ornaments in the monogamous swallow. Nature 332
(6165), 640–2.
Box 5.2 Leks
A lek site is the traditional location at which a group of
males come together to compete and display to visiting
females. As a system lekking, as the behaviour is termed,
is rare but it has evolved several times and is found in a
number of bird groups.
Lekking is an unusual mating system in that males are
chosen by the females as mates but they do not then provide
any parental care or any direct territorial/resource benefit.
The females gain nothing other than the genes that their
offspring will inherit. One of the features of a lek is that matings are actually achieved by relatively few (sometimes only
one) of the males that are present. This fact has been viewed
as something of a paradox, the question being asked if most
males will not mate why do they attend the lek? In an
attempt to resolve this paradox four main hypotheses
have been proposed: hot-spots, hot-shots, kin selection and
female preference.
The hot-spot hypothesis suggests that leks of males form
in particular locations that are regularly visited by the
females in a population. This would maximize the chances
that males would encounter potential mates. Some support
for this hypothesis does come from the observation that males
typically choose particular habitat features when establishing a display arena. Male Houbara Bustard Chlamydotis
undulata choose to lek in open areas where their displays
can be seen by females who more typically inhabit dry wadis
and scrubby cover. On the other hand, the locations of the
leks of Blue-crowned Manakin Lepidothrix coronata have
been shown to be at sites no more likely to be visited than
any other areas of their range. Similarly when the dominant
Great Snipe Gallinago media is removed from its position at
the centre of a lek its place is not occupied by another bird,
instead the lek collapsed. This suggests that in this case hotshots rather than hot-spots are significant. The hot-shot
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hypothesis suggests that inferior males cluster around a
superior a male hoping to gain access to at least some of the
females attracted to him and in some species it has been
shown that those males with a territory/lek position close to
the alpha bird do have better breeding success than those
on the fringes of the lek.
The kin selection hypothesis suggests that leks are composed of related males in effect cooperating to attract
females and gaining an indirect fitness benefit when genes
that they have in common with a more successful relative
are inherited by his offspring. It has been shown that captive
male Peacock Pavo cristatus reared in isolation tend to form
leks with relatives, but lek mates have been shown to be
unrelated in a number of other species including several
of the manakins Pipidae and the Greater Sage Grouse
Centrocercus urophasionus.
As an alternative the female preference hypothesis suggests that leks form as a result of females seeking out larger
groups of males in order to compare them and secure high
5.3 Courtship and mate choice
As the ‘rarer’ sex females are most often the choosier sex (see Boxes 5.2 and 5.3) but how do birds
attract a mate? Males of many species sing repetitive or complex songs that are energetically costly
to produce and may expose them to predators.
Others sport elaborate ornamentation, think of the
fanned tail of the male Indian Peacock Pavo cristatus
for example. Male bowerbirds create bowers in
carefully maintained arenas that they decorate with
colourful objects, and the males of some species of
raptor carry out apparently death defying acrobatics diving and tumbling downwards through the
sky. Some males defend a territory, a space in which
a brood of chicks could be successfully raised;
others provide a female with gifts of food. Whatever
the method of courtship these behaviours enable
members of the choosing sex to discriminate in
some way between potential suitors. Females of
some species make the choice on the basis of the
promise of a resource communicated by a signal
whereas the females of other species seem to be
making the choice on the basis of the signal itself.
5.3.1 Resource provision
Through their courtship behaviour male birds
can have an indirect effect upon the reproductive
99
quality males. If this were the case then we would expect to
see a female preference for larger rather than smaller leks
and exactly this result has been obtained through observation of Little Bustard Tetrax tetrax lek sites.
Interestingly it has been suggested that leks might not be
so far removed from conventional territorial breeding systems as was previously thought and it has been suggested
that clusters of territories may act as ‘hidden leks’ clustered
around a high quality male or location (hot-shot or hotspot), clustered around a group of related males (kinselection) or to facilitate female comparison of males
(female-preference).
Further reading
Fletcher, R.J. and Miller, C.W. (2006) On the evolution of hidden leks and the implications for reproductive and habitat
selection behaviours. Animal Behaviour 71(5), 1247–51.
Högland, J. and Alato, R.V. (1995) Leks. Princeton University
Press, Princeton.
behaviour of their mates. Jon Brommer and his colleagues have demonstrated one such effect through
their study of a Finnish Tawny Owl Strix aluco population. They found that females who had chosen to
mate with larger males were more likely to lay their
eggs earlier in the breeding season. This could, they
suggest, be related to the possibility that larger
males provide more food for their mates during the
pre-laying courtship-feeding period. Interestingly
although male owls continue to feed their mates
during the incubation period, they did not find a
relationship between male size and clutch size, in
spite of the fact that earlier clutches do tend to be
larger. This suggests that clutch size is a trait determined by the female (see chapter 4, section 4.3).
Flight path: females vary their clutch sizes in relation
to environmental factors, page 78.
Key reference
Brommer, J.E., Karell, P., Aaltonen, E., et al. (2015)
Dissecting direct and indirect parental effects in a wild
bird of prey: dad affects when but not how much.
Behavioural Ecology and Sociobiology 69(2), 293–302.
Great Grey Shrikes Lanius excubitor (Figure 5.3) are
socially monogamous, raptor-like passerines that
form territorial breeding pairs. It is usual for both
male and female to contribute to the raising of their
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ESSENTIAL ORNITHOLOGY
Figure 5.3 Great Grey Shrike Lanius excubitor (© Ian Robinson).
young. Male shrikes are well known for their habit of
impaling food items (large insects, small mammals,
birds, and reptiles) on thorns or barbed wire fences, a
habit that has earned them the title butcher birds. The
quality of this larder, the size and nutritional value of
the food it contains, has been shown experimentally
to be one of the key factors used by a female when she
chooses her mate. Larger prey items are presumed to
require a greater effort on the part of the male in terms
of his ability to capture them and the energy that he
expends manipulating them; they are therefore likely
to be an indicator of his physical quality.
I said earlier that these shrikes are socially monogamous. Remember that in saying this I mean that
two birds (one of each sex) form a breeding pair that
rears young together. You should also remember
however that this does not imply that these birds are
necessarily faithful to one another. Great Grey Shrike
males do cuckold their neighbours, fertilizing an
egg that is raised by an unsuspecting foster parent.
But why do the females take part in these promiscuous liaisons, surely they have a suitable mate? Piotr
Tryjanowski and Martin Hromada have made
detailed observations of a population of these birds
and have shown that in fact the males effectively
pay for sex with already mated females by providing them with choice items of food from the larders
that initially impressed their own mates.
Their data (Figure 5.4) show that males are more
likely to be successful when they offer a female a
better gift, and that they tend to offer the best
gifts (the most energetically valuable) to their ‘mistresses’. These gifts they estimate to contribute 66
per cent of the daily food requirement of a female
(compared to the 16 per cent they provide their
mate). Cheating females benefit from these EPCs
because they have an opportunity to mate with
high quality males (presumably males of higher
quality than their own mates). Their cuckolded
partners however do lose out because they will
invest resources raising the chicks of a rival male.
However it would be quite wrong to think of these
hapless males as being unable to avoid the costs
associated with promiscuity and there is abundant
evidence that males do their utmost to avoid being
the ‘victims’ of EPCs.
Francisco Valera and co-workers have made similarly detailed observations of the breeding behaviour
of a population of Lesser Grey Shrikes Lanius minor,
a close relative of the Great Grey and another butcher
bird that uses food as a nuptial gift. They noted that
territorial intrusions by males, that they presumed to
be actively seeking EPCs, were seven times more
common during the fertile period of the resident
female. During this period the resident male was
particularly attentive to his mate, spending almost 80
per cent of his time within 50 m of her. He was also
particularly aggressive towards male intruders,
attacking them and chasing them away. So mate
guarding seems to be an effective EPC minimization
strategy. But what about the 20 per cent of the time
he didn’t guard his mate? To find out what would
happen if males had apparent reason to suspect that
an EPC had occurred the researchers captured
females during their fertile period and removed
them from their territory for one hour. They then
released them back into an adjacent territory so that
when they returned to their mate it would appear
that they had visited his rival. Males responded to
this apparent infidelity by punishing their mate,
attacking her and in many cases aggressively forcing
copulation. Such retaliatory copulations are of course
an important paternity assurance strategy (see
Box 5.1). The same did not however happen if the
removal had taken place outside of the fertile period
(during incubation or chick rearing for example).
There is also a suggestion that unlike males the
females in this population are reluctant to seek EPCs,
they rarely leave their territory during their fertile
phase even if their male has been temporarily
removed. Genetic paternity analysis has revealed
that male mate guarding and female punishment are
an effective strategy in the case of this species because
mixed paternity broods are extremely rare.
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101
14
Number of prey items
12
10
8
6
4
2
0
Birds
Voles
Lizards
Insects
Without gift
Key reference
Valera F., Hoi, H., and Krištín, A. (2003) Male shrikes
punish unfaithful females. Behavioural Ecology 14(3),
403–8.
5.3.2 Ornaments and displays
Male Long-tailed Widowbirds Euplectes progne
have, as their name suggests, an extremely long tail.
In fact this 15–20 cm long bird can have a tail around
50 cm long during the breeding season. We saw in
chapter 2 that feathers can be expensive and there
must surely be an aerodynamic cost to be paid
when towing a streamer this long. So why do these
males have such a long tail? It seems to have
evolved as a result of sexual selection because there
is good experimental evidence of a link between tail
length, male reproductive success, and female
choice. Simply put, females want males with long
tails. The evidence for this comes from a particularly
elegant experiment carried out by ornithologist Malte
Andersson who captured males and artificially
elongated or shortened their tails and then observed
the effect that this had upon their subsequent reproductive success. Long-tailed Widowbirds are polygamous. Males defend an area of grassland from
other males and advertise their presence to females
by means of a conspicuous, bouncing display
flight—showing off their tails to good effect. Each
male attempts to attract a harem of females to his
territory, all of whom will rear his young (assuming
no EPCs take place of course) without his assistance. Andersson trapped male birds and assigned
them randomly to three groups. One set of birds
had their tail feathers cut in half and re-joined with
Figure 5.4 Male Great Grey Shrikes provide more (and
better) gifts when seeking extra-pair copulations (solid bars)
than when seeking to mate with their partner (open bars).
Tryjanowski, P. and Hromada, M. (2004) Do males of the great
grey shrike Lanius excubitor, trade food for extra-pair
copulations? Animal Behaviour 69, 529–33.
no net change in length (this was done as an experimental control). Another group had a 25 cm long
section of their tail removed and the tip was rejoined to the base—thereby shortening the tail.
These 25 cm long removed sections were inserted
into the cut tails of the final experimental group,
thereby lengthening their tails. Andersson then
released the birds back into their territories and
recorded the number of additional nests that each
bird built (a measure of the number of additional
females attracted to him). The results (Figure 5.5A)
show clearly that males with the longest tails attract
the most mates.
However, the results of another tail lengthening
experiment carried out by Sarah Pryke and Staffan
Andersson (Figure 5.5B) provide an intriguing
insight into the basis of the evolution of this courtship signal. They manipulated the tails of a relatively
short-tailed species, the Red-shouldered Widowbird
Euplectes axillaries. Males of this species are slightly
smaller than male Long tailed Widowbirds but they
have very much shorter tails (around 7 cm long).
When these tails were artificially lengthened (in
some cases to 22 cm long) males attracted as many
as six females; three times as many as the longest
tailed unmanipulated individual. So it seems that
female widow birds have a generalized preference
for longer tails, and that this sensory bias has driven
the evolution of the extraordinarily long tails of
some species.
5.3.3 Sharing a mate
Both male and female Dunnock Prunella modularis
seem content to share their mates under some circumstances (see Box 5.4). Female widowbirds seem
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Mean number of new
nests per male
(A)
2
1
0
7
Mean number of active nests
6
5
4
3
Natural tail frequency
(B)
Shortened
Control
Elongated
Tail treatment
120
80
40
0
2
1
0
2
4
6
7
8
10
12
14
16
18
20
22
Manipulated tail length (cm)
Figure 5.5 The relationship between male tail length and reproductive success in the Long-tailed Widowbird (A) and the short-tailed
Red-shouldered Widowbird (B). From (A) Andersson M (1982) Female choice selects for extreme tail length in a widowbird. Nature 299, 818–20;
(B) Pryke, S.R. and Andersson, S. (2002) A generalized female bias for long tails in the short-tailed widowbird. Proceedings of the Royal Society
B: Biological Sciences 269, 2146.
content to share their male with others in his harem.
This is probably because all they require of him are
his genes and access to the resources available in his
territory. They rear their young without his assistance.
In some species however polygyny appears to result
in reduced reproductive success for at least some of
the females involved. So why do they accept it?
In 1969 Gordon Orians published a very influential paper in which he proposed a mathematical
model to explain female acceptance of polygyny. In
his polygyny threshold model (PTM) Orians envisioned a situation in which females would sample
and compare the territories of available males and
then using the information that they have gathered,
elect to join an already mated male in a polygamous
relationship, or to settle with an unmated male in a
monogamous one. This model assumes that females
should prefer monogamy because there will be a
cost to polygamy and that females should only
accept polygamy when the benefits of that relationship outweigh its costs relative to monogamy with
an available unmated male. The point at which this
economic decision is made is the polygamy threshold (see Figure 5.6).
Key reference
Orians, G.H. (1960) On the evolution of mating
systems in birds and mammals. American Naturalist
104, 589–603.
Do female birds really behave in a manner consistent with the PTM? Stanislav Pribil and William
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103
Box 5.3 Turning the tables: reproductive role reversal in the Spotted Sandpiper
In the vast majority of bird species males compete with one
another for the attentions of choosier females and females
are able to make the most of good males and favourable
breeding conditions by varying the numbers of eggs that are
laid in a clutch. The Spotted Sandpiper Actitis macularis is an
interesting exception to this rule. Female Spotted Sandpipers
always lay four eggs in a clutch. Unable to vary their clutch
size, the only way that they could increase their output in a
good year would therefore be to lay a second clutch of four
eggs. However, the sandpiper breeding season is a short one
and it is doubtful that a female could manage to rear one
brood of chicks to fledging and then have time to rear a
second before migrating.
Faced with these difficulties female Spotted Sandpipers
employ an interesting strategy—they act like males. Females
arrive on the summer breeding grounds first and compete
with one another to secure territories. When the males do
arrive the females actively court them and the ‘best’ females
secure mates quickly and lay a clutch of four eggs.
When resources allow it the females of some populations
then abandon their newly laid eggs leaving their mate to
incubate and rear the brood alone. Males are only able to do
this because the sandpipers time their breeding to coincide
A
?
B
Further reading
Oring, L.W., Fleischer, R.C., Reed, J.M., and Marsden, K.E.
(1992) Cuckoldry through stored sperm in the sequentially polyandrous spotted sandpiper. Nature 359, 631–3.
Monogamous
(B)
Female reproductive success
(A)
with the emergence of a superabundance of insect food and
because newly hatched sandpipers are precocial (able to
thermoregulate and fend for themselves from hatching).
Furthermore, the system works because males are slightly
more common in the population than females and so after
abandoning their first mate, females are able to secure a
second and lay a second clutch of eggs to be reared by him.
The first males to pair up clearly benefit because they
have secured for their offspring the genes of the best females
and because the best that they can do is secure for themselves a clutch of four eggs. But do the females compromise
the quality of their offspring when they take a second male?
After all these are the males that were ‘left on the shelf’ first
time around and so are presumably inferior in some way. In
fact DNA paternity analysis has revealed that second brood
chicks are often fertilized by first male sperm that have been
stored by the female, in this way females are able to make
the most of the genetic resources available to them.
c
2nd
polygyny
PT
B
A
Territory quality
or quantity of breeding situation
Searcy have demonstrated experimentally that in
the case of at least one species, the Red-winged
Blackbird Aegaius phoecniceus, they do. The PTM
makes a number of testable assumptions: i) that
polygamy is costly to females, so they prefer
monogamy, ii) that females choose males on the
basis of either male quality or the quality of the ter-
Figure 5.6 The polygyny threshold model. The model
presumes that females have choice and can choose to pair
with already mated or unmated males (A). Female
reproductive success varies according to the quality of the
territory of the male chosen. If a female can gain more by
choosing an already mated male than she can by choosing a
single bird, then she should choose polygamy over
monogamy (B). From Scott G.W. (2005) Essential Animal
Behavior. Blackwell Science, Oxford; adapted from Orians,
G.H. (1969) On the evolution of mating systems in birds and
mammals. American Naturalist 104, 589–603.
ritory of the male, and, iii) that faced with a choice
between a low quality monogamous male/territory
and a high quality polygamous male/territory,
females will choose polygamy (if the cost of polygamy is lower than the cost of choosing monogamy
in this situation). Through their observations and
experiments Pribil and Searcy have shown that all
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ESSENTIAL ORNITHOLOGY
three of these assumptions are met in the case of
their Red-winged Blackbird study populations.
Key references
Pribil, S. (2000) Experimental evidence for the cost of
polygyny in the red-winged blackbird Agelaius
phoeniceus. Behaviour 137, 1153–73.
Pribil, S. and Searcy, W.A. (2001) Experimental
confirmation of the polygyny threshold model for
red-winged blackbirds. Proceedings of the Royal
Society of London B 268, 1643–6.
Pribil began by confirming the first prediction of the
model when he demonstrated that female Redwinged Blackbirds suffered a reproductive cost if they
chose to mate with an already mated male; he found
that they fledged fewer and lighter young. This observation is important because survival to maturity in
this and many species is significantly correlated with
fledging weight; heavier birds survive better. As
would be predicted from these results he also showed
that when offered the choice of two males, one with a
mate and one without, experimental females invariably chose to enter into a monogamous relationship.
When they have the choice, female Red-winged
Blackbirds also discriminate between males on the
basis of territory quality (the second of the model’s
predictions). They will preferentially mate with an
unmated male controlling a territory that offers the
opportunity to build a nest overhanging water (presumably because such nests offer enhanced protection from predators).
To test the model’s third and perhaps most significant prediction; that faced with a choice between
a low quality monogamous male/territory and a
high quality polygamous male/territory, females
will choose polygamy (if the cost of polygamy is
lower than the cost of choosing monogamy in this
situation) Pribil and Searcy designed an elegant
field-based experiment in which they manipulated
the choices available to females. In it they compared
the attractiveness to females of males whose territories were manipulated such that one in each pair
offered an unmated male with no over-water nest
site while the other offered a high quality nest
(over-water, see Figure 5.7) that was occupied by an
already mated male. In almost all cases newly arriving females chose polygyny rather than monogamy,
exactly as would be predicted by the PTM.
(A)
(B)
Figure 5.7 (a) Male Red-winged Blackbird Aegaius phoecniceus
(© Ian Robinson). (b) This Red-winged Blackbird nest was built on a
platform designed by Searcy and Pribil to provide females with high
quality over-water nest sites (© Stanislav Pribil).
Box 5.4 The Dunnock: a case study in sexual conflict
Within a single population of the Dunnock it is possible
to recognize genetic monogamy, social monogamy,
polygyny, polyandry, and even polygynandry. As a consequence, the study of the reproductive behaviour of this
otherwise unobtrusive bird by Nick Davies and his
Cambridge University colleagues is quite possibly one of
the best, and best-known, case studies of bird breeding
behaviour.
Central to the system is sexual conflict, the conflict of
interests of males and females. Figure 5.8 summarizes the
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105
average. Primary males therefore attempt to drive away
secondary males.
A similar state of affairs exists in the case of males in that they
can do considerably better if they persuade a second female to
join them in a polgynous group, and if polyandry is inevitable
then by attracting another female to change a polyandrous
group into a polygynandrous one he can at least not lose out.
The actual system that is established will represent a
compromise on the part of one or all of the parties involved
and of course through EPCs and EPC counter measures the
actual genetic composition of broods may be even more
complicated than even Figure 5.8 would suggest.
benefits and costs of each system (in terms of chicks produced) to both males and females.
Taking monogamy as a starting point, males and females
both benefit equally—raising 5 young each (assuming that
this is genetic and social monogamy). But note that a
female can improve upon this situation if she persuades a
secondary male to join a polyandrous group—she will raise
6.7 chicks, and the secondary male benefits because rather
than have none he will have sired 3 chicks. Female Dunnocks
regularly court males in an attempt to benefit in this way.
However, this arrangement clearly does not benefit the primary male, rather than siring 5 chicks he sires just 3.7 on
Monogamy
=5
=5
a
= 7.6
= 3.8
b
= 3.8
= 3.0
Polygyny
= 6.7
a
= 3.7
Polyandry
a
a
= 3.6
=5
b = 2.2
= 3.6
Polygynandry
5.4 Song
Male birds of a number of species sing a courtship
song to attract a mate and as a form of resource
defence (Figure 5.9). We will consider both of these
functions of song below, but first we should consider the song and singing behaviour itself. We
should also note that only three groups of birds
(the songbirds, the hummingbirds, and the parrots)
have the capacity to learn and reproduce new
sounds. The vocalizations of all other birds groups
are innate and inherited from their parents.
Figure 5.8 The complex mating system of the
Dunnock. Several scenarios are illustrated and in each
case the average number of young produced per
individual is given. See text for detailed explanation.
From Davies, N.B. (1992) Dunnock Behaviour and Social
Evolution. Oxford University Press, Oxford.
Bird song is produced when air passes through
the syrinx, the avian equivalent of the human
voice box. The variations in song that we hear are
a result of the carefully controlled contraction of
the muscles and membranes of the syrinx, which
are in turn controlled by nervous signals originating in a clearly defined area of the hindbrain,
termed the tracheosyringeal motor nucleus (often
referred to as nXIIts). Singing is triggered by a
wide range of environmental stimuli (by environment here I mean both the environment external to
the bird—the physical and social environment,
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effect has yet to be confirmed). As the male HVC
develops, it forms two major projections, one of
which connects it to an area of the hindbrain termed
RA (the Robust nucleus of the Arcopallium) that is
involved in the production of learned sounds and is
part of the same control pathway as nXIIts. In female
brains, the HVC-RA pathway does not develop. The
other projection is to the enigmatically labelled forebrain Area X, which is associated with song learning
and to which I will return later in this chapter.
Figure 5.9 This male Whitethroat Sylvia communis is in full song,
proclaiming ownership of a territory and availability to mate (© Ian
Robinson).
and the bird’s internal environment—the particular
hormones in its bloodstream etc.). However, song
production is under the control of a specific cluster
of brain cells termed the High Vocal Centre (HVC)
from which neuronal signals propagate through a
pathway involving specific areas of the fore, mid,
and hindbrain, ultimately connecting with nXIIts
and the syrinx. The details of this pathway are
beyond the scope of an introductory text such as
this, but if interested readers did want to know
more the excellent book Nature’s Music by Peter
Marler and Hans Slabbekoorn would be a very
good place to start.
The HVC of male songbirds is significantly more
developed than that of female birds and this difference is initiated at an early stage in the development
of the brain. But what exactly triggers this sexual difference in the neurological basis of song has been a
mystery. Recently however Xuqi Chen and colleagues have reported that HVC development in the
brain of the male Zebra Finch Taeniopygia guttata is
temporally linked to the expression of a Z-linked
gene which codes for the protein tyrosine kinase
receptor B (trkB) which acts as a receptor for a neurotransmitter termed BDNF. BDNF in turn is known to
be involved in the differentiation of brain cells and in
the development on the HVC in particular. As we
might reasonably expect male birds have far higher
trkB levels, having twice as many trkB Z-linked
genes than females. Thus a direct link between a sexlinked gene and a sex-specific behaviour has been
established (although the exact mechanism for its
Key references
Chen, X., Agate, R.J., Itoh, Y., and Arnold, A.P. (2005)
Sexually dimorphic expression of trkB, a Z-linked gene,
in early posthatch zebra finch brain. Proceedings of
the National Academy of Sciences of the USA
102(21), 7730–5.
Marler, P. and Slabbekoorn, H. (2004) Nature’s Music:
The Science of Birdsong. Elsevier, San Diego.
5.4.1 Song learning
Song production is innate in that males reared in
isolation will sing at maturity. However, singing the
right song seems to largely depend upon a male
learning from an appropriate tutor. (Although it
has been recently shown that in the Reed Warbler
Acrocephalus schoenobaenus birds reared in isolation
can mature to sing normally). Birds learn songs in a
variety of ways. Some such as the White-crowned
Sparrow Zonotrichia leucophrys can only learn their
songs during a very short period of their early lives
(often referred to as a sensitive period). In the
Chaffinch Fringilla coelebs this sensitive period is
longer (lasting for the whole of the first year of a
bird’s life). Such birds are termed closed-ended
learners or age-limited learners. On the other hand
males of some species such as the Willow Warbler
Phylloscopus trochilus are able to learn new songs
and add to their repertoires throughout their lives.
The various mechanisms by which song learning takes place are proving to be more variable
than was originally thought to be the case and I would
recommend that the interested reader consult the
excellent review of the topic by Beecher and Brenowitz.
However, the basic model of learning seems to include
three steps: a preliminary sensory acquisition phase, a
silent phase, and finally a sensorimotor phase.
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Key references
Beecher, M.D. and Brenowitz, E.A. (2005) Functional
aspects of song learning in songbirds. Trends in
Ecology and Evolution 20(3), 143–9.
Wheelwright, N., Swett, M.B., Levin, I.I., et al. (2008)
The influence of different tutor types on song learning
in a natural bird population. Animal Behaviour 75,
1479–93.
Young birds seem to have an innate template that
can be modified to some degree by a process of
learning. During the first phase of song development (the sensory acquisition phase which equates
to the sensitive period) a young bird will hear a wide
range of noises but evidence suggests that they are
most sensitive to the song that most closely matches
their own innate template—the song of a suitable
conspecific tutor. In some cases such as the Zebra
Finch Taenoipygia guttata and galapagos finches
Geospizidae the tutors are always, or almost always,
the rearing male parent. In others however the song
that a bird learns is not a complete copy of that of its
father. In a study of a wild population of Savannah
Sparrow Passerculus sandwichensis Nathaniel Wheelwright and colleagues have shown that males in
their study population developed a song similar to
(but not the same as) that of their social father in
only 12 per cent of cases, the majority of the population learning a song more similar to that of their
neighbours. Their results also suggest that in this
population individuals incorporate elements of
song from a number of tutors into their repertoire.
During this learning phase it appears that a bird
memorizes aspects of tutor song and uses them to
refine its original innate template thereby producing
a more exact one that conforms to the specific song
pattern of its species. Some birds in isolation will
learn from a recording but learning does appear to be
enhanced when a live tutor is present and in some
cases, such as the Zebra Finch, a live tutor is essential. After song acquisition there follows a silent
phase when singing is not taking place but during
which the components of song that the bird has
learned are stored for future use. Prior to the onset of
the breeding season (when the testes regenerate) testosterone triggers singing and the final phase of song
acquisition, the sensorimotor phase, occurs. Now the
bird sings. Initially the song that is produced will not
107
be perfect but it will be a very close approximation of
the song typical of the species. Through time (and
actually very quickly) the song is refined until it is
perfected or crystallized. It seems that hearing oneself is crucial at this time and that birds match the
songs that they produce against their now completed
internal template. But how does the bird know that it
is getting it right? Jesse Goldberg, Vikram Gadagkar,
and their colleagues have demonstrated that Area X,
that part of the forebrain that is connected to the
HVC is crucial to the development of the correct
song. As a ‘practising’ bird develops its song it can
essentially sing two types of note—the right ones
and the wrong ones. By recording the activity of the
neurons of a the ventral tegmental area (VTA), which
project to Area X, the Goldberg group determined
that VTA neurons had an inhibitory effect on brain
activity when the bird produced an incorrect note,
but when the right note was produced they stimulated a dopamine response. In essence the bird was
rewarded, and when it eventually perfected a note
that it had struggled with for some time, the level of
the dopamine reward was larger. It would seem
therefore that the VTA neurons act as a sort of internal
critic, using a reward to reinforce success.
Key reference
Gadagkar, V., Puzerey, P.A., Chen, R., et al. (2016)
Dopamine neurons encode performance error in
singing birds. Neuroscience 35, 12–82.
5.4.2 Functions of song
Bird song has two primary functions. It is used primarily by male birds as both a courtship signal to
attract mates and as a signal to other males that a
territory is occupied (see Box 5.5). Artificially muted
male birds in a number of studies have been shown
to be unable to either gain territories or attract
mates. Recently, experimental evidence has been
provided suggesting that male birds evaluate their
rivals based upon the songs they sing. Samuel
Hill and his co-workers have carried out playback
experiments to explore the responses of territorial
male Tui Prosthemadera novaeseelandaie (a New
Zealand endemic) to recordings of songs of increasing complexity. Their results demonstrate that males
approach, and respond to, more complex songs
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ESSENTIAL ORNITHOLOGY
Box 5.5 What’s in a song?
European Starlings Sturnus vulgaris have been described as
being amongst the most accomplished of singers. Males
have extremely varied repertoires and sing for prolonged
periods during their breeding season. To demonstrate that
their song has both a female attractant and male deterrent
function, James Mountjoy and Robert Lemon studied a wild
population of starlings (breeding readily in nest-boxes). To
see if the birds would be attracted to it, starling song was
played from some of the boxes. As a control, and for comparison, each box was paired with a second, from which no
song was broadcast. Throughout their observation period
the team saw no female starlings at silent boxes, but they
saw 12 investigating the boxes from which song was being
broadcast. The song was evidently attractive to them. We
might have expected male starlings to behave differently—
given that we assume song to serve as a deterrent to rivals
but in fact of 20 birds seen at boxes, 17 were investigating
the ones with a playback. So is song a deterrent to rival
males in this species? A further refinement of the experiment
showed that it is.
In a second experiment they paired boxes with a playback
of a very simple starling song with boxes playing a very complex one. This time the sexes did behave differently. All of the
females observed were attracted to the complex song whereas
(A)
90 per cent of the males were attracted to the simple song. So
it would seem that a complex song would benefit a male
because it would attract females and deter male rivals.
Further evidence that female starlings consider males
with a complex song to be higher quality comes from
another piece of research carried out by Mountjoy and
Lemon. They made further detailed observations of their
study population, this time recording the complexity of the
song of individual males during the courtship period and
then noting the date at which the first egg was laid in the
boxes occupied by each of these males. Their prediction was
that the males with the most complex songs would be in
the best condition and would therefore be the most attractive to the females. The females should therefore be prepared to commit to pair with and lay eggs with these males
preferentially.
From Figure 5.10A it is clear that a positive relationship
between song complexity and body condition (in this case
an expression of size and mass) exists—fitter birds are better singers. As would be predicted Figure 5.10B shows that
females paired to males with the biggest repertoires lay eggs
sooner than those that pair to poorer males. Research carried out by Deborah Duffy and Gregory Ball has revealed
another potentially important indication that song could be
(B)
55
30
Delay until first egg (days)
50
Repertoire size
45
40
35
30
24
18
11
25
20
–0.06
–0.04
–0.02
0.00
Condition
0.02
0.04
0.06
5
20
26
32
38
43
Repertoire size
49
55
Figure 5.10 A The relationship between male starling song repertoire size and body condition of male; and, Figure 5.10B The relationship
between male starling song repertoire size and delay until the laying of the first egg. From Mountjoy, D.J. and Lemon, R.E. (1996) Female
choice for complex song in the European Starling: a field experiment. Behavioural Ecology and Sociobiology 38, 65–71, by permission of
Oxford University Press.
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used by female starlings to assess the quality of potential
mates (and presumably therefore to influence the potential
quality of their eventual offspring). They have demonstrated
a correlation between the male song variables bout length
(the mean length of a single song) and singing rate (the
mean number of times a bird sings in an hour) and two
measures of the strength of the immune system of the birds.
more quickly and more aggressively in comparison
to their responses to simple songs. This suggests
that these males perceive a complex song (and presumably therefore a bird that sings it) as being more
of a threat and the researchers have speculated that
song complexity may therefore communicate information about the quality, attractiveness to females,
and/or territorial intentions of an individual.
Although reports of female song are rare, some
female birds have been observed singing in behavioural contexts that suggest they too use song to
defend territories and mates. For example Dustin
Reichard and his colleagues have recorded female
Dark-eyed Junco Hyemalis thurberi in a Californian
urban population singing a male-like song (but
across a narrower frequency range) when they and
their male partner are exposed to the presence of a
potential female rival.
Key references
Reichard, D.G., Brothers, D.E., George, S.E., et al.
(2018) Female Dark-eyed Juncos (Junco Hyemalis
thurberi) produce male-like song in a territorial
context during the early breeding season. Journal of
Avian Biology 49(2), 1–6.
Hill, S.D., Brunton, D.H., Anderson, M.G., and Ji, W.
(2018) Fighting talk: complex song elicits more
aggressive responses in a vocally complex songbird.
Ibis 160, 257–68.
The temporal coincidence of male singing behaviour and the onset of reproductive behaviour is in
itself highly suggestive that singing has a courtship
function and evidence that this is the case comes
from a range of field and laboratory studies. Singing
rates of territorial males have been shown to be
higher before a female joins a male on his territory
than they are once the pair is established. However,
if a female is temporarily removed from the territory, the resident male responds by increasing his
109
In both cases their results demonstrated clearly that better
singers had the most robust immune system.
References
Duffy, L.D., and Ball, G.F. (2001) Song predicts immunocompetence in male European starlings (Sturnus vulgaris).
Proceedings of the Royal Society Series B. 269, 847–52.
singing rate. Presumably he is attempting to replace
his ‘lost’ mate. Similarly males may increase their
singing behaviour while their mate incubates their
clutch of eggs. Presumably these birds are attempting to attract a second mate or to secure EPCs. Dag
Eriksson and Lars Wallin have demonstrated very
clearly that male song attracts females in the case of
both the Collared Flycatcher Ficedula hypoleuca and
the Pied Flycatcher Ficedula albicollis. These birds
nest readily in nest-boxes and the boxes can be used
to trap birds that enter them (trapped birds are
released unharmed very quickly). The researchers
arranged 28 nest-boxes throughout their study
population, each box having a model flycatcher
about 1 m from it on a prominent perch (live flycatcher males usually sing from such perches presumably to attract females to them). From half of
the boxes they played the song of the same species
as the male model perched outside. The other half
of the boxes were silent. The results of this study
clearly show that females were far more likely to
inspect the boxes of singing males and song can
therefore be presumed to have attracted them to the
territory and persuaded them that the nest-box
might make a suitable home. Of the female flycatchers trapped whilst inspecting nest-boxes, 90 per
cent were attracted to those boxes having both a
model male and a recording of his song.
Key reference
Eriksson, D. and Wallin, L. (1986) Male bird song
attracts females—a field experiment. Behavioural
Ecology and Sociobiology 19, 297–9.
Females are able to discriminate between males on
the basis of their songs, preferring some song types
over others. Female dunnocks for example have
been shown to pay more attention to a recording of
the song of their mate when he has been removed
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ESSENTIAL ORNITHOLOGY
than to the song of a neighbour. Furthermore this is
particularly the case during the female’s fertile
period suggesting that she uses her mate’s song as a
way of finding him to seek out copulations.
5.4.3 Synchronized singing
Although the songs of individuals of a species do
vary, often markedly, a consequence of birds learning from those around them may be that all of the
birds in an area develop a broadly similar repertoire. This seems to be an advantage in some cases
and males are known to match their repertoires during singing contests. In some situations it appears
that singing a similar song to that of a rival can
reveal to him that you are a familiar neighbour and
may therefore be tolerated. On the other hand, a
song repertoire that is different is more likely to be
responded to aggressively because it reveals the
singer to be an unknown intruder and therefore to
be a greater potential threat.
Song matching however, the singing of the same
song as a rival at the same time as a rival, and the
overlapping of singing bouts between rivals does
appear to be a particularly aggressive signal in some
species, even between neighbours. Birds matching or
overlapping in this way are more likely to escalate
their contest to a full-blown fight. Perhaps not surprisingly these contests are more common between
strangers or between neighbouring birds that are
establishing territories at the start of a breeding season than between established territorial neighbours.
Perhaps to facilitate comparison, the males of
many populations of birds synchronize their singing
behaviour; the dawn chorus being perhaps the
most familiar example of this phenomenon. The still,
dawn air enhances sound transmission, and it has
been suggested that low light levels and low air
temperatures at dawn make other behaviours less
possible (feeding on insects for example). There
may also be less interference from noise pollution at
dawn (see Box 5.6). Perhaps overnight mortality is
high and singing at dawn allows males to identify
gaps between territories? Or perhaps a synchronized
chorus simply makes it easier for males to compete
with one another and for females to compare them.
Evidence from radio tracking has revealed that in the
Nightingale Luscinia megarhynchos at least, the dawn
chorus is a means by which males can compete with
one another and identify vacant territories. Tobias
Roth and his colleagues have radio tracked female
nightingales and recorded male singing behaviour.
They found that during the early part of the breeding
season (before females migrate into their breeding
areas) males sing most at dawn (although famously
they do of course sing all night) (Figure 5.11A). Once
the females arrive, paired males continue to be most
vocal towards the end of the night and at dawn
(Figure 5.11B), but bachelor males increase their singing throughout the night. Radio tracked females
(released into the area by the researchers to simulate
new arrivals) were found to be most mobile at night
(Figure 5.11C). Roth and his co-workers interpret
these observations as follows. They suggest that
newly arrived females visit several males over the
course of a night, listening to the song of each of
them prior to choosing a mate (this is why bachelors
rather than paired males sing at this time). At dawn
the females become inactive and the function of
singing switches from mate attraction to territorial
defence (all male territory holders sing at this time).
A further advantage of synchronized singing may
be that it helps the birds of an area to synchronize the
rest of their reproductive behaviour. Doing so could
be an advantage in that synchronized production of
young may swamp local predator populations with
prey and thereby ensure survival of a greater proportion of young birds and increase individual survival
probability of each chick. It may also enable sharing
of nest/chick defence activity and improve the efficiency of foraging parents (if they are able to feed as
flock mates with other foraging parents). In the case
of Zebra Finch Taeniopygia guttata Joseph Wass and
his colleagues have shown that exposure to the
sounds of a breeding colony of finches (including
male courtship song) caused male Zebra Finches to
increase their own singing rate (particularly if the
sounds were recorded from their own colony). They
also found that females were more synchronous in
their egg laying when they were played colony
sounds and they produced larger clutches of eggs.
Key reference
Wass, J.R., Colgan, P.W., and Boag, P.T. (2005) Playback
of colony sound alters the breeding schedule and
clutch size in zebra finch (Taeniopygia guttata) colonies.
Proceedings of the Royal Society B 272, 383–8.
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REPRODUCTION
Singing activity (%)
(A)
(B)
0.8
0.6
0.4
0.2
0
Dusk N1 N2 N3 N4 N5 N6 N7 Dawn
20:20 21:30 22:40 23:50 01:00 02:10 03:20 04:30 05:40
Time of day
Distance covered per hour (km)
(C)
2.0
Dusk N1 N2 N3 N4 N5 N6 N7 Dawn
20:36 21:41 22:46 23:51 00:56 02:01 03:06 04:11 05:16
Time of day
10101010 9 9 9 9 1010 8 8 8 7 8 7 7 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 5 6 6 6 5 5 5 5
1.5
1.0
0.5
0
12
14
16
18
20
22
24
02
04
06
08 10 12
Time of day
14
16
18
20
22
24
02
04
06
Figure 5.11 Female movement and male singing behaviour of Nightingales; (A) prior to female arrival, birds that will eventually find a mate
(closed circles) and those that will not (open circles) both increase their singing activity as dawn approaches, (B) after female arrival, paired birds
and birds that will eventually find a mate (closed circles) sing most at dusk and as dawn approaches, and (C) females searching for prospective
mates are most active at night. From Roth, T., Sprau, P., Schmidt, R., et al. (2009) Sex specific timing of mate searching and territory prospecting in
the nightingale: nocturnal life of females. Proceedings of the Royal Society B, 276, 2045–50.
Box 5.6 Bird song and noise pollution
In 2003 Frank Rheindt censused the birds breeding along
woodland transects moving away from a busy German
motorway and found that species with low frequency songs
such as the Chiffchaff Phylloscopus collybita and Great
Spotted Woodpecker Dendrocopos major were 60–75 per
cent less common closer to the road. Because birds with
higher frequency songs were not similarly affected, he concluded that birds were probably avoiding areas close to
roads because ambient low frequency traffic noise drowned
out their song. Since then numerous studies have suggested
an impact of urban noise pollution from traffic and from
industry, on birds and particularly upon aspects of birds’
breeding behaviour. For example in 2006, Hans Slabbekoorn
and Ardie den Boer-Visser co-authored a report with the
attention grabbing title Cities Change the Songs of Birds. In
this thought-provoking article they made the chilling claim
that worldwide urbanisation and the on-going rise of urban
noise levels form a major threat to living conditions in and
around cities. Specifically they, like Rheindt, were highlighting the problem faced by songbirds having to compete with
urban noise pollution to make themselves heard. In their
study Slabbekoorn and den Boer-Visser compared the songs
of Great Tits Parus major breeding in ten major European
cities with woodland populations close to each of them.
They too concluded that low frequency urban noise pollution
masks low frequency bird song. But in this case they also
found that by altering their songs, the birds were fighting
back. Analyses of the songs of the Great Tits in their study
continued
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ESSENTIAL ORNITHOLOGY
Box 5.6 Continued
populations revealed a frequency shift in urban birds. They
were no longer singing the lower notes of their song at a
low frequency. Although the upper frequency of their song
remained unchanged, the lower notes were now higher in
urban than rural settings and so the frequency range of their
song was narrower. This ability to respond and adapt might
seem like good news, and in the context of Great Tits being
able to hear one another it probably is. More recently however a range of experiments involving manipulations of
ambient noise levels in both the laboratory and the field suggest that increased exposure to noise has a much broader
range of impacts upon birds than just making their songs
difficult to hear. Noise pollution can in fact have physiological impacts upon adults and nestlings. It has also been
demonstrated by Alizée Meillère and colleagues that exposure to noise results in reduced telomere length in House
Sparrow Passer domesticus nestlings, which may affect their
survival in the longer term. Also, birds exposed to noise often
have a reduced immune response and associated higher
blood concentrations of stress indicators. Migrating birds
have been shown to avoid stop-over sites that have higher
(B)
15
Female Settlement Rank
Male Settlement Rank
(A)
10
5
20
15
10
5
45
50
55
60
Amplitude (dBA)
45
50
55
60
Amplitude (dBA)
(D)
Apr 16
Apr 20
Apr 24
Mean nestling BCI per nest
(C)
Egg-laying date
levels of noise pollution, potentially impacting upon their
ability to adequately refuel for their onward journey.
Recently Allison Injaian and co-workers at the University
of California have conducted a particularly elegant fieldbased experiment involving a population of nest-box breeding Tree Swallows Tachycineta bicolor to better understand
how exposure to noise pollution, and an associated reduction in perceived habitat quality, can affect bird territorial
settlement patterns and reproductive success. To measure
the impact of noise pollution, the researchers assigned some
clusters of nest-boxes to an experimental group where they
played loud recordings of traffic noise from a few days prior
to the return of any swallows from their migration grounds
until after all of the boxes in the study had been occupied
(no eggs or chicks were exposed to elevated noise levels).
The other clusters of boxes were used as controls for comparison and no recordings of traffic noise were played there.
By recording the occupancy of experimental and control
nest-boxes, and by monitoring the reproductive success of
the swallows, the team were able to demonstrate the impact
of increased noise levels upon both settlement rates and
Control
Noise
1.5
1.0
0.5
0.0
–0.5
–1.0
–1.5
Control
Noise
Figure 5.12 shows the order in which
nest-boxes were occupied in relation to the
level of ambient noise (amplitude in dBA)
at each of them for male (A) and female
(B) tree swallows. Quieter boxes were
settled first. Female swallows laid their first
egg sooner in quiet nest-boxes than in
noisy nest-boxes (C), and that nestlings in
noisier boxes had poorer body condition
(D) (body condition index (BCI) measured
as mass/wing length). From Injaian, A.S.,
Poon, L.Y., and Patricelli, G.L. (2018) Effects
of experimental anthropogenic noise on
avian settlement patterns and reproductive
success. Behavioural Ecology 29(5),
1181–9, by permission of Oxford
University Press.
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aspects of reproductive success. Specifically they found that
control (quiet) nest-boxes were occupied more quickly by
returning birds than noisy experimental nest-boxes, an indication that the birds prefer the quiet nest-boxes. They also
found that females were more likely to lay eggs sooner in
quiet boxes (on average 3.8 days sooner) and that clutches
of eggs laid in noisy nest-boxes were on average 0.58 eggs
smaller than those in quiet boxes. In addition, although survival to fledging was not related to noise levels, nestlings
in noisy nest-boxes did have poorer body condition, even
though they had not been directly exposed to the noise as
either eggs or chicks. These findings suggest that birds
perceive noise polluted areas to be poorer quality territories
and confirm that noise pollution has a negative impact
upon important aspects of reproductive success. From
Figures 5.12A and 5.12B though it is apparent that the
impact of noise on settlement rates is stronger for females
than it is for males, something that the researchers suggest
might be explained by the fact that extra-pair copulation
rates are particularly high in Tree Swallows (50 per cent of all
broods have extra-pair offspring) and that the fitness costs
for males occupying noisy territories may be lower than for
Flight path: Swamping predators can reduce
individual vulnerability to predation. page 137.
5.5 Raising a family
You will recall from chapter 4 that most young birds
require some degree of parental care; the exception
being the fully independent super-precocial chicks
of some megapode species. The degree of care
required varies from a relatively low level of protection and tuition (precocial chicks) to that required
by the altricial passerines that are blind, deaf, and
completely helpless at hatching. During the posthatching period chicks are not efficient thermoregulators and rely to a large extent upon their parents
for warmth or for shade (when the problem is an
inability to stay cool). Both precocial and altricial
chicks develop quickly though, and after about a
week most are largely able to control their own
body temperature. To do this they rely upon their
insulating down and growing contour feathers to
regulate heat loss and upon the heat-generating
shivering of their developed leg and breast muscles.
Rapid growth requires a lot of energy and so
chicks typically have prodigious appetites. At this
113
females because through EPCs males can ensure that some
of their offspring develop in quieter nest-boxes.
It seems clear that noise pollution in the form of traffic
noise has a detrimental impact upon birds, but what can we
do about it? Where appropriate, roadside barriers could be
erected, or vegetation managed to reduce noise transmission. However, research suggests that much of the noise
produced by traffic is related to the speed vehicles travel and
the interaction of tyres and road surfaces. So one strategy
might be to impose speed limits and to use noise dampening
road surfaces (such as porous asphalt) in areas that are of
particular conservation significance.
References
Meillère, A., Brischoux, F., Ribout, C., and Angelier, F. (2015)
Traffic noise exposure affects telomere length in nestling
house sparrows. Biology Letters 11(9), 1–5.
Rheindt, F.E. (2003) The impact of roads on birds: Does song
frequency play a role in determining susceptibility to noise
pollution? Journal für Ornithologie 144, 295–306.
Slabbekoorn, H. and den Boer-Visser, A. (2006) Cities change
the songs of birds. Current Biology 16, 2326–31.
time birds often have a diet that differs from that
of adults of their species to enable them to obtain
higher than usual amounts of protein, fat, and calcium for muscle and bone development. Most passerine chicks for example are raised on a diet of
soft-bodied insects, snails, and fragments of egg
shell even if as an adult their diet would be
restricted to grains and fruits. Some specialists such
as pigeons and penguins regurgitate a nutritious
mixture of fats and protein to facilitate very rapid
chick growth. The ‘milk’ regurgitated by pigeons
is composed largely of sloughed off oesophageal
epithelial cells.
5.5.1 Begging
Chicks solicit food from their parents by begging, a
behaviour that typically involves a screaming call, a
wide gape, and exaggerated head movements. In
the case of some birds, and particularly those in
darker nests, the flanges of the gape and the palate
are often brightly coloured to make them a more
conspicuous stimulus (Figure 5.13). Initially most
young birds are indiscriminate in their begging
behaviour. For example, the very young chicks of
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ESSENTIAL ORNITHOLOGY
Amount of pecking
114
0
5
Days in nest
10
Figure 5.14 Although equally likely to beg from (peck) models of
both Herring Gulls (open symbols, broken line) and Laughing Gulls
(filled symbols, solid line) when newly hatched, Herring Gull chicks
learn to focus their attention on a model of their parent. From
Hailman, J.P. (1969) How an instinct is learned. Scientific American
221(6), 106.
Figure 5.13 The bright yellow gapes of these begging Barn
Swallow Hirundo rustica are an effective signal of hunger to their hard
working parents (© Bill Scott).
cavity nesting passerines will beg at any shadow passing in front of the nest entrance be it friend or foe. As
they mature, their behaviour becomes more refined
and eventually they become more discriminating;
directing their begging only towards their parents and
responding to other shadows with silence and a
crouch. This ability to discriminate and beg only when
it is appropriate to do so is essential because begging
calls have been shown to attract predators.
In a set of experiments now quite properly regarded
as being ‘classics’ Jack Hailman demonstrated this
phenomenon in the case of the Herring Gull Larus
argentatus. These chicks had been previously shown,
by Niko Tinbergen, to instinctively peck at any
beak-like stimulus just so long as it was vaguely
similar to a real beak (long, thin, and with a contrasting mark towards its tip). Herring Gull beaks
are yellow with a red spot towards the tip of the
lower mandible. Chicks peck at the spot instinctively and the pecking stimulates the adult bird to
regurgitate food—so pecking is a begging behaviour. Prior to Hailman’s work it had been assumed
that instinctive behaviours such as this one were
inflexible, but by presenting wild Herring Gull
chicks in their own nests with models of Herring
Gull heads and beaks and Laughing Gull Larus atricilla heads and beaks (all red) he showed that this
was not in fact the case. As the data presented in
Figure 5.14 show, the chicks did initially peck at
both stimuli, but through time their interest in the
Laughing Gull model waned. Why? Well because
these chicks were of course being fed by their parents and so learned to associate a Herring Gull head
and beak with food and to ignore the inappropriate
stimulus of a Laughing Gull head; a process termed
perceptual sharpening.
Recently further subtleties of the begging relationship have been explored. Clearly chicks beg to
be fed and parents should respond to begging by
feeding chicks, but do the needs of the parents and
chicks and of siblings in the nest always coincide?
Key reference
Moreno-Rueda, G., Soler, M., Soler, J.J., et al. (2007)
Rules of food allocation between nestlings of the
Black-billed Magpie Pica pica, a species showing
brood reduction. Ardea 54(1), 15–25.
Gregorio Moreno-Rueda and his colleagues have
demonstrated that Black-billed Magpie Pica pica
parents respond to the differing needs of their
brood by feeding the chick that begs with the highest intensity. As begging intensity is known to correlate strongly with hunger in this and other species
this does seem to be a sensible strategy on the part
of the adult birds. What would happen though if
insufficient food was available and the whole brood
could not be successfully fledged? (In most birds
there is a strong relationship between size/mass
at fledging and subsequent survival rates.) By
always feeding the hungriest chick the parents may
disadvantage the strongest and therefore reduce
their own reproductive success. Moreno-Rueda’s
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observations suggest that a further refinement of
the behaviour of the parent birds allows them to
avoid this problem.
Flight path: Page 78. Magpie broods suffer losses at
the nestling stage.
Although the parent magpies do preferentially feed
chicks that beg intensely, they also preferentially
feed larger chicks, and because magpie eggs hatch
asynchronously there is often quite a size range
amongst chicks within a brood. In a poor season
therefore smaller chicks will in effect be allowed to
starve so that their siblings can survive.
Key reference
Porkert, J. and Špinka, M. (2006) Begging in Common
Redstart nestlings: scramble competition or signalling
of need? Ethology 112, 398–410.
Brood reduction of this type is not an uncommon
response to resource limitations and in many cases
such as some of the herons, raptors, and parasitic
cuckoos it is the norm. It is often more brutal and
competitor chicks are ejected from the nest, killed
and/or cannibalized by their siblings. However, it
is not the case that all brood mates compete in this
cutthroat way. For example Jiři Porkert and Marek
Špinka have shown that in the Common Redstart
Phoenicurus phoenicurus begging intensity is an honest signal of need (hungrier chicks beg more) and
that like magpies, adult redstarts do preferentially
feed the hungriest chicks. In this species chicks
within a brood vary very little in weight at fledging
suggesting that there is little competition between
them. So do the parent redstarts have other feeding
preferences? Yes they do. They preferentially feed
those chicks that beg most closely to the entrance of
the nest cavity. So does this mean that some chicks
are fed more than others as was the case in the magpie? Through observation of the behaviour of the
nestlings within broods, Porkert and Špinka found
that once it had been fed to satiation a chick typically moved to the back of the nest, allowing its hungry nest-mates to take their turn at the front.
This may not mean however that redstart parents
feed all chicks equally. You may recall that in chapter 4 I mentioned that female birds vary the investment that they make in each of the eggs that they
115
lay. In effect they give favoured offspring a head
start. We have also seen that this kind of differential
parental investment persists after eggs have hatched,
with some chicks receiving more food than others.
It has been recently shown that this phenomenon
can be more sophisticated than we might have
thought. Male Spotless Starlings Sturnus unicolor
have been shown to provide more food for chicks
that hatch from darker shelled eggs. By doing this
the males are thought to favour the chicks that have
hatched from the highest quality eggs. It is also the
case that by some, as yet undetermined means,
male birds are able to assess the likelihood that the
chicks in their brood are unrelated to them and
therefore the result of extra-pair copulations. Having
done so they allocate their feeding accordingly and
preferentially feed those chicks most likely to have
been sired by them. Sometimes of course this
kind of differential allocation of feeding effort may
not be a means of increasing individual fitness by
favouring those chicks that are themselves presumed to be fit, it may simply be a means by which
a pair of birds can make the process of raising a
family more efficient.
Key reference
Draganoiu, T.I., Nagel, L., Musseau, R., and Kreutzer,
M. (2006) In a songbird, the Black Redstart, parents
use acoustic cues to discriminate between their
different fledglings. Animal Behaviour 71, 1039–46.
In the case of redstarts, and specifically the Black
Redstart Phoenicurus ochruros, Tudor Draganoiu
and his colleagues have shown that the members of
a breeding pair each preferentially feed some members of the brood while paying little if any attention
to the others. Often they observed males to feed
fewer of the chicks than females and in some cases
the division of the labour was such that the female
parents fed three times as many chicks as the males.
Although the reason for this behaviour has not
been determined in this species, Draganoiu and his
team have demonstrated that birds are able to recognize the chicks that they will feed. By observing
the response of adults to recordings of chick
begging calls, they have shown that adults are
able to discriminate between the begging calls of
individual chicks.
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ESSENTIAL ORNITHOLOGY
Box 5.7 Helpers at the nest
Raising a family can be a chore and evidence that two
parents are better able than one to do the job is commonly cited in the scientific literature. However there are
cases when even two parents are not sufficient and in
these situations it is common for bands of birds to work
together to cooperatively raise a brood. In some cases a
number of pairs will breed close to one another in a colony, sharing the roles of food finding and defence. But in
some species it is common for a territorial pair of birds to
be assisted in rearing their brood by non-breeding helpers.
One of the cooperative breeding species that we know
most about is the Seychelles Warbler Acrocephalus sechellensis (Figure 5.15).
In the mid 1960s this species was on the verge of extinction with a population of just 26 pairs and was confined to
Cousin Island in the Seychelles archipelago. Effective conservation interventions by the International Council for Bird
Preservation (ICBP) have included the removal of predators,
the planting of trees that support an abundance of the insect
food the birds rely upon, and the translocation of birds to
other islands in the archipelago. As a result the most recent
IUCN assessment of the warbler population (2016) estimates that there are at least 3000 individuals across the
archipelago (Cousin, Frégate, Denis, and Aride Islands) and
that the population continues to grow. As a result the
Seychelles Warbler is no longer considered to be in danger of
extinction and is classified by the IUCN as Near Threatened,
this is an excellent example of a conservation success story.
During the initial period of population growth of Cousin
Island pairs of warblers defended their territories, incubated
their eggs, and raised their families alone. But then as the
population grew it became more common for breeding pairs
of birds to be helped by non-breeding conspecifics. Jan
Komdeur and his colleagues monitored the breeding warblers
throughout this period and Figure 5.16 highlights two key
points. First, the number of occupied territories plateaus in
the early 1980s at about 120, which is thought to be the
carrying capacity of the island. This means that as the population of birds grew, a point was reached where there were
many more breeding age birds than there were territories
available. Secondly, at about that time when the island
became effectively saturated, some birds stopped dispersing
when they became independent and chose instead to remain
on their natal territory as helpers. Confirmation of the
Figure 5.15 Seychelles Warbler Acrocephalus sechellensis (©
Daniel Wade).
Birds
Territorios
200
400
Birds
120
200
100
0
80
Cooperative
breeding
40
55
60
65
70
75
Year
80
85
90
0
Territorios
160
300
Figure 5.16 The growth of the population of
Cousin Island Seychelles Warblers. From Komdeur,
J. (1992) Importance of habitat saturation and territory quality for evolution of cooperative breeding in
the Seychelles Warbler. Nature 358, 493–495.
Reprinted by permission.
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REPRODUCTION
(A)
(B)
530
Annual survival
0.8
0.6
99
435
69
7
31
1.0
4
91
0.4
31
4
6
8 10 12 14 16
Age of female dominant (years)
388
18
190
0.6
33
9
104
0.4
34
Without helper
With helper
0.0
2
2
97
0.2
Without helper
With helper
0.0
42
0.8
211
61
0.2
89
592
Annual survival
1.0
3
2
4
6
8 10 12 14 16
Age of male dominant (years)
18
Figure 5.17 Age dependent survival of female (A) and male (B) Seychelles Warblers who were (solid lines) and were not (dashed lines)
assisted by helpers at the nest. The lines show model predicted slopes derived from the available data. From Hammers, M., Kingma, S.A.,
Spurgin, L.G., et al. (2019) Breeders that receive help age more slowly in a cooperatively breeding bird. Nature Communications 10(1301),
1–10. Reprinted by permission.
generality of this sequence of helper behaviour development has come from ongoing conservation efforts that have
introduced small numbers of the warblers to adjacent Aride,
Frégate, and Denis Islands. In the case of Aride no helping
was recorded until the island had reached its carrying
capacity.
These helpers assist their parents in incubation (females
only), chick feeding, territory defence, and predator mobbing. They are most often found on higher quality territories;
the ones that are particularly rich in insect food and so able
to support a larger population of birds. As territories become
available helpers have a choice—stay on at home or move
out to occupy the vacant space. Researchers have found that
in many ways they act in a manner similar to that predicted
by the Polygyny Threshold Model: When the first vacancy to
arise is in a poor quality territory they stay home and wait
until something better ‘comes to market’. If a high quality
territory becomes available first they moved onto it. Essentially
this seems to be because, considered over a reproductive
lifetime, the immediate term benefit of taking up a low quality opportunity and then staying on that territory for the
remainder of one’s life is less than the benefits to be gained
by waiting until the high quality territories come along.
Remember all of the time that a helper is assisting in the
raising of its siblings or grandchildren it is in effect helping to
propagate genes that it shares with them. In this way a bird
that delays dispersal and breeding is still making an indirect
contribution to its own genetic fitness.
It isn’t just young birds that help, research by Komdeur
and his co-workers has also revealed that grandparents are
helpers too! Over a 24-year observation period almost 14
per cent of breeding females were deposed by one of their
younger relatives. Rather than disperse and become nonbreeding floaters (birds without a territory), 68 per cent of
these grandmothers stayed on and assisted their offspring
in the raising of the next generation. Recent research suggests
that grandparents are able to help in this species because
they themselves were helped as breeders. Martijn Hammers
and colleagues have shown that although survival rates
of breeding male and female warblers with and without
helpers are similar, late-life decline in survival is significantly lower among older females when a helper is present
(Figure 5.17) and a similar non-significant trend is apparent
among older males. Intriguingly the researchers have also
found that the telomeres of older females without helpers
are shorter than those of birds with helpers. Telomere shortening is associated with age-related senescence and so this
suggests that a benefit of having helpers is that they help
breeding females to maintain their body condition, and in
effect to delay the impact of ageing.
Further reading
Richardson, D.S., Burke, T., and Komdeur, J. (2007) Grandparent
helpers: The adaptive significance of older, post dominant
helpers in the Seychelles Warbler. Evolution 61(12),
2790–800.
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ESSENTIAL ORNITHOLOGY
5.5.2 Imprinting and independence
During the nestling and post fledging stage, before
they become fully independent, young birds imprint
upon their parents. This very specific learning process serves to ‘fix’ the species identity of the individual and set it on a behavioural path that will
persist into adulthood. As we saw in the case of the
sensitive period of song acquisition, the imprinting
period is a short and discrete period in the young
bird’s life. As an example of the significance of
imprinting consider the mating preferences of adult
birds that were imprinted upon a ‘parent’ of a species other than their own. If Zebra Finch Taeniopygia
guttata eggs are cross-fostered to be hatched and
reared by the domesticated Bengalese Finch Lonchura
striata parents, the resulting male Zebra Finches
will preferentially court female Bengalese Finches
and ignore females of their own species. For this
reason birds that are hand-reared as part of a conservation programme must be maintained in a carefully controlled environment and provided with
suitable specific stimuli to ensure normal development. Sometimes though there is occasionally an
advantage to inappropriate imprinting. Male raptors
have been hand-reared specifically to imprint them
upon a human trainer and can be encouraged to
mate and ejaculate with their trainer’s gloved hand
to facilitate the collection of semen to be used in
artificial insemination programmes.
Eventually, if a chick has survived the competition with its siblings, the vulnerable period in the
nest and the risky business of fledging into a hostile
environment there comes a time when it must
become independent. In some cases birds remain in
extended family groups (see Box 5.7) but in most
cases they drift away from, or are chased away by,
their parents to disperse and begin their adult life.
Marion Germain and co-workers have explored
the potential impact of dispersing to an unfamiliar
area by capturing and translocating members of a
population of Collared Flycatcher Ficedula albicollis
shortly after they arrived on their Swedish summer
breeding grounds. Some of the birds were simply
captured and released, while others were captured
and moved to a new area. This was done to separate
the effects of capture per se from the effects of displacement. Some of the translocated birds found
their way back to their capture site and bred there,
others bred at their release site. By comparing the
14.6
N = 203
Predicted nestling body mass (g)
14.4
N = 1210
14.2
N = 640
14
13.8
N = 140
13.6
13.4
13.2
Non
experimental
Control
Displacedreturned
Displacednot returned
Figure 5.18 Although birds that were displaced from their breeding area reared lighter nestlings than birds that had not been displaced, those
that did find their way back to their initial breeding site reared heavier nestlings than those that did not. From Germain, M., Part, T., Doligez, B.,
et al. (2017) Lower settlement following a forced displacement experiment: nonbreeding as a dispersal cost in a wild bird? Animal Behaviour 133,
109–21. Reprinted with permission from Elsevier.
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REPRODUCTION
reproductive success of these experimental birds
with the control birds, and birds that had not been
captured at all, the researchers have provided evidence that there is a cost associated with breeding
in a novel area. Figure 5.18 shows that birds that
bred in a novel area reared lighter nestlings than
birds that found their way back to their initial capture site and birds that were not moved. As we saw
earlier in the chapter, nestling size is a measure of
reproductive success because smaller fledglings are
less likely to survive than heavier ones.
119
Summary
As a result of anisogamy the priorities of males and
females differ—although of course both are primarily driven to pass on their genes. Consequently
a wide range of mating/breeding strategies has
evolved. Females choose males on the basis of song,
display, resource provision or genetic quality, and
males compete for access to mates. Chicks manipulate their parents but mothers and fathers may also
manipulate the care that they provide.
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C H A PT ER 6
Foraging and avoiding predators
‘A curious bird is the Pelican, its beak can hold more than its belly can!’
D.L. Merritt, Nashville Banner (1913)
Birds need to eat and drink. The basic principles of
foraging for food and water are common to all species be they a predatory owl, an herbivorous goose,
a generalist omnivore like the crows, or a highly
specialized feeder like the nectivorous hummingbirds. Food or water has to be found, captured or
obtained, and then processed and ingested. At the
same time a foraging individual has to make decisions about food quality, perhaps choosing one item
over another, make decisions about how much to
eat and in some cases how much to store, and make
decisions about when to share with flock-mates and
when to defend the resource. Think about this next
time you watch a feeding bird—their behaviour
may not be as simple as it appears!
Chapter overview
6.1
6.2
6.3
6.4
Finding food and capturing prey
Optimal foraging
Risk and foraging
Predator avoidance
6.1 Finding food and capturing prey
In chapter 3 we saw that birds such as the chickadees and titmice are able to relocate previously
stored food by impressive acts of memory. In many
cases, however, foraging involves the location and
acquisition of previously unidentified food sources
and involves the use of the full range of senses.
Flight path: Foraging can involve navigation and
spatial memory. page 66.
Birds have highly developed eyes and high visual
acuity, so it should come as no surprise that many of
them rely upon sight to locate prey. Some such as the
hawks and owls have forward-pointing eyes that
facilitate binocular vision—essential for a bird that
grabs moving prey. Others have eyes more towards
the sides of their heads, a compromise between binocular vision for prey capture and something closer
to monocular vision, with a wider field of view, for
predator avoidance. These birds often have to cock
their head from side to side to get an accurate fix on
their target prior to pecking. Of course there are occasions when sight is not sufficient. Nocturnal owls can
see by moonlight, but they rely to a greater extent
upon their hearing to locate prey. Similarly it has been
demonstrated experimentally by Robert Montgomerie
and Patrick Weatherhead that American Robin Turdus
migratorius listen out for their prey too. Although foraging robins do use visual cues when hunting for
worms in leaf litter and soil, they are less able to locate
their prey when it is immobile or if the sounds made
by crawling worms are masked by white noise. This
suggests that robins use auditory cues to find worms.
Key reference
Montgomerie, R. and Weatherhead, P.J. (1997) How
robins find worms. Animal Behaviour 54, 143–51.
Wading birds feeding on soft sediments are able
to see prey and visual cues to the presence of prey
Essential Ornithology. Second Edition. Graham Scott, Oxford University Press (2020). © Graham Scott (2020).
DOI: 10.1093/oso/9780198804741.003.0006
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F O R A G I N G A N D AV O I D I N G P R E D ATO R S
(worm casts and burrow mouths) during the day or
under a bright moon. However, the pressures of
feeding between the tides mean that these birds
often have to feed when they are unable to see well,
and of course long billed birds like curlews cannot
see the prey that they seek when they probe deep
into soft mud. In such cases waders feel for their
food. The tip of the wader beak is sensitive to touch
and able to discriminate prey from non-prey. Smaller
billed waders, sandpipers, and plovers, use a similar tactic when searching for surface prey in the
dark. By day they can see their prey and dart across
the sand to snatch it up with a single, well aimed
peck. At night they hunt by ‘stitching’ repeated,
rapid jabs at the sand/mud as they walk across it
(like the stabbing of a sewing machine needle—
hence the term stitching), occasionally swallowing
food that they encounter.
Nocturnal kiwi feed largely on burrowing earthworms that they capture by probing into soft earth
with their long beak in much the same way as the
121
long billed waders. In this case however smell rather
than touch seems to be the important sense. Whereas
the nostrils of most birds are situated at the base of
the beak, those of the kiwi are close to the tip. It seems
that they find their prey by sniffing out burrows.
Similarly it has recently been shown that some of the
oceanic albatrosses and petrels are stimulated to follow the scent of pyrazine. This is a chemical compound that is released when plankton and krill are
eaten by fish or other birds. This might explain how
some species are able to home in on patchily distributed but locally super-abundant swarms of krill.
Unfortunately many species of seabird hunting krill,
squid, and jellyfish accidentally consume marine
plastic pollution with fatal results (see Box 6.1).
Key reference
Nevitt, G., Reid, K., and Trathan, P. (2004) Testing
olfactory foraging strategies in an Antarctic seabird
assemblage. Journal of Experimental Biology 207,
3537–44.
Box 6.1 Plastic pollution
Plastic pollution is a global problem, and marine plastic pollution is known to impact seabirds in particular. In fact more
than half of the world’s seabird species have been reported
to have ingested potentially harmful plastic fragments. It is
currently estimated that between 15 and 51 trillion pieces of
plastic, or 250,000 tonnes, are currently floating in the seas
and oceans of the world. In spite of an increasing global
awareness of this issue it is likely that the scale of the problem will continue to increase for at least the medium-term
future. Marine plastics are ubiquitous but tend to concentrate in hot-spots such as the Southern Ocean boundary of
the Australasian Tasman Sea, which is coincidentally one of
the sites of greatest seabird biodiversity on the planet.
Plastic ingestion by seabirds is not a new phenomenon, it
was first reported in the 1960s. I remember vividly my initial
surprise when finding small plastic pellets in the regurgitated stomach contents of the young Scottish Fulmars that I
ringed as part of a monitoring programme in the 1990s
(regurgitation is a highly effective defence strategy employed
by the immobile chicks). The potential scale of the problem,
and growing public outrage at the environmental impact of
plastic pollution have, however, intensified in recent years.
To better understand the impact of plastic pollution
upon seabirds, Lauren Roman and her colleagues collected
the bodies of more than 1,700 birds of 51 Procellariiform
species from sites around Western Australia, Tasmania, and
New Zealand, and examined them to determine cause of
death and to record the amount and type of plastic that
they had ingested. They recorded plastic ingestion by individuals of all of the species encountered, but as Figure 6.1A
shows, the level of plastic ingestion varied and so it seems
likely that not all species are equally at risk of consuming
plastic. So why the variation? Based upon their analyses
the researchers believe that the foraging strategy employed
by a species determines the likelihood that it will encounter and ingest floating plastic debris. The albatrosses for
example, hunt for fish below the water surface and as a
consequence encounter and consume less plastic than say
the storm petrels who flutter across the surface picking up
shallow swimming crustacean (which bear a more than
superficial resemblance to fragments of floating plastic).
Species that consume squid are also thought to be particularly at risk because balloon fragments and some other
marine plastics look very like squid. In this study all of
the species found to have ingested balloons typically
hunt squid.
continued
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ESSENTIAL ORNITHOLOGY
Box 6.1 Continued
(B)
40
(A)
Albatrosses
Giant petrels
30
Procellarine petrels
Sum of Debris
Fulmarine petrels
Gadfly petrels
Shearwaters
Prions
20
Storm petrels
Diving petrels
10
0
10
20
30
Number debris of items ingested
40
0
KND
Ind
KD
Figure 6.1 (A) The numbers of items of plastic that had been ingested by birds in each of the Procellariiforme taxonomic groups, and
(B) the quantity of marine debris that had been ingested by birds that have died as a result of debris ingestion (KD), where death was not
related to debris (KND), and where the ingestion of debris may have played some part (Ind). From (A) Roman, L., Bell, E., Wilcox, C., et al. (2019)
Ecological drivers of marine debris ingestion in Procellariiform seabirds. Nature Scientific Reports January. (B) Roman, L., Hardesty, B.D., Hindell,
M.A., and Wilcox, C. (2019) A quantitative analysis linking seabird mortality and marine debris ingestion. Nature Scientific Reports March.
But how much of a problem is plastic ingestion? Of the
birds examined 32 per cent had ingested between 1 and 40
pieces of plastic, typically hard plastic fragments and pellets
(92 per cent of pieces). Less commonly ingested items included
balloon fragments, rubber pieces, fishing debris, and soft
packaging. Although the researchers were only able to attribute plastic ingestion as the cause of death in a small number
of cases (13 birds), they were able to determine that plastic
ingestion probably played a significant role in the mortality of
6.1.1 Sharing information
Although petrels may follow pyrazine slicks to
locate food, if the krill are under attack by other surface feeding birds the visual stimulus of a feeding
27 per cent of their sample (459 birds). The more plastic a bird
had ingested, the higher the mortality risk (Figure 6.1B). The
13 birds that were known to have died directly as a result of
plastic ingestion did so because their gut wall had been perforated by hard plastic, or because their gastrointestinal tract
had been blocked by plastic. Although balloon fragments were
relatively rare (just 2 per cent of all fragments recovered) birds
that has swallowed balloon pieces were 32 per cent more
likely to die than birds that had ingested hard plastic.
frenzy is likely to be a very strong cue to any bird in
the area as to the whereabouts of that food patch.
The idea that birds might use the sight of the success of other foraging birds as a cue to the hunt is
encapsulated in the ‘information transfer hypothesis’
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123
Number of departures from colony
F O R A G I N G A N D AV O I D I N G P R E D ATO R S
No
information
No
fish
Winter
flounder
Alewife
Pollock
Smelt
Figure 6.2 Departures from an Osprey colony are more common when birds have observed a successful colony-mate returning with a shoaling
fish. From Greene, E. (1987) Individuals in an osprey colony discriminate between high and low quality information. Nature 329, 239–41.
Reprinted by permission.
which simply predicts that animals should act upon
information from others for their own benefit. In the
case of a petrel flying towards a mob of feeding birds
there is of course no suggestion that the cue is an
intentional signal designed to recruit others, but in
some cases intentional communication does seem to
be used to recruit flock-mates to good feeding areas.
During observations of a colony of Osprey Pandion
haliaetus, Erik Greene noted that whilst birds returning to the colony after an unsuccessful fishing trip
flew directly to their nest or favoured perch, birds
that had been successful (they were carrying a fish)
did not. Instead successful birds performed an elaborate undulating display flight accompanied by a
persistent call. Greene hypothesized that if these
birds were intentionally advertising their success
then their colony-mates should take advantage of
the information provided to them and fly out to
hunt more often when they are ‘told’ that fish are
available, and fly most often in the direction from
which the successful hunter approached the colony.
This is exactly what he recorded happening.
There is an added sophistication to this behaviour.
From Figure 6.2 it is clear that when the returning
hunter carries an Alewife, Pollock or Smelt into the
colony there is an increase in the number of birds
setting out on a hunting trip (compared to the number setting out with no information or with negative information). The figure also shows that when
the hunter returned with a Winter Flounder colony
mates did not respond. This is because unlike
the shoaling Alewife, Pollock and Smelt, Winter
Flounder is a solitary fish.
6.1.2 Foraging flocks
Sharing information and working together can
enable birds to forage more efficiently as a flock and
to have a higher level of success than they would
were they to forage alone. For example, experiments with captive flocks of fishing Black-headed
Gull Larus ridibundus have shown that as flock size
increases, the likelihood of an individual catching a
fish also increases (Figure 6.3). This is probably
because fish fleeing from lots of predators are likely,
in their confusion, to blunder into the beak of one of
them rather than because the birds are actively
working together.
In the case of the Harris Hawk Parabuteo unicinctus however, real cooperation is the order of the day.
Groups of hawks gather in the early morning and
then spend the day actively searching for prey in an
extended flock. Individual hawks leap-frog over
one another as they search for rabbits and other
small mammals (see Figure 6.4).
Once one hawk has found a prey animal the
others in the group converge upon it and then they
work together to move it into a position from which
one or more of them can launch an attack. Sometimes
they drive the animal into the open and then several
birds pounce upon it from different directions. If
the prey takes to cover, one bird will follow it to
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ESSENTIAL ORNITHOLOGY
Average number of fish eater
40
Flock of 6 birds
Flock of 3 birds
Single bird
30
20
10
0
1
5
Trial number
10
Figure 6.3 Birds in larger flocks are more successful when hunting than are solitary birds. From Göttmark, F., Winkler, D., and Andersson,
M. (1986) Flock-feeding on fish schools increases success in gulls. Nature 319, 589–91. Reprinted by permission.
Cottontail kill
N
14.28
14.31
Five hawks
Fed until 15:50
12.40
13.17
Unsuccessful
strike at prey
13:47
14:21
12:27
Start monitoring
13:48
14:05
13:51
13:58
14:01
0
500 m
Figure 6.4 Sequence of movements of Harris Hawks during an ultimately successful hunt. Perched hawks indicate the number of birds recorded
in the group at that time and location. From Bednarz, J.C. (1988) Cooperative hunting in Harris' Hawks (Parabuteo unicinctus). Science 239,
1525–7. Reprinted with permission from AAAS.
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125
flush it out towards the others who are waiting in
ambush. When a kill is made all members of the
group share in the meal and it would appear that a
single rabbit is sufficient to satiate several hawks.
Solitary Harris Hawks are rarely seen hunting and
so cooperative hunting would appear to be the
norm in this species. Indeed Bednarz suggested that
on the basis of his observations it is probably the only
way that Harris Hawks can survive in the harsh
desert environment of southeastern New Mexico.
return a little too early to beat their competitors.
Observations of grazing geese made by Herbert
Prins and his co-workers have shown that on Dutch
saltmarshes Brent Geese do cooperate to re-crop
areas on a four-day rotation. They have also shown
(by experimentally clipping the plants) that four
days is the optimal time to return to maximize the
amount of new growth material available to them.
So it would seem that cooperation is as much of an
advantage to herbivores as it is to predators.
6.1.3 Do herbivores cooperate?
6.2 Optimal foraging
It is easy to see how, by confusing prey or cooperating to overcome it, gulls and hawks are coordinating
their behaviour to maximize their individual success. But can the same ever be said of herbivores?
Plants do not need to be overcome, nor do they try to
escape (although of course it would be wrong to
think that they were defenceless—just grasp a nettle!). Later in this chapter we will see that flock formation in herbivorous birds may be a predator
avoidance strategy but here I would like to consider
the possibility that it is also a means by which birds
can maximize their individual success in terms of the
quality of the food that they have available to them.
The geese that we have just considered are behaving as ‘intelligent foragers’ in an optimal fashion.
That is to say their behaviour is exactly what we
would predict if they are attempting to maximize
the benefits (food intake) of their activity at the
same time as minimizing the costs.
Many species of coastal bird feed upon intertidal
molluscs. Some like the Eurasian Oystercatcher
Haematopus ostralegus use their beaks to open their
prey, and as an aside they have evolved two distinct
morphologies and behaviours to do this. Some oystercatchers have sharp pointed beaks that they use to
stab between the valves (shells) of their prey and then
prise or twist the shells apart to access the flesh. Others
have a heavy, blunt ended beak that they use as a
hammer or chisel to smash open the shells of their
prey. Gulls and crows however use a different strategy. Having selected a potential prey item they carry it
into the air and drop it to shatter on the rocks below.
During a study of the whelk dropping behaviour
of Northwestern Crows Corvus caurinus Reto Zach
noted that birds were very selective when choosing
a whelk to drop. Although whelks ranging from
around 1.5 cm to 5 cm were available in the environment, the crows preferentially selected larger whelks
for dropping (see Figure 6.5A). He also noted that
they consistently dropped whelks from a height of
around 5 m and tended to have preferred drop-zones
(which were littered with broken shells).
Through a series of experiments Zach ruled out
the possibility that smaller whelks were unpalatable (crows were equally likely to consume the flesh
of smaller and larger whelks when presented with a
choice). He also found that larger whelks broke more
easily than smaller ones when dropped (Figure 6.5B)
and unsurprisingly provided the greatest reward
Key reference
Prins, H.H.T., Ydenberg, R.C., and Drent, R.H. (1980)
The interaction of Brent Geese Branta bernicla and
Sea Plantain Plantago maritime during spring staging:
Field observations and experiments. Acta Bot Neerl
29, 585–96.
In Europe, Brent Geese Branta bernicla spend the
winter on temperate estuaries and salt-marshes
where they feed on coastal vegetation, and in particular on Sea Plantain Platago maritima. The plants
that they eat are not particularly nutritious but they
are abundant and supplies are replenished through
re-growth within a few days of grazing. New shoots
are more nutritious than old growth. So we would
predict that the best strategy for a bird is to feed on a
patch and then to stay away from it until re-growth
has occurred—but not to stay away so long that the
growth becomes old and tough. Of course this can
only work if all of the members of a flock coordinate
the way that they re-graze particular patches. If they
do not then birds would probably always attempt to
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ESSENTIAL ORNITHOLOGY
(A)
PER CENT FREQUENCIES
30
20
10
0
1.4
NUMBER OF DROPS
PER WHELK
(B)
2.6
3.2
3.8
LENGTH (cm)
2.0
60
4.4
5.0
SMALL
MEDIUM
LARGE
40
20
0
1
3
5
7
9
11
HEIGHT OF DROP (M)
13
15
Figure 6.5 (A) Although whelks ranging in size from 1.4 cm to 5 cm in length were available (white bars) crows preferentially selected rarer,
larger whelks (black bars). (B) Large whelks require fewer drops to break their shells than do smaller whelks. From Zach R (1979) Shell dropping:
Decision-making and optimal foraging in Northwestern Crows. Behaviour 68, 106–17.
(having most flesh). He also found that shells were
more likely to break if he dropped them in the
crows’ preferred drop-zones than if he dropped
them elsewhere. But most significantly, he calculated that by making multiple drops from 5 m
(rather than fewer from a higher height) the birds
maximized their net energy return when they ate the
whelk (net energy return remember is the amount of
energy obtained from the food minus that spent finding it and making the flights to break it). He showed
that the birds were foraging in an optimal fashion.
6.2.1 Feeding territories
As we saw in chapter 5 one of the functions of a territory is to provide the resources a bird or a pair or
group of birds need to raise their young. But many
birds retain their territories (or acquire new ones)
outside of the breeding season. In some cases these
non-breeding territories occupy all or most of the
same area as the breeding territory and it is likely
that they are retained between years to facilitate
breeding. Others are only held outside of the breeding season and so their prime function seems to be
to provide the holder with access to sufficient food.
In this respect some territories may be quite small
and persist for a very short period.
For example Sanderling Calidris alba congregate
on beaches in feeding flocks and large numbers of
birds can often be seen feeding alongside one
another. However, these diminutive waders may,
under certain conditions, defend small feeding territories. Myers and co-workers made observations
of the flocking and territorial behaviour of Sanderling feeding on the isopod Exirolana linguifrons
on a sandy beach. Their results (Figure 6.6)
indicate that the decision to defend a territory
depends upon the amount of food available. They
found that when prey were scarce birds fed alongside
one another, presumably it would be impossible for
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% of area defended by sanderlings
100
80
60
40
20
0
200
400
600
800 1000
Density of prey (animals/m2)
1200
Figure 6.6 Sanderling defend feeding territories only at
intermediate prey densities. From Myers, J.P., Connor, P.G., and Pitelka,
F.A. (1979) Territory size in wintering sanderlings: the effects of prey
abundance and intruder density. Auk 96, 551–61. Reprinted by
permission of Oxford University Press.
an individual to defend an area large enough to
provide sufficient food. Similarly, when food is
super-abundant there is presumably no need to
defend the resource and birds do not have territories. However, at intermediate prey densities (and
the thresholds involved are quite narrow) the birds
do become territorial. Here the costs of defence are
outweighed by the benefits of controlling access to
the available food.
Key references
Gill, F.B. and Wolf, L.L. (1975) Economics of feeding
territoriality in the Golden-winged Sunbird. Ecology
56, 333–45.
Geerts, S. and Pauw A. (2009) African sunbirds hover
to pollinate an invasive hummingbird-pollinated plant.
Oikos 118, 573–9.
The actual energetics of the trade-off involved in
this kind of territorial defence have been investigated in the case of the old world sunbirds and new
world hummingbirds. Both rely to a great extent
upon energy rich nectar and nectar availability is
a key determinant of territory size. For example
in a now classic study of the foraging energetics
of Golden-winged Sunbird Nectarinia reichenowi,
Frank Gill and Larry Wolf showed that in defended
patches of flowers nectar levels were higher than in
undefended patches. They calculated that birds
defending patches expended around 26 kJ of energy
127
during an eight-hour observation period, whereas
those birds without a territory spent around 32 kJ.
Sunbirds generally feed on nectar whilst perched
on flowers but recently the invasion of parts of
South Africa by a new world plant, Nicotina glauca,
which is usually pollinated by hovering hummingbirds, has resulted in a startling behavioural development. Sjirk Geets and Anton Pauw have reported
that the members of a community of Double-collared
Sunbirds Cinnyris afer and Malachite Sunbirds
Nectarinia famosa (Figure 6.7) have started to hover
to obtain nectar from Nicotina glauca (and to pollinate the flowers in the process). The effects of this has
been that areas with Nicotina glauca support larger
numbers of sunbirds than do areas with only native
flower species present, and sunbirds delay their seasonal migration spending longer in Nicotina-rich
areas than would previously have been the case.
Recent advances in technology are providing
ornithologists with unprecedented insights into the
foraging behaviours of difficult to observe species.
Take for example the Thick-billed Murre Uria lomvia, a generalist fish-eater that spends most of its
foraging time at sea. Until recently the only way
that we could have studied their diet would have be
to record the food items that they brought back to
their breeding colonies to provision their chicks.
But by attaching an array of data collection devices
(biologgers) to murres (see Figure 6.8) Émile
Brisson-Curadeau and Kyle Elliott have gained a
far more detailed understanding of murre behaviour. They attached camera loggers, GPS locators,
and depth recorders to birds and with them were
able to record where birds travelled to catch their
prey, how deep they dived when hunting it, how
long it took them to handle it, and what it was.
These data enabled the researchers to test predictions about foraging behaviour made by the Central
Place Foraging Theory (CPFT) proposed by Orions
and Pearson. The CPFT predicts that when foraging
from a central place (such as a breeding colony)
birds should select larger prey if they travel a long
way to hunt (and smaller prey when hunting close
to the colony). It also suggests that adults should
select larger prey when hunting to provision their
chick than they do when they are self-feeding.
The data collected confirmed the predictions of the
CPFT. On average murres travelled further and dived
deeper when provisioning chicks than they did when
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ESSENTIAL ORNITHOLOGY
Figure 6.7 A hovering Malachite Sunbird taking nectar from Nicotina (© Sjirk Geerts).
incubating and self-feeding. In fact provisioning
phase dives were on average 47 m deep whilst incubation phase dives reached only 27 m. Furthermore the
rate of capture of larger prey (cod for example) was six
times higher when chicks were being fed than when
birds were self-feeding and the diet of adult birds
was almost entirely composed of small amphipods
(shrimps, etc.). GPS data revealed that larger prey like
cod were typically caught some 35–45 km from the
colony, whereas trips to catch the smaller amphipod
prey were generally shorter than 10 km. Interestingly
however, the data also revealed that individual
birds tended to specialize in particular prey types
and to hunt for their prey in particular areas.
Key references
Figure 6.8 This Thick-billed Murre Uria lomvia is wearing a data
logger, in this case a depth-temperature-accelerometer, on its back.
The bird hasn’t been injured—the red mark on its breast is a dab of
paint used by the researchers to quickly re-find the bird in its colony
when they need to retrieve their hardware (© Kyle Elliott).
Brisson-Curadeau, É. and Elliott, K.H. (2019) Prey
capture and selection throughout the breeding season
in a deep-diving generalist seabird, the thick-billed
murre. Journal of Avian Biology 2019, e01930.
Orians, G.H. and Pearson, N.E. (1979) On the theory
of central place foraging. Annual Review of Ecology
and Systematics 157–77.
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129
Box 6.2 City living
City living birds can get something of a reputation for being
a nuisance when it comes to the dietary shift that often
accompanies urbanization. In my hometown for example,
Herring Gulls Larus argentatus are viewed by some as being
a real pest because of their habit of stealing food from the
hands of incautious tourists. The local council do warn
visitors—there are posters all over the place explaining that
the gulls will steal food, that we can all do our bit by taking
sensible precautions when eating out of doors, and, by not
encouraging gulls to see people as a provider of food.
Despite these warnings many of the same people that will
cry foul when robbed of their chips can be seen throwing
their food scraps to the gulls because we do all like to feed
the birds!
So what characterizes a successful city living bird? Through
a comparison of urban and non-urban species Facundo
Xavier Palacio has shown that those species of bird that
thrive in an urban setting tend to have features in common.
They tend to be larger than non-urban congeners and to
have a broader diet, typically feeding on the ground or
aerially, traits that enable them to exploit the diversity of
resources available (seeds, carrion, and human waste). Nonurban comparison species on the other hand feed more
often in the mid strata and canopy of wooded areas, they are
more likely to include fruit in their diet and they are more
likely to be specialist insectivores or granivores. But when I
think about the birds I see in urban gardens I do see specialists some of the time and that is probably because supplementary garden bird feeding directly supports species with
quite specific dietary needs (Figure 6.9). As an example in the
Figure 6.9 This Marsh Tit Poecile palustris is taking advantage
of a garden bird feeder filled with shelled sunflower seeds
(© Margaret Boyd).
UK, Goldfinch Carduelis carduelis only really became common garden birds in the late 1990s when people started to
put out the niger seed that they particularly like.
Globally garden bird feeding is a multi-billion dollar
industry and one that an estimated 50 per cent of all households in the UK and the USA enjoy. In the UK it has been
estimated that homeowners supply enough additional food
to support 196 million garden birds (more than twice the
actual number). I am fifty years old and can remember feeding birds in my own garden from a very early age. Back then
in the UK we mostly fed birds peanuts and kitchen scraps,
today we provide an amazing array of foods specifically
‘formulated’ to attract particular species to the garden and
delivered via an equally amazing variety of bird feeders.
Across Europe and North America garden bird feeding has
modified local food abundance, particularly during the winter months (we tend to feed birds when we perceive them to
be suffering from a resource shortage or as having a particularly hard time). As a result it is likely that we have had, and
continue to have, a significant impact upon the health and
composition of bird communities. Using 40 years’ worth of
data collected by the British Trust for Ornithology, Kate
Plummer and her colleagues have described increased use of
garden feeders by a number species of bird and have shown
that as a result of the range of food types that are offered,
the garden bird community is more diverse today than it has
ever been and that in fact more than half of the species of
birds known to breed or winter in the UK can now be seen
in urban gardens. Moreover the populations of urban birds
that use garden feeders are increasing (those that do not are
not) probably due to a combination of increased survival,
enhanced physiological fitness, and increased productivity.
Experimental evidence to support this has also been provided by Kate Plummer and her colleagues in a related study
of non-urban birds. In this work the researchers explored the
impact of supplementary winter feeding on populations of
Blue Tits Cyanistes caeruleus resident in British woodlands.
Before their experiment the team assessed the body condition of the birds by measuring the carotenoid concentration
of their feathers, taking advantage of the fact that Blue Tits
moult before winter when the feeding would take place.
Over the winter period they provided some populations of
birds with no additional food, some received fat-rich foodstuffs, and others were given a fat-rich diet enriched with
vitamin E. During the subsequent breeding season, the team
assessed the body condition of birds and recorded their
breeding success. Their results showed that whilst a fat-rich
continued
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Box 6.2 Continued
diet actually led to poorer breeding season body condition, a
fat-rich diet with added vitamin E did improve the overwinter
survival and breeding condition of birds, particularly those who
started the winter in poorer shape. These results suggest that
it is the type of food that is provided rather than the provision
of food per se and that dietary balance rather than sheer
volume is key. So we should think carefully about the quality of
the food that we put out for the birds in our own gardens.
Poor diet is only one of a number of potential drawbacks to
supplementary garden feeding. As birds are concentrated in
gardens the risk they face from domestic cats and other predators also increases and it has been estimated that domestic
cats kill billions of birds annually. There is also evidence that a
concentration of birds at bird feeders presents an increased risk
of disease transmission, particularly if our feeder hygiene is
poor. In the UK during the early years of this century the numbers of Greenfinch Carduelis chloris and Chaffinch Fringilla
coelebs declined markedly as a result of trichomonosis, a disease caused by the protozoal parasite Trichomonas gallinae. It
is suggested that the disease jumped from pigeons to doves
and finches when these species were brought into close proximity at bird feeders (the incidence of the disease began to
increase shortly after pigeons became markedly more common
in gardens), and then spread quickly at feeders where birds fed
in close, possibly artificially close, proximity to one another.
Some 50 per cent or 2.5 million greenfinches are thought to
have died between 2005 when the disease reached epidemic
level and 2009. In my own garden a Greenfinch is now
something remarked upon, a bird that once I took for granted.
Confirmation that crowded feeders are sites of disease
transmission has been reported by Sahnzi Moyers and her
co-workers who carefully monitored the feeding behaviour
a
6.3 Risk and foraging
Flight path: Mixed species flocks divide up a resource
to minimize competition. page 147.
So far we have considered foraging as an isolated
behaviour but of course in reality finding food is
just one of a number of concurrent activities undertaken by an individual. The individual doesn’t just
have to decide what to eat it also has to decide when
to eat it. This might involve storing food during a
glut as a way to survive a future shortage, like
the Coal Tits discussed in chapter 3. It might also
involve weighing up the risks of feeding against the
and disease state of captive house finches in experimental
conditions. The researchers inoculated individual House Finches
Haemorhous mexicanus with a common bacterial low virulence pathogen Mycoplasma gallisepticum and then allocated them each to flocks that had access to different
numbers of feeders, simulating different feeding densities.
Although overall rates of disease transmission were low,
they were significantly higher in flocks with higher feeding
densities demonstrating that feeding in close proximity to
one another, or at sites frequented by more birds increases
disease transmission risk. So if you are going to feed the
birds make sure that you have a number of feeders in your
garden rather than just one, and clean them regularly.
References
Lawson, B., Robinson, R.R., Colvile, K.M., et al. (2012) The
emergence and spread of finch trichomonosis in the British
Isles. Philosophical Transactions of the Royal SocietyB
367, 2852–63.
Moyers, S.C., Adelman, J.S., Farine, D.R., et al. (2018) Feeder
density enhances house finch disease transmission in
experimental epidemics. Philosophical Transactions of the
Royal Society B 373, 20170090.
Palacio, F.X. (2019) Urban exploiters have broader dietary
niches than urban avoiders. Ibis.
Plummer, K.E., Risley, K., Toms, M.P., and Siriwardena, G.
(2019) The composition of British bird communities is
associated with long-term garden bird feeding. Nature
Communications 10, 2088.
Plummer, K.E., Bearhop S., Leech, D.I., et al. (2018) Effects of
winter food provisioning on the phenotypes of breeding
blue tits. Ecology and Evolution 8, 5059–68.
risks of not doing so (which might ultimately be
starvation). For example many birds are reluctant to
forage far from cover. Titmice, sparrows, and juncos
have all been shown to prefer to feed closer to cover
into which they might flee when disturbed or
attacked and evidence exists that birds are able to
modify their behaviour in response to changing
levels of risk. For example Jukka Suhonen found
that during periods of relatively low predation
risk Crested Tits Parus cristatus, foraging in trees,
utilize both high and low branches and feed close to
the trunk and outwards to branch tips. However
during years when small mammal populations were
particularly low and Pygmy Owls Glaucidium
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passerinum changed their behaviour to hunt birds,
the tits responded by concentrating their own foraging closer to tree trunks where they would be less
likely to be attacked.
131
which they are exposed. In this section I would like
to consider predator avoidance in more detail.
6.4.1 Camouflage
Key reference
Suhonen, J. (1993) Predation risk influences the use of
foraging sites by tits. Ecology 74, 1197–1203.
Lima, S.L., Wiebe, K.L., and Dill, L.M. (1987) Protective
cover and the use of space by finches: is closer better?
Oikos 50, 225–30.
Lima, S.L. (1988) Initiation and termination of daily
feeding in dark-eyed juncos: influences of predation
risk and energy reserves. Oikos 53, 3–11.
On the other hand there are situations in which
birds will take risks, or at least appear to do so. For
example Stephen Lima and his colleagues have
shown that towhees and song sparrows feed further
from cover than would be expected if they were
behaving in a way that would minimize the time
taken to flee to safety. This is possibly because cover
is paradoxically also a risk—many predators make
ambush attacks from cover and in such cases feeding
in the open might be an advantage. Lima’s observations suggest that the finches he studied optimize
their behaviour by arriving at a compromise between
the costs and benefits of proximity to cover.
It has also been shown that when resources are
scarce, or competition close to cover is high, subordinate birds (presumed to be those least able to
compete) will take increased risks and feed in the
open. In another study Lima has shown that those
Dark-eyed Juncos Junco hyemalis starting their day
with the lowest energy reserves (stored fat) are more
likely to start feeding in low light when predators
are more difficult to locate and both nocturnal and
diurnal predators may be active. Birds with sufficient
fat stores are more likely to wait until light levels
and therefore relative safety from predators increase.
Concept
Camouflage
When we find it difficult to see a bird because its
colouration blends with that of its environment
we think of it as being camouflaged. However, it is
important to remember that what one animal sees as
being camouflaged another may not. Birds are able to
see reflected UV light and species that look dull to us
may therefore be very bright to other birds.
Many birds are difficult to see. Some simply skulk
and remain inconspicuous, others have evolved
plumage that is camouflaged. My personal experience of camouflage is one of frustration and amazement. I know first hand how difficult it can be to
find an inconspicuous leaf-warbler amongst a canopy of leaves or a straw-coloured bittern on the
fringes of a reed bed, and on countless occasions I
have almost trodden on a Ringed Plover Charadrius
hiaticula chick as it crouches pebble-like on a rocky
beach (Figure 6.10). But what evidence is there that
camouflage benefits birds by protecting them from
predators rather than from the gaze of a curious
birder?
6.4 Predator avoidance
It is likely that some level of risk is inevitable and
that at some stage of their life-cycle all birds face the
threat of predation. In the preceding section of this
chapter however we saw that by adjusting their
behaviour birds are able to adjust the level of risk to
Figure 6.10 When immobile this Ringed Plover chick is almost
indistinguishable from the pebbles around it (© Graham Scott).
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Key reference
Hutta, E., Rytkönen, S., and Solonen, T. (2003)
Plumage brightness of prey increases predation risk:
an among-species comparison. Ecology 84, 1793–9.
Esa Hutta and co-workers have approached this
question from an unusual angle. Rather than
attempting to show that camouflage reduces predation risk they have demonstrated that the inverse is
true, i.e. that brightness increases predation risk. To
assess vulnerability to predation they looked at the
relative proportions of the remains of bright and
dull plumaged passerine remains found in and
around Sparrowhawk Accipiter nisus nests and
known plucking posts over a 30-year period. Their
analysis revealed that as they predicted, brightly
plumaged species were overrepresented in the
hawks’ diet and were presumably therefore easier
for hunting hawks to catch than were dull plumaged, camouflaged, species.
In another study involving Sparrowhawks and
their prey, Götmark and Olsson have dramatically
demonstrated the cost of increased conspicuousness. To do this they manipulated the plumage of
young Great Tits while they were still in the nest.
Great Tits have striking yellow, black, white, and
greenish plumage which might sound quite conspicuous, but is in fact relatively inconspicuous
against the mottled light and shade of a woodland
canopy. Some of the birds were made less conspicuous by having the white feathers on their cheeks,
wings, and tails painted yellow. Others were made
more conspicuous by having their white feathers
painted red. All of the chicks were fitted with numbered metal rings to facilitate individual recognition and then allowed to fledge normally.
The main predators of fledgling Great Tits are
Sparrowhawks which time the hatching of their
own eggs to coincide with the annual titmouse
glut. Two weeks after the tits fledged the
researchers used a metal detector to search for
their rings in the area of Sparrowhawk nests and
plucking posts. The results of their searches
(Figure 6.11) revealed that red-painted birds were
38 per cent more likely to be predated then yellowpainted birds, evidence that conspicuousness
increases predation risk and that inconspicuousness (camouflage) decreases it.
Tits recovered at hawk nests (%)
132
N = 308
6
N = 365
4
N = 445
N = 537
2
0
Red Control
1994
Red Control
1995
Figure 6.11 The percentages of conspicuous red-painted and
inconspicuous yellow-painted Great Tits recovered from the nests of
Sparrowhawks during two seasons. N indicates the total number of
each class of tits painted in each season. From Götmark, F. and
Olsson, J. (1997) Artificial colour mutation: do red-painted tits
experience increased or decreased predation? Animal Behaviour 53,
83–91. Reprinted by permission from Elsevier.
6.4.2 Predator distraction displays
Plovers and other ground nesting birds are generally well camouflaged, as are their eggs and mobile
young (see Figure 6.10). However in terms of avoiding predation the plovers are better known for their
unusually conspicuous behaviour and habit of
drawing attention to themselves, behaviour which
might at first seem paradoxical in the face of a predation threat.
Plover nests are typically on open ground and a
vigilant bird will detect a threat (a fox or mustelid
typically) when it is still some distance away.
Having identified a predator the plover discreetly
leaves its nest and walks a little distance from it.
The bird will then employ one or more of a number
of anti-predator strategies. Plovers that have been
incubating eggs often sit and pretend to incubate,
allowing the predator to find and flush them. The
bird then flies to safety leaving the hapless predator
to search in vain for non-existent eggs.
In other cases if the plover is in long grass and
cannot be easily seen by the hunter, it will scurry
away uttering a high pitched squeaking sound
effectively impersonating a small rodent. Typically
the predator will give chase and when it has moved
a sufficient distance from the nest or young the
plover will fly to safety. If the predator seems not to
want to follow it the plover will often run towards
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Figure 6.12 This bundle of feathers is a perfectly healthy adult Ringed Plover feigning extreme injury to lure me away from its chicks. Seconds
later it took flight and uttered what I can only describe as a mocking call! (© Graham Scott).
it calling loudly and then at the last moment darting
away, usually followed by the predator which is by
now well and truly hooked.
There is however another behaviour for which
the plovers are renowned, and that I can confirm is
highly effective having fallen for it myself on
numerous occasions. This is the broken-wing display. Having identified a threat the plover will
stand in a conspicuous position and draw attention
to itself with a repetitive pipping call. At the same
time it will lower one wing (feigning an injury) and
start to slowly ‘limp’ away. Presented with such an
easy target the predator gives chase and the plover
following an irregular path leads it away from its
nest or chicks (chicks crouch immobile in response
to an alarm call from their parent). If the predator
appears to lose interest the plover exaggerates its
plight even more, often falling to the ground and
flailing an apparently useless wing (see Figure 6.12).
But as soon as the predator comes close to grabbing
its prey or has moved a sufficient distance from the
nest, the plover utters an almost mocking call and
flies to safety.
6.4.3 Tonic immobility
If these strategies fail and chicks are found, they too
have a ruse by which to effect their escape. When
they are picked up by a predator the chicks of
ground nesting birds exhibit what is referred to as
tonic immobility—basically they become limp and
play dead. Because such chicks tend to come in
groups, predators often drop ‘dead’ chicks in the
hope that they will find another. Of course when
they subsequently return to reclaim their prize they
find it gone. Tonic immobility can be induced if a
chick is presented with a stimulus mimicking two
forward pointing eyes (like those of a predator) and
can be sustained for up to 30 minutes if the stimulus
is not removed. During this time the chicks will
regularly open one eye a little just to check that the
danger is still present.
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ESSENTIAL ORNITHOLOGY
6.4.4 Alarm calls
When they detect a predator, individuals of most, if
not all, bird species produce an alarm call. One of
the functions of such calls, and indeed of other
forms of alarm behaviour, is probably to inform the
predator that it has been detected and that having
lost the element of surprise an attack is unlikely to
succeed. In this way alarm calls could act as a
predator deterrent. The other main function of
alarm calls is to provide flock-mates with the vital
information that a predator has been detected and
to stimulate them to take appropriate anti-predator
actions. Such responses might include becoming
silent and inconspicuous (particularly in the case of
nestlings and dependent young birds), fleeing, or
somewhat paradoxically making one’s presence
known to the predator and even attacking it as we
shall see later in this chapter when we consider
mobbing behaviour.
Walking in English woodland one of the most
common calls that I hear is a high pitched seet.
Usually this is the alarm call of a European Robin
Erithacus rubecula that has been disturbed by my
presence. Through this call the Robin shares with
the wider community of woodland birds the information that I am there and that I am a potential
threat (of course I’m not really!). This multi-species
sharing of information is enhanced because the
alarm calls of most, if not all, of the members of the
community have evolved to become very similar
indeed (see Figure 6.13). Typically they are relatively drawn out calls with a rather narrow frequency range making them very difficult for a
predator to locate accurately. This of course is an
advantage to the birds in that a predator cannot
attack a target that it is unable to locate.
At first glance the alarm call system would therefore appear to be a relatively simple one. However
recent research has revealed that in fact it is often
used in quite a sophisticated way. For example it
has been shown by Christopher Templeton and his
co-workers that Black-capped Chickadees Poecile
atricapillus vary their alarm call in response to the
identity of the predator that they have detected. The
chickadees are named for their chick-a-dee-dee call
which is used as an alarm/mobbing call when
predators are detected. By exposing chickadees to
models of a range of potential predators, the
researchers found that they varied their call, primarily by adding in more repeats of the terminal dee
note, in response to increasing predator size (see
Figure 6.14A). Furthermore, by playing back a range
of chickadee alarm calls they also showed that conspecifics vary their responses to different alarm calls,
taking note of the content of the call and decoding
the potential risk that the predator poses. So for
example they respond most strongly to smaller
predators, which are themselves more likely to attack
chickadees than are larger predators (Figure 6.14B).
Templeton and Greene have also shown that
members of other species in the forest community
are able to decode the messages transmitted between
alarm calling chickadees. For example Red-breasted
Nuthatches Sitta canadensis respond to the alarm
calls of neighbouring Black-capped Chickadees and
take note of more than the presence of a threat. In
response to chickadee alarm calls stimulated by the
presence of a Northern Pygmy Owl Glaucidium
gnoma, a species which also predates nuthatches,
they responded with high intensity alarming and
mobbing. But when the chickadees’ alarm calls
were a response to the presence of a Great Horned
Owl Bubo virginianus, a species which is not known
to hunt nuthatches, their anti-predator response
was far less strong.
Key references
Templeton, C.N. and Greene, E. (2007) Nuthatches
eavesdrop on variations in heterospecific chickadee
mobbing alarm calls. Proceedings of the National
Academy of Science 104(13), 5479–82.
Ridley, A.R., Child, M.F., and Bell, M.B.V. (2007)
Interspecific audience effects on the alarm-calling
behaviour of a kleptoparasitic bird. Biology Letters 3,
589–91.
Concept
Sentinels
Single and mixed-species flocks often include individuals who take on the role of sentinel. These individuals
act as a lookout for the flock, devoting more time to
vigilance and therefore less time to foraging than their
flock-mates.
There is however evidence that heeding the warnings of others may sometimes be a costly behaviour.
Fork-tailed Drongo Dicrurus adsimilis are insectivorous
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9
Blackbird
7
5
9
Great Tit
7
5
9
Blue Titmouse
7
5
9
Chaffinch
7
Stonechat
Wren
Garden
Warber
8
Robin
(B)
Mistle
Thrush
5
Blackbird
Kilocycles\s
Kilocycles\s
Kilocycles\s
Kilocycles\s
(A)
135
Kilocycles\s
6
4
2
0
Time (s)
1s
Figure 6.13 Sonograms of alarm calls (A) and mobbing calls (B) of a range of coexisting European woodland birds. Note that whereas alarm
calls typically have a narrow frequency range, making them difficult to pinpoint, mobbing calls have a wide frequency range and are easily locked
onto by predators. Note also the convergence in the evolution of both types of call. From Marler, P. (1959) Developments in the study of animal
communication. In Darwin’s Biological Work. Bell, P.R. (ed.) Cambridge University Press, Cambridge.
and tend to take prey by hawking it from the air.
They will however also take prey from the ground,
particularly when it has been disturbed by a
ground-foraging bird, a form of kleptoparasitism.
When foraging alone Drongos will alarm call in
response to the threat posed by an aerial predator,
but they rarely call in response to a terrestrial one.
However, when in the company of ground-foraging
Pied Babblers Turdoides bicolor, the Drongos take on
a sentinel role and will alarm in response to both
aerial and terrestrial predators. This of course benefits the Babblers who, relying upon their Drongo
lookouts, reduce the level of their own vigilance
(spending more time foraging) and respond to the
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ESSENTIAL ORNITHOLOGY
Number of D notes per call
(A)
(B)
40
4.5
4.0
Saw-whet
Pygmy-owl
3.5
3.0
Cooper’s
merlin
kestrel
2.5
short-eared
2.0
1.5
1.0
Peregrine
red tail
great-horned
gyrfalcon
great
praine
grey
bobwhite
rough-leg
20 40 60 80 100 120 140
Predator wingspan (cm)
Number of “chick-a-dee” calls
136
30
20
10
0
Control
Large
Small
predator predator
Alarm call treatment
Figure 6.14 (A) Intensity of alarm call (number of dee (D) notes in the call) clearly increases as predator size decreases and chickadees clearly
respond most strongly to hearing alarm calls that are a response to the greater threat posed by the presence of a smaller predator (B). Each
taxonomic group of raptors is represented by a different symbol (⚫ owl; ▲, falcon; ◼, hawk). A bobwhite quail (♢) was used as the procedural
control. The dashed line displays the mean number of D notes per control trial without any stimulus. Adapted from Templeton, C.N., Greene, E., and
Davis, K. (2005) Allometry of alarm calls: Black-capped chickadees encode information about predator size. Science 308, 1935–7. Reprinted with
permission from AAAS.
Drongo alarm by fleeing to the safety of deep cover.
The intriguing question of course is why do the
Drongos go to this effort? Amanda Ridley and her
colleagues have shown that in some cases they use
this relationship to their own advantage. Occasionally
they will alarm dishonestly (i.e. when there is no
predator present) causing the fleeing Babblers to
drop or leave their own prey which is quickly
snapped up by the hungry Drongo. This dishonesty
can persist because it is a strategy that the Drongo
uses sparingly and the Babbler is unable to call its
bluff.
6.4.5 Mobbing
Whilst alarm calls appear to have evolved to have a
frequency range which reduces the chances that a
predator will be able to locate the caller, mobbing
calls in contrast have evolved to be easily located
(Figure 6.13B). As a strategy, mobbing depends
upon the predator knowing that it has been detected
and that an attempt to hunt will probably result in
failure. Mobbing is most commonly observed when
passerine birds respond to the presence of an aerial
predator. It may begin with a single mobbing bird,
calling and diving at the predator repeatedly, perhaps
even striking it. As the behaviour continues other
birds are recruited and very quickly a small flock of
birds will form, all harassing the unfortunate hunter.
Typically, having lost the element of surprise or
because it just cannot take any more, the predator
will move on to hunt elsewhere. Numerous studies
have demonstrated that mobbing is a successful
strategy, and most birders will have seen it at work.
In fact learning to recognize mobbing behaviour
can be a great way to detect predators that you
might otherwise have overlooked!
Mobbing does however have a potential cost and
there are reports of predators taking a mobbing bird
that came too close. This is perhaps why birds
tend to cooperate and mob in flocks. Brown and
Hoogland, in a comparative study involving the
mobbing behaviour of solitary and colonial species
of swallow, have shown that solitary mobbers are
forced to take greater risks (coming closer to the
predator) than are mobbers in flocks (Figure 6.15).
6.4.6 Flocks and colonies
Lowering individual risk and increasing the chance
of success in mobbing birds is just one of the antipredator advantages of group living and/or colonial breeding. Whilst being part of a large and
conspicuous group might on the face of it seem to
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make a bird more obvious to predators, there is in
fact safety in numbers. By breeding in huge colonies,
and synchronizing the hatching of their young, sea(A)
4%
(B)
35%
Colonial species
Solitary species
Figure 6.15 The percentage of mobbing actions that are high risk
(shaded segments) are lower for colonial swallows mobbing as part of
a flock (A) than they are for solitary birds (B). From Scott, G.W. (2005)
Essential Animal Behavior, Blackwell Publishing, Oxford adapted from
Brown, C. and Hoogland, J.L. (1986) Risk in mobbing for solitary and
colonial swallows. Animal Behaviour 34, 1319–23. Reprinted by
permission from Elsevier.
137
birds are able to increase the effectiveness of their
mobbing behaviour to deter predators, and to
simply swamp them with food. There are so many
eggs and chicks available that even the hungriest
of predator populations will make relatively little
impact upon the prey population as a whole.
Conservationists can take advantage of this principle by providing food to divert the attention of
predators away from the species that they are trying
to protect (see Box 6.3).
At a very simple level a phenomenon known as
the dilution effect comes into play as group size
increases. If a bird in a flock of one is attacked by
a predator it has a 100 per cent chance of being the
target of the hunter. A bird in a flock of 2 has a 50
percent chance, and one in a flock of 100 has only
a 1 per cent chance (all things being equal) (see for
example Figure 6.16). This effect is clearly at work
in the large seabird colonies described previously
Probability of attack on individuals
(A)
Mean interscan interval (s)
(B)
0.14
0.11
0.08
0.06
0.03
0
2–5 6–10 11–20 21–3031–40 41–50 51–6061–100
Flock size class
30
20
10
0
1–5
6–10 11–15 16–20 21–25 26–30 31–40 41+
Flock size class
Figure 6.16 Increasing flock size results in a decreasing probability that any individual Redshank will be the target of a predator (A), and allows
individuals to forage for longer between bouts of vigilance (scans) (B). From Cresswell, W. (1994) Flocking is an effective anti-predator strategy in
redshanks, Tringa totanus. Animal Behaviour 47, 433–42. Reprinted by permission from Elsevier.
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ESSENTIAL ORNITHOLOGY
Box 6.3 Feeding predators to protect prey
The Little Tern Sternula albifrons is one of the least common
seabirds breeding in the UK. These terns breed in colonies on
sandy beaches, just above the strandline and are therefore
at risk of inundation, disturbance and sadly, persecution
from people—their eggs and chicks are particularly vulnerable to predation. Conservation efforts are intensive and
include 24/7 observation by dedicated volunteers and nature
reserve wardens as well as fencing to keep people, dogs, and
Kestrel predation (LT chicks
hour–1 ±95%Cl)
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
noDF
DF
Figure 6.17 The average hourly rate of Kestrel predation on Little
Tern chicks with (grey bar) and without (white bar) diversionary
feeding. From Smart, J. and Amar, A. (2018) Diversionary feeding as
a means of reducing raptor predation at seabird breeding colonies.
Journal for Nature Conservation 46, 48–55. Reprinted by permission
from Elsevier.
and it probably also explains the flocking behaviour of female sea duck such as the Eider Somateria
mollissima who bring together their chicks into
often quite large crèches during their first vulnerable days at sea. During this period the chicks are
easy prey for hungry gulls and there is little that
either mother or chick can do to deter an attacking
bird. Instead they rely upon the dilution effect
and the ability of a number of females working
together to spot danger and respond to it (by diving and encouraging the chicks to dive) sooner
than a mother on her own would.
Further evidence that flocking is an effective antipredator strategy has been provided by Will
Cresswell who has carried out an exhaustive study
of the relationship between hunting Sparrowhawks
Accipiter nisus and Peregrine Falcons Falco peregrinus, and their Redshank Tringa totanus prey.
foxes out of their colonies. But in spite of all of this, terns
remain at risk from aerial predators, in particular from raptors such as the Kestrel Falco tinninculus. So what to do?
Although predators are controlled in some conservation
situations (think of the example of rat eradication programmes on seabird islands) lethal control of one threatened species to protect another poses something of an
ethical dilemma to put it mildly. One innovative solution is to
feed the predator. This diversionary feeding as it is known
operates under the assumption that a well fed predator
poses a lesser threat. But does it work? Jennifer Smart and
Arjun Amar have shown that it does.
Taking advantage of the fact that Little Tern colonies are
under intense scrutiny and every predator attempt made by
a Kestrel can be observed, they compared predator success
(and tern success) during years when no diversionary feeding took place and during years when the local Kestrel population was able to feed on dead chicks and mice that were
surplus to the needs of an animal breeding programme. Their
results (Figure 6.17) demonstrate the effectiveness of this
conservation strategy. Not only were significantly fewer tern
chicks taken by Kestrels during years when diversionary
feeding was in place, the predators took fewer items of other
wild prey species. The researchers estimate that this strategy
reduced chick predation from around 275 birds per year to
around 30, a real success story.
Cresswell has demonstrated that the larger a
Redshank flock, the lower the probability that a
given individual will be attacked by predators
(Figure 6.16A). The Redshank in the winter population that he observed faced two basic pressures
each day—the need to avoid being eaten and the
need to gain enough energy themselves. To an
extent the two are in part difficult to reconcile
because a feeding Redshank often has its head
down and so when actively foraging is far less able
to see approaching predators. However, through
group membership, individual birds are able to
increase the interval between bouts of vigilance
behaviour and so maximize feeding time
(Figure 6.16B). This is because in a sufficiently large
group there will by chance always be some individuals on the lookout. There is an additional level of
flexibility in this system in that all members of the
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flock increase their vigilance levels in response to a
heightened perception of risk—immediately after a
predator has been seen in the area for example.
One might expect Redshank that have spotted
a predator to use an alarm call, and some do.
Others however do not. How can this be explained?
Cresswell observed that Redshank did call more
often when escaping from an obvious threat (a raptor
attack) than they did when the cause of their alarm
was not apparent (flocks often simply spook themselves). Furthermore he also noted more alarm calls
by fleeing birds that had been feeding in a habitat
that was visually obstructive (i.e. fellow flock members were not easy to see) than on an open mud-flat.
In the latter habitat they were much more likely to
escape with a silent and direct fast flight to safety.
Both escape behaviours had the same effect on the
rest of the flock—causing all of the Redshank in the
area to take to the air. So as was suggested previously
in the chapter, one function of the alarm call does
seem to be to coordinate an escape. Birds that do
alarm call, potentially drawing attention to themselves, were no more likely than non-callers to be
targeted by the raptor, so calling in itself is not a
high risk strategy in this case. It is a highly effective
strategy though because a coordinated escape presents a hunter with a mass of moving targets making
it impossible for it to pick out one to chase—this is
often referred to as the confusion effect, another
anti-predator benefit of flocking.
Will Cresswell made a number of other important
observations about the behavioural relationship
between avian predators and their avian prey and
I would recommend that any interested reader take
the time to read his numerous papers. But one of
his observations I find particularly intriguing and
139
I will mention it briefly to round off this discussion. Remember that the Redshank Cresswell
observed were attacked by two different predators,
Sparrowhawk and Peregrine Falcon, both of which
use very different strategies to capture their prey.
Sparrowhawk are a stealth hunter—typically breaking low from dense cover and hoping to snatch surprised prey from the ground. Peregrines on the
other hand are pursuit hunters, stooping (a diving
flight) towards prey from a height and at great speed
and preferring to take airborne prey. Cresswell
noted that the Redshank consistently responded to
these predators in different ways. When attacked
by a Sparrowhawk they bolt and escape with a low
zigzag flight pattern. In response to a Peregrine
they freeze and crouch low to the ground. So in just
fractions of a second birds are able to identify a
potential threat, recognize the predator, evaluate its
likely mode of attack and take appropriate evasive
action. An impressive feat, but an essential one—
making a mistake would be fatal.
Summary
Foraging birds utilize a wide range of behavioural
strategies when feeding and that behaviour continues
to evolve to take advantage of new food resources.
Essentially however they forage in an optimal fashion. The anti-predator behaviour of birds is similarly diverse. Some species rely upon camouflage;
some cooperate to confuse a predator. Some take
risks, exposing themselves to danger when mobbing hunters. The provision of supplementary food
can be an important conservation strategy, but providing the right food and maintaining good feeder
station hygiene is essential.
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C H A PT ER 7
Populations, communities,
and conservation
‘Man, however much he may like to pretend the contrary, is part of nature’
Rachel Carson (1962)
Although birds can be found in almost every corner
of the globe it is apparent to even the most casual
observer that they are not distributed evenly.
Some places have more species of bird than others.
Furthermore, whilst some individual species have
very broad distributions, others are often found
only in a particular type of place or even in just one
very restricted area. To explain these patterns we
have to consider some of the characteristics of bird
populations and communities, particularly if essential conservation efforts are to be a success.
very often act in concert. In addition the relationships between populations of species which form
communities (see section 7.2) will mean that a shift
in one population may have consequences for
others and so have an impact at the community and
ecological network level.
Chapter overview
7.1.1 Life history strategies influence
population growth
7.1 Populations
7.2 Communities
7.3 Extinction and conservation
7.1 Populations
Bird populations vary in size dramatically. Populations of some species, such as the African RedBilled Quelea Quelea quelea are counted in their
millions whilst populations of island endemics
might include only a handful of individuals.
Some populations appear to be stable (but fluctuate
around a mean from year to year), others are growing, but many are a shrinking at such a rate that
they are of immediate conservation concern. The
factors governing both population size per se and
trends in population size change are numerous and
Concept
Populations can be defined as those members of
a species which interact and have the potential to
interbreed.
Some species have a naturally low capacity for
population growth because of their particular
life history strategy. Populations of larger birds
with delayed maturation and small or infrequent
clutches are typically slow to grow. For example
although considerable conservation efforts have been
made on their behalf the recovery of the Californian
Condor Gymnogyps californianus (Figure 7.1) has
been painfully slow. These birds have a life span of
some 50 years and take at least six to reach sexual
maturity. When they have found a mate and do
begin to breed their natural rate of productivity is
very low. In 1987 only 22 of these magnificent birds
remained and all of them were captured and taken
into captivity as the basis of a captive breeding
programme. Eventually birds were returned to the
Essential Ornithology. Second Edition. Graham Scott, Oxford University Press (2020). © Graham Scott (2020).
DOI: 10.1093/oso/9780198804741.003.0007
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141
Figure 7.1 This wing-tagged Californian Condor soaring above the Big Sur is the living embodiment of a conservation success story
© Peter Dunn.
2.0
1.5
CBC Index
wild and the conservation programme is a success,
but the total population remains small. By 2017 it
had only grown to 463 birds (290 in the wild and
the remainder in captivity).
Small passerines on the other hand have a much
higher capacity for population growth. A pair of
European Starling for example can reproduce at one
year old and can produce 10 chicks per year (from
two clutches of five eggs) for several years. As a
dramatic example of the kind of population growth
that can result from such a life history strategy consider the fact that in 1890 Eugene Scheifflen introduced a founder population of between 60 and 110
(estimates vary) European Starling into New York’s
Central Park and that in 2009 they were estimated
to be the most numerous bird in the USA (there
were estimated to be more than 200 million of
them). It took them around 50 years to colonize the
USA from east to west and as they did so they
wreaked ecological havoc out-competing native
species for access to nest cavities. Today in the USA
these starlings are considered a pest species, spreading zoonotic disease and causing significant agricultural losses. Where necessary their numbers are
controlled through culling by the application of a
bird-specific pesticide (DRC1339) which is administered as poisoned bait. Paradoxically in the UK the
1.0
0.5
0.0
1960
1970
1980
Year
1990
2000
Figure 7.2 The population of Starlings in the UK declined
dramatically over the period 1960 to 2000 (solid line and 95 per cent
C.I.—dotted lines). The decline in the index used (derived from the
British Trust for Ornithology Common Birds Census) equates to a loss
of more than 50 per cent of the UK population. Robinson, R.A,
Siriwardena, G.M., and Crick, H.Q.P. (2005) Status and population
trends of Starling Sturnus vulgaris in Great Britain. Bird Study 52,
252–60. Reproduced with permission from the British Trust for
Ornithology.
Starling is a bird of conservation concern. Although
not uncommon, the UK population has declined
rapidly in recent years (Figure 7.2), possibly as a
result of changes in agricultural practice that have
reduced food availability and as a result of a loss
of suitable nest sites as building regulations and
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ESSENTIAL ORNITHOLOGY
standards reduce the number of cavities available
in domestic roof spaces.
Concept
Zoonoses are diseases which can potentially be
transmitted from animals to humans, several are known
to be transmitted from birds to man directly and others
involve birds as an intermediate host or vector. See for
example Abulreesh, H., Goulder, R., and Scott, G.W. (2007)
Wild birds and human pathogens in the context of ringing
and migration. Ringing and Migration 23(4),193–200.
7.1.2 Population change
In spite of their intrinsic capacity for growth some
populations are in decline or have their growth
limited in some way. Throughout the remainder of
this chapter we will largely focus upon examples of
such populations. We will consider a range of
factors that check population growth and then we
will go on to consider some of the ways in which
population changes are involved in the structuring
of bird communities.
Populations grow as a result of increased productivity and/or decreased mortality. This may be possible because resources become more abundant as a
result of a climate shift, a human intervention or
even the misfortunes of another species. Or it could
be a result of a decrease in predator pressure, or in
a conservation context because of an increase in protection. On the other hand populations decline when
productivity falls and/or mortality increases, perhaps because predator pressure increases, or a
parasite or disease invades a population. It could be a
result of increased competition as a result of a species
introduction or a range expansion. Alternatively it
could be the result of a shortage in resources because
of poor weather or habitat loss. It could simply be that
an extreme weather event kills lots of birds. Box 7.1
illustrates the impact of species introductions, competition, and disease upon bird populations.
Box 7.1 Aliens, pathogens, and competition
During the second half of the nineteenth century House
Sparrows Passer domesticus were introduced to several sites
across the USA. Today this successful generalist is one of the
most common birds in the USA. It is a pest in many contexts
and is held responsible for preventing the expansion of
populations of native species because it out-competes them
for resources. However, in the second half of the twentieth century things started to go badly for the sparrow, it
lost ground to another alien invader—the House Finch
Carpodacus mexicanus.
House Finches were translocated from their native western USA to Long Island in the east in 1940. This new eastern
population struggled to get a foot-hold initially but eventually it did establish itself and then quickly spread throughout
the eastern states. As the finches spread it was noted that
where they coexisted, sparrow numbers seemed to be falling. Was this more than a coincidence? The diets of the two
species are very similar (both eat mainly seeds and vegetation); they are known to fight over resources when they
meet; and, there were reports that finches were breeding at
sites traditionally occupied by sparrows. It certainly looked
like the finches were competitively dominant with respect to
the sparrows.
Evidence to support this hypothesis came as a result of an
unusual natural experiment, one which in itself provides an
excellent example of the impact of pathogens as a cause of
density dependent population decline. In the 1990s the
eastern House Finch population was still growing strongly
and expanding its range but then in the winter of 1993–
1994 birders in the state of Maryland began to report cases
of a House Finch specific conjunctivitis. Dubbed ‘House Finch
disease’ this was found to be caused by a bacterium,
Mycoplasma gallisepticum, a pathogen previously restricted
to domestic poultry (the same pathogen discussed in Box
6.2). Subsequent research revealed that the disease was
highly contagious and highly pathogenic—as Figure 7.3
shows, as many as 60 per cent of the birds in infected populations died within five years of the disease emerging. It also
spread very quickly, having reached Texas, Missouri, and
Minesota by 1997.
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Population size (% of expected)
P O P U L AT I O N S, C O M M U N I T I E S, A N D C O N S E R VAT I O N
120
100
80
60
40
20
–1
0
1
2
3
4
Years since epizootic began
5
In(counts/party-hour)
Figure 7.3 Changes in House Finch abundance following the
emergence of Mycoplasma gallisepticum in a population. The data
are expressed as changes relative to 100 per cent (year -1, or one
year prior to pathogen emergence). From Hochachka, W.M. and
Dhondt A.A. (2000) Density-dependent decline of host abundance
resulting from a new infectious disease. Proceedings of the
National Academy of Science 97(10), 5303–6. Copyright National
Academy of Sciences, USA.
It seems likely that this pathogen was able to spread so
quickly precisely because of the ecological traits that made
the finches such a successful species in the first place—their
ability to tolerate one another and feed in large compact
flocks (sites of infection) and their ability to rapidly disperse
and colonize new areas (enhancing the geographical spread
of the disease).
What about the sparrows? Remember that as the
House Finch population increased a decrease in sparrow
numbers was recorded. If the population dynamics of the
two species are inter-linked such that finch numbers are
the check on the sparrow population, we should expect to
see the sparrows, being immune to Mycoplasma gallisepticum, to bounce back once the competitive pressure was
released. This is exactly what has been recorded by the
veritable army of professional and amateur ornithologists
in the USA who take part in the annual Christmas Bird
Count (Figure 7.4).
2.5
2.0
1.5
1.0
0.5
0
–0.5
–1.0
–1.5
1965 1970 1975 1980 1985 1990 1995 2000 2005 2010
Key reference
Newton, I. (2007) Weather-related mass mortality
events in migrants. Ibis 149, 453–67.
So, for example it is not unusual for populations of
small passerines to crash during a very cold winter.
Similarly populations of migrants are often dramatically reduced as a result of extreme climate events
either during their migration or shortly after arrival
at their breeding grounds. In his excellent review of
this phenomenon, Ian Newton reports that in 1993 a
single tornado/storm event off the Louisiana coast
resulted in the death of more than 40,000 migrating
birds, and that unseasonal cold snaps in Europe
143
Figure 7.4 Abundance (log transformed) of House
Sparrows (solid line and dotted line) and House Finches
(points) recorded in the Christmas Bird Count (1970–2005).
The shift from a solid to dotted line in the case of the
sparrows indicates the change in the direction of their
population trend coincident with the emergence of
Mycoplasma gallisepticum in 1993/4. From Cooper, C.B.,
Hochachka, W.M., and Dhondt, A.A. (2007) Contrasting
natural experiments confirm competition between House
Finches and House Sparrows. Ecology 88, 864–70.
have on occasion resulted in local hirundine population reductions of as much as 90 per cent.
Key reference
Kluijver, H.N. (1966) Regulation of a bird population.
Ostrich (supplement) 6, 389–96.
Populations that have suffered these crashes often
rebound during the following years (assuming that
mass mortality events are not repeated) because this
mortality event may have lessened competition for
nest sites/territories and food resources during the
following spring, allowing a productivity increase
for those birds fortunate enough to have survived.
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ESSENTIAL ORNITHOLOGY
Natural experiments like this have been duplicated under controlled conditions and similar
effects measured. For example Hans Kluijver has
simulated an increase in breeding season mortality
in Great Tit populations isolated on a Dutch island.
He found that by removing a little over half of
the breeding season population (adult birds and
eggs/chicks) he was able to stimulate a significant
increase in the survival of the remaining population
(adults and birds in their first year) over the following winter, presumably because competition for
winter food had been reduced. In this situation it
seems that winter food availability (or possibly
access to winter roost sites) is the factor that limits
growth of this tit population. But populations may
be limited by a range of factors. In one of the Scottish
Blue Tit populations with which I am familiar, the
population was not limited by food availability
during the winter (I personally provided more than
was required at feeding stations), but was limited
by competition for nest sites—by putting out large
numbers of nest boxes I was able to record a significant increase in the local population. You may recall
from Box 5.7 that Jan Komdeur and colleagues were
able to increase the world population of Seychelles
Warbler by increasing the number of potential
breeding territories for the birds. We will consider
competition and population regulation again later
in this chapter when we consider its impact upon
bird community structure.
Flight path: Space to breed, availability of nest
sites and/or territories can limit productivity and drive
changes in mating systems. page 116.
7.2 Communities
In my garden, on the edge of a small village in the
north of England, I might record as many as ten
species of bird in a day and as many as 15 over the
course of a year, the biggest flocks I record are of
between six and ten House Sparrows Passer domesticus. My garden is not particularly rich in birds but it
does provide the requirements of the particular
community found there. It provides water (I have a
small pond), food (I put out seeds, I tolerate some
weeds, and the plants that I cultivate support a
bewildering array of insect pests), and places to
breed (I put out nest boxes and birds nest in shrubs,
trees, and under my eaves and roof tiles). Life for
birds in my garden is not however without risk;
local cats no doubt take their share of fledglings.
Just 3 km from home is my local nature reserve
which although small supports very many more
birds. This site, which is also on the edge of a village, consists of patches of reed- and rush-fringed
open water, a small woodland, wet grassland, and
muddy flashes. I regularly record more than 30
species in a visit and more than 60 species over the
course of a year. Here I record flocks of 20 or 30 Tree
Sparrows Passer montanus and of 50 to 100 Starlings
regularly. So why are these two bird communities so different? Essentially the nature reserve
provides birds with the same resources as my
garden—food, water, and nest sites—but of course
it does it on a different scale. It provides a wider
range of seeds and fruits, insects, small mammals,
fishes, and amphibians as potential food. There are
nest-boxes, shrubs, trees, scrub, ditches, and banks
for nests; islands for safe roosting by gulls; mud
and wet grassland for feeding waders, shallow
water and submerged vegetation for dabbling
duck, and deep water for diving duck and grebes.
The nature reserve is both larger than my garden
and more complex ecologically. It provides a
greater number of potential niches and as we will
see in section 7.2, it therefore has the potential to
support a community that includes a greater number of species.
Populations of species of birds (those members of
a species living and interbreeding in a particular
area) do not generally exist in isolation. They each
live alongside populations of several other species
forming multi-species communities. In some cases
the member species of a community may initially
appear to have little to do with one another, simply
existing in the same place. In others however the
relationship between species is very clear. For
example, in Scandinavian woodlands Coal Tits
Periparus ater and Pygmy Owls Glaucidium passernium are members of the same bird community, and
one (the tit) is the food of the other. The Pygmy Owl
has the same relationship with Willow Tits Poecile
montanus in the community, and as we will see later
in this chapter the ecologies of the two tit species
interact such that the density of one has an effect
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upon the population of the other (but this is not a
predator/prey relationship).
Typically a bird community will consist of a small
number of species that are very numerous, and
smaller numbers of less common species. Each of
these will have a particular ecological role and will be
an intrinsic part of the ecological network of which the
community is a constituent part. As we have already
seen some species will be the food of others, some will
prey upon non-avian animal members of the network’s food web, others will be plant ‘predators’, but
some will also be pollinators and seed dispersers.
7.2.1 Communities are dynamic
R2
R1
R2
R3
Island Species Richness
Extinction rate
Immigration rate
Although I have a pretty good idea that the community of birds in my garden will be the same tomorrow
as it was today it would be wrong to think of communities as being fixed. Fifty years ago Collared Doves
Streptopelia decaocto would have been unknown in our
village. These doves expanded their range northwards to colonize most of Europe over the course of
the twentieth century. Ten years ago they woke me up
in the morning with their cooing call. Sadly today they
are a relative rarity probably as a result of the trichomonosis epidemic that I discussed in Box 6.2.
Communities change as a result of the immigration of new species and the extinction of old ones
and community stability is presumed to be achieved
when immigration and extinction rates are balanced (see Figure 7.5).
This apparent community stability is the basis of a
concept termed equilibrium theory, one of a group
145
of ecological theories developed as a result of studies that have been made of island systems and are
often collectively referred to as island biogeography.
Key references
MacArthur, R.H. and Wilson, E.O. (1967) The theory
of island biogeography. Princeton University Press,
Princeton.
Tzung-Su, D., Hsiao-Wei, Y., Shu, G., et al. (2006)
Macro-scale bird species richness patterns of the East
Asian mainland and islands: energy, area and
isolation. Journal of Biogeography 33, 683–93.
In their now classic 1967 book Robert MacArthur and
Edward O. Wilson described another general phenomenon of island biogeography, the fact that bigger
islands typically have more species than do those of
smaller islands. In fact their data suggest that each
ten-fold increase in island size is correlated with a
ten-fold increase in species number. Research by
Tzung-su and colleagues who have studied the avian
communities of East Asian islands provides part of
the explanation for this phenomenon. As would be
expected Tzung-Su and colleagues found that there
were more species of birds on larger East Asian
islands, but they have shown that species richness is
also positively related to a measure of habitat heterogeneity, in this case an index of vegetation productivity. We will return to this link between species
diversity and habitat diversity later in this chapter.
In the case of the results described by Tzung-su,
the islands concerned are real oceanic islands, i.e.
land surrounded by sea, but if we were to think of
islands as being one habitat surrounded by another,
Figure 7.5 The number of species (species richness) on an island of
a given size represents a balance between rates of immigration and
extinction. The equilibrium point (number of species present) will vary
in relation to both the size of the island and to its proximity to a
mainland. In the figure a distant, small island has R1 species, a
closer, small island and a larger, distant island both have R2, and a
large, close island has R3.
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ESSENTIAL ORNITHOLOGY
we can shift our thinking to consider woodland
fragments as islands in a ‘sea’ of grassland for
example, and as Figure 7.6 shows, the species–area
relationship still applies. When Robyn Wethered
and Michael Lawes surveyed the bird communities
of fragmented montane forests in South Africa
they found a very strong relationship between forest fragment area and the number of bird species
that fragments supported.
The second point that I want to draw from the
theory of island biogeography concerns island isolation. You will recall (from Figure 7.5) that islands
closer to one another, or to a mainland (or in the
case of habitat islands—those that are part of a
matrix of similar habitats or close to a significant
contiguous area of that habitat), have a greater
potential for colonization by new species. This means
that in addition to island size, island connectivity
1.69
Log15Species richness
1.64
1.59
1.54
1.49
1.44
1.39
1.34
–0.50
0.00
0.50
1.50
1.00
Log10Area (ha)
2.00
2.50
3.00
Figure 7.6 The number of species of bird present in a
natural montane forest fragment increases with the area of
the fragment. This relationship is apparent when the natural
forest is surrounded by natural grassland (closed symbols,
solid line) and when it is surrounded by a habitat matrix that
includes artificial forest plantations (open symbols, solid line).
From Wethered, R. and Lawes, M.J. (2003) Matrix effects on
bird assemblages in fragmented Afromontane forests in South
Africa. Biological Conservation 114, 327–340. With
permission from Elsevier.
Species richness
(corrected for area and habitat effects)
0.9
0.6
0.3
0.0
–0.3
–0.6
–0.9
–1.2
2
3
10
15
20 25 30
5
Density of wooded banks (m/ha)
Figure 7.7 The density of wooded banks (a measure of
habitat connectivity) is a key determinant of species richness
in both the eastern Netherlands (top line) and the central/
southern Netherlands (bottom line). van Dorp, D. and
Opdam, P.F.M. (1987) Effects of patch size, isolation and
regional abundance on forest bird communities. Landscape
Ecology 1, 59–73. Reprinted by permission from Springer.
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is also a key determinant of observed species
richness.
Whilst carrying out a study of the woodland bird
communities of the Netherlands, van Dorp and
Opdam have also confirmed woodland patch size is
the single most significant determinant of bird community size, but they have also demonstrated the
importance of habitat connectivity and the proximity of patches to one another (Figure 7.7). In 1987,
when they conducted their work, only 8 per cent of
the Netherlands were wooded and all of the woodland fragments were scattered throughout an agricultural landscape. However, in some parts of the
country the density of small woodland fragments
was greater than in others (i.e. fragments were
closer to one another) and were to some extent connected to one another by wooded ditches. Van Dorp
and Opdam found that those woodlands that were
part of a matrix of similar habitats interconnected
by wooded ditches supported a richer bird community than did very isolated woodlands.
147
Flight path: Adaptive radiations facilitate niche
divergence and specialization. page 10.
7.2.2 Niche divergence
You will recall that in chapter 1 I discussed the
mechanisms of natural selection and adaptive radiation by which individual species within communities evolve to coexist by specializing in their ecology
in some way so as to avoid or at least minimize
inter-specific competition. We saw for example that
through beak specialization the Charidriiform
waders are able to feed alongside one another in
multi-species flocks on estuarine mud-flats and
Box 7.2 illustrates niche separation in a community
of river birds. The Geospizid finches of the Galapagos
islands have evolved beak morphologies which
allow them to co-exist and exploit the full range of
feeding opportunities available to them. This is possible because faced with an array of different feeding opportunities at a single site the birds are able to
Box 7.2 Niche segregation in a riparian community
The fast-flowing mountain streams of the Himalaya are
thought to be home to more species of specialist riparian
birds than any other river system. However, until Sebastian
Buckton and Steve Ormerod made detailed observations of
the behaviour of these birds and compared their body measurements, no ecologist had attempted to explain the mechanisms by which they coexist. Working in four valleys in
central Nepal, the researchers studied five species of
insectivore: the Spotted Forktail Enicurus maculates, Little
Forktail Enicurus scouleri, White-capped Water Redstart
Chiamorrornis leucocephalus, Plumbeous Water Redstart,
Rhyacornis fuliginosus, and Brown Dipper Cinclus pallasii.
They captured and measured examples of each species, collected their faeces (to determine diet), and recorded how
each of them used riverine microhabitats whilst foraging.
They found that the birds spent between 50 per cent
(Brown Dipper) and more than 80 per cent (Forktails) of
their time foraging, but that the species foraged in different
ways and in different places from one another, presumably
therefore minimizing competition. The Brown Dipper was
the only species to forage underwater (a behaviour characteristic of dippers the world over), and was observed at
both the edges of streams and in their centres. Similarly
Plumbeous Water Redstarts foraged along stream edges
and in stream centres where they tended to fly-catch above
dry boulders and occasionally pick between them. In contrast White-capped Water Redstarts favoured stream margins where they foraged amongst dry boulders, only
occasionally fly-catching or picking food from the splash
zone. The two forktails also exhibited micro-habitat based
segregation; the Spotted Forktails preferring dry areas and
litter and the Little Forktails utilizing the splash zone where
they fed on wet boulders and submerged gravels. Faecal
analysis revealed that by using the available micro-habitats
in this way the five species were able to some degree to
avoid competition and specialize to some extent in their
diets (see Figure 7.8). Although it is clear from Figure 7.8
that there is considerable overlap in prey taken, it is also
clear that the two more aquatic species, Brown Dipper and
Plumbeous Water Redstart, show least overlap and the
three less aquatic species are also separated from one
another. Furthermore the sizes of individual prey items
selected was also found to further contribute to dietary
separation. For example although both Brown Dipper and
continued
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ESSENTIAL ORNITHOLOGY
Box 7.2 Continued
Plecoptera
Simuliidae
4
3.5
3
LF
SF
PWR
WWR
BD
Axis 2
2.5
2
1.5
1
0.5
Chironomidae 0
0
Terrestrial prey
1
2
Coleoptera
Terrestrial prey
3
Axis 1
4
5
6
Ephemeroptera
Trichoptera
Diptera
Aquatic prey
Figure 7.8 Prey selection as an indicator of niche segregation in Little Forktail (LF), Spotted Forktail (SF), Plumbeous Water Redstart
(PWR), White-capped Water Redstart (WWR), and Brown Dipper (BD). From Buckton, S.T. and Ormerod, S.J. (2008) Niche segregation of
Himalayan river birds. Journal of Field Ornithology 79(2), 176–85.
Little Forktails fed on Ephemeroptera, those individuals
eaten by dippers were considerable larger.
It is clear therefore that the members of this particular
community of birds are able to coexist because they each
specialize to some extent in aspects of their foraging behav-
specialize and each therefore occupies a different
feeding niche. The kind of adaptive radiation exemplified by the Galapagos finches is possible because
the ancestral finch colonized an island system that
contained an array of vacant niches and this is a
fundamental part of the explanation for the species
area relationship previously discussed—quite simply larger islands have more potential niches and so
can support a greater number of species.
Although we often focus on feeding behaviour
when we discuss the niche it is in fact a far broader
concept. Each species of bird has a fundamental
niche that can be described as being the ecological
space in which it can exist (where it is, what it does,
iour. In this particular example the researchers did not
observe inter-specific aggression and so it seems likely that
the species have evolved to complement one another rather
than having achieved resource partitioning as a result of
intense competition.
what it eats etc.). However when we consider the
ecology of birds as members of particular ecological
networks and avian communities we most commonly record a sub-set of the fundamental niche
termed the realized niche. This is that part of the
fundamental niche that the bird can actually use at
that time—being effectively squeezed as it is between
other competing species.
7.2.3 Niche shifts, ecological release,
and competition
The competitive exclusion principle dictates that no
two species may occupy the same niche at the same
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time and in the same place, and so where species
overlap in range they have evolved competitively or
through complementarity to each occupy a smaller
realized niche. This is perhaps most apparent when a
community shift occurs and competitive pressure is
removed, with the result that a species expands its
ecology and moves beyond the confines of the realized niche. For example where they co-occur, Yellowrumped Warblers Dendroica coronata and Blackthroated Green Warblers Dendroica virens exhibit
niche segregation and both utilize different areas of
the spruce trees in which they forage. The Yellowrumped Warblers concentrate their activity in the
bottom six feet or so of the tree whilst the Blackthroated Green Warblers feed in the top part of the
tree. In fact there can be other species of Dendroica
warbler using the same trees and under such conditions foraging area specialisms can become even
more marked. In some parts of their ranges these two
species do not co-occur and when the Black-Throated
Green Warbler is absent the Yellow-rumped Warbler
undergoes a niche expansion (sometimes referred to
as a competitive release) and forages 30 per cent
higher into the tree. Interestingly when the situation
is reversed and it is the Yellow-rumped Warbler that
is absent, the Black-throated Green Warbler does not
exhibit a shift in niche. This suggests strongly that
this is behaviourally and ecologically the dominant
species and that its presence dictates the realized
niche breadth of the Yellow-rumped Warbler.
Flight path: Birds segregate when feeding to
minimize competition. page 10 and 127.
Key reference
Morse, D.H. (1980) Foraging and coexistence of
spruce-wood warblers. Living Bird 18, 7–25.
The fact that one member of the spruce warbler
community dictates the feeding opportunities of
another is an excellent example of the role of
competition in structuring bird communities. It is
often the case however that community structure is
also strongly influenced by a range of factors that
have a cumulative effect. For example Cecilia
Kullberg and Jan Ekman have shown that the
structure of the European tit community found on
Scandinavian islands is a result of an interaction of
149
two forms of inter-specific competition (exploitation
competition and interference competition) and the
actions of a predator. The communities that they have
studied include four species: the diminutive Coal Tit
Periparus ater, the larger Crested Tit Lophophanes cristatus, the Willow Tit Poecile montanus, and the Pygmy
Owl Glaucidium passerinum which is a tit predator.
Key reference
Kullberg, C. and Ekman, J. (2000) Does predation
maintain tit community diversity? Oikos 89, 41–5.
Throughout Scandinavia these tits are found sympatrically and when they are the birds segregate
when feeding in a manner similar to the Dendroica
warblers that we have just discussed. The smaller
Coal Tits forage closer to branch tips and the larger
Crested and Willow Tits utilize the areas of the tree
closer to the trunk. But on islands where there are
only Coal Tits present they forage throughout the
tree having undergone an apparent niche expansion.
Coal Tit-only islands are occasionally colonized
by either Willow or Crested Tits but they seem to be
unable to establish stable populations. Coal Tits are
also more efficient foragers than either Willow Tits
or Crested Tits and are superior in exploitation
competition for food. The may also out-compete the
larger species because they are more productive,
having up to two large broods per season when
Crested and Willow Tits manage only a single,
smaller brood each year.
Flight path: The presence of a predator can alter
feeding behaviour. page 130.
However the situation changes when Pygmy Owls
are present on an island. In these situations the
larger Crested and Willow Tits exploit their social
dominance over Coal Tits and monopolize the safer
feeding areas close to the tree trunk through interference competition. This forces the Coal Tits to forage in risky areas on the outside of the tree and as a
result they suffer disproportionately from owl predation. Because the owls limit the Coal Tit population, exploitation competition becomes irrelevant
and a stable community of the three tit species
becomes possible. In this situation, the Pygmy Owl
is clearly acting as a keystone predator and its
actions maintain community diversity.
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ESSENTIAL ORNITHOLOGY
7.3 Extinction and conservation
When a population shrinks below a minimum viable
size it becomes effectively extinct. It no longer fulfils
an ecological role and it no longer has the capacity to
recover and grow. Without human assistance (and
in many cases even with it) such populations shrink
until there are no birds left and they become extinct
in the traditional sense of the word. If another population of the same species exists in another place
there is the chance that natural re-colonization will
occur as has happened in Scotland in the case of the
Osprey. This species became extinct in Scotland in
1916 (having already been lost in England in 1840),
but in 1954 a pair returned to breed. Since that time,
thanks to the conservation efforts of many individuals
and organizations, the British population has grown
to around 150 pairs.
If natural re-colonization is unlikely, then conservation efforts might result in the successful reintroduction of the species, moving members of a surviving population into the area to be colonized. This
strategy was used to re-introduce the Osprey to southern England when it became apparent that a rapid
natural spread southwards from Scotland was unlikely.
However, as we all know, there comes a point
when a species goes the way of the Dodo Raphus cucullatus, the Passenger Pigeon Ectopistes migratorius,
and the Great Auk Penguinius impennis, when the
last population shrinks to the point that the last individuals die, then the species becomes extinct and is
extinct for ever. In 2006 the IUCN (International
Union for the Conservation of Nature) stated that
135 bird species had become extinct since the year
1500. A sobering thought, particularly when one
takes into account the rate of increase in extinction
rate over the same time period (Figure 7.9).
Clearly, small populations are particularly vulnerable to extinction, but small numbers alone however do not explain what makes a species vulnerable
to extinction. After all, the Passenger Pigeon went
from being one of the most numerous birds known
to being extinct in a very short period—birds that
are hunted by man, but which man makes no effort
to harvest in a sustainable way are at particular risk.
A number of factors make one species more likely to
become extinct than another, and when a number of
these coincide the odds are not good.
Number of extinctions
150
100
75
50
25
0
1500
1600
1700
1800
Year
Extinctions observed
Extinct
Critically Endangered
(Possibly Extinct)
1900
2006
Extinctions prevented
Extinct in the Wild
Critically Endangered
(Possibly Extinct in the Wild)
Extant
Figure 7.9 Estimated numbers of bird extinctions and of numbers
of critically endangered bird species in the past five centuries. The
inset bird, the Atitlàn Grebe, Podiymbus gigas was found on lake
Atitlàn, Guatemala. It became extinct in 1986. From Rodrigues,
A.S. (2006) Are global conservation efforts successful? Science 313,
1051–52. Reprinted with permission from AAAS.
For example species with a very narrow geographical or ecological range are at particular risk,
birds found on just one oceanic island, or extreme
specialists for example. Loss of habitat in such a
situation could be catastrophic. Conservation efforts
can however make a difference in such situations.
Recall that Jan Komdeur and his colleagues greatly
increased the world population of the Seychelles
Warbler by trans-locating a group of birds to a second island (see chapter 5).
Key reference
Diamond, J.M., Bishop, K.D., and van Balen, S. (1987)
Bird survival in an isolated Javan woodland: Island or
mirror? Conservation Biology 7, 39–52.
However, even though the threat to the warblers is
lessened, these small populations remain particularly vulnerable. There is often little scope for movement of individuals between such populations and
each is in itself vulnerable by virtue of its small size.
For example Jared Diamond and co-workers have
reported that of the birds in the Bogor Bogor
Arboretum and Botanical Garden, Java, a green
space which had been isolated from similar habitats
for 50 years at the time of Diamond’s work, 75 per
cent of those species with a small initial population
became extinct, whereas all of the species with an
initially large population survived.
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Small populations, or populations that have
rapidly grown from a small founder population,
face another problem—reduced genetic diversity—
which may make them more susceptible to emergent diseases because they are unable to evolve
resistance. This could for example explain the
susceptibility of the House Finch to Mycoplasma
gallisepticum.
Species with low population densities, or large
range requirements (such as the larger birds of
prey) are particularly vulnerable, their habitats are
susceptible to fragmentation and encounters with
potential mates can become infrequent. We have
already seen that a species with a naturally low rate
of productivity is less able to expand its population;
similarly species with low dispersal potential are at
risk. They simply lack the ability to spread. Island
rail species are an excellent example of this phenomenon. Many have lost the ability to fly (in some
cases they are psychologically flightless even
though they retain the mechanical ability). Most, if
not all, are threatened with extinction.
Migrants rely upon multiple locations and stopping off points between them and so are particularly susceptible to habitat loss. They are often
funnelled through geographical bottlenecks where
predators can concentrate their effect and in some
cases, such as the North American warblers, have
very restricted wintering grounds. A single hurricane could make a species extinct just because it
destroys the forests of a single Caribbean island.
This scenario is not at all far fetched—Bachman’s
151
Warbler Vermivora bachmanii is thought to have
become extinct in the 1960s as a result of the deforestation of Cuban forests to make way for sugar
cane plantations.
7.3.1 Conservation can be a success
Earlier in this section I cited the sobering statistics
provided by Ana Rodrigues which bring home the
scale of the threat of extinction faced by birds.
However we should not lose hope. Throughout
this chapter and elsewhere in this book I have
described examples of monitoring programmes,
nest-box schemes, habitat management, breeding
programmes, re-introductions and translocations,
and other practical conservation efforts. The human
love of, and admiration for, birds is such that armies
of citizen scientists can be mobilized across the
globe to raise funds and carry out practical work in
an effort to conserve birds and thereby conserve the
ecosystems that both we and birds are part of. But is
it working? I think that it is. Ana Rodrigues provides evidence that the tide is turning (Figure 7.10)
and at the scale of my own experience I can see
birds in the UK today that were locally extinct in my
memory and that conservation efforts have restored
to us. As a bird ringer and birder I can see the passion and dedication of private individuals for their
own conservation actions and as an academic I am
aware of the advances in our understanding that
leaders in the field of ornithology are making. But
good science alone will not be enough, as Box 7.3
Number of bird species
9950
9900
9850
9800
9750
1500
1600
1700
Year
1800
1900
2006
Expected number of species in absence of human activities
Observed number of species
Predicted number of species in absence of conservation action
Impact of human activities
Impact of conservation action
Figure 7.10 The estimated impact of global
conservation actions to prevent bird extinctions. In the last
100 or so years conservation efforts have resulted in more
than 30 species being brought back from the brink of
extinction. From Rodrigues, A.S. (2006) Are global
conservation efforts successful? Science 313, 1051–2.
Reprinted with permission from AAAS.
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ESSENTIAL ORNITHOLOGY
Box 7.3 How much does conservation cost?
Governments, non-governmental organizations and charities, and concerned private individuals invest huge amounts
of money in conservation projects annually. But how much
does it actually cost to save a species from extinction? Well
there is no single answer to that question; obviously the
costs incurred will vary from case to case and location to
location. But Antonio Barbosa and José Tella have attempted
to answer the question in the case of one bird species, Lear’s
Macaw Anodorhynchus leari. When it was discovered in
north-eastern Brazil Lear’s Macaw was already rare, it had
been hunted for food, persecuted as a crop pest, captured
for the pet trade, and suffered as a result of habitat loss. In
(A)
(B)
(C)
Figure 7.11 Birders visit north-eastern Brazil specifically to see the rare Lear’s Macaw Anodorhynchus leari (A; © José L. Tella). While they
are there, birders contribute to the local economy and conservation efforts by buying souvenirs like these models (B; © José L. Tella) and
baskets (C; © Simone Tenório) made from the wood and leaves of the licuri palm.
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P O P U L AT I O N S, C O M M U N I T I E S, A N D C O N S E R VAT I O N
1978, when it was first recognized as a distinct species, the
global population was estimated to be only 60 birds but as
a result of a mixture of in situ and ex situ conservation measures the most recent population estimate is of 1263 birds in
two subpopulations. Barbosa and Tella carried out extensive
research to determine the amounts of money that were
invested in the in situ conservation of the species (i.e. direct
action to conserve the populations in the wild) by the
Brazilian government and by a number of key NGOs and
commercial sponsors. The activities that they considered
included the expenses associated with habitat protection
and species surveillance, education and outreach activities
to raise awareness with local people, the administrative
costs of coordinating multiple conservation efforts, and the
costs of censusing the populations. Their synthesis of these
data revealed to them that over the 25-year period between
1992 and 2017 around US$ 3,660,000 was invested. Most
(51 per cent) of this money supported research work to better understand the species’ conservation needs, 22 per cent
was spent on direct protection of the endangered populations, and 16 per cent was spent on social projects. The
remaining smaller amounts were spent on census work and
administration.
It is also important however that the continued survival
(and perhaps to some degree rarity) of the macaw in the
region does result in a flow of monies into the local economy.
shows there is a real cost to conservation and to
be effective it is essential that scientists work with
local communities and both governmental and
non-governmental agencies.
7.3.2 The task that faces us as ornithologists
There are ornithological conservation success stories, and I have highlighted some of them in this
book, but there is still a lot of work to do. Kenneth
Rosenberg and his colleagues have been able to
bring together data from a range of standardized
long-term surveys and from a network of 143
weather radars, capable of detecting nocturnally
migrating birds, to examine changes in the abundance of 73 per cent (529 species) of the breeding
birds of the USA and Canada between 1970 and
2018. The positive news is that numbers of 100 species of breeding bird have increased, there are more
raptors, game birds, ducks, and other waterfowl
that there have been in the past. Presumably
153
Ornithological tourism supports four small companies who
guide around 50 tourists per year to view the birds
(Figure 7.11A); generating approximately US$ 1000 to the
local economy each year. Making and selling macaw-related
handicrafts as souvenirs for the tourists (Figures 7.11B, C)
supplements local salaries (each artisan is thought to derive
around 18 per cent of their monthly income from this work).
These commercial benefits of eco-tourism could be further
enhanced if a plan was developed to increase the number of
visitors each year and to both lengthen their stay and
encourage them to view the other endemic species of the
area. The birds also provide an important ecosystem service
because they, like other macaws, are efficient seed dispersers.
In the case of Lear’s Macaw they are efficient dispersers of
the seeds of the licuri palm. This palm is their main food stuff,
the main habitat of the other endemic species of the region,
the main material used by artisans to create macaw-related
souvenirs, and has up to 537 uses for local people. By
supporting the regeneration of the palm, the macaw has an
important conservation, economic, and social impact.
Reference
Barbosa, A.E.A. and Tella, J.L. (2019) How much does it cost
to save a species from extinction? Costs and rewards of
conserving the Lear’s Macaw. Royal Society Open Science
6, 190.
species- and habitat-focused conservation efforts
and the banning of DDT have had a positive impact
here. The fact that some species of non-native introduced bird have experienced population shrinkage
might be seen as a positive too, because it could
reduce competition with native species. Overall
however the picture is a very gloomy one and their
estimates suggest that there has been a staggering
cumulative loss of three billion birds during this
period. Significant declines in the numbers of 303
(57 per cent) species were recorded, and some families have suffered disproportionately; 90 per cent of
all of the birds lost come from just 12 families and
more than half of the loss involves the sparrows,
warblers, and blackbirds. All habitats have been
affected but grassland birds have fared particularly
poorly and 74 per cent of grassland species have
declined in numbers. Richard Inger and his colleagues have reported a similar situation in Europe.
Their data from 144 species over a 30-year period
(1980–2009) suggest a loss of more than 400 million
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ESSENTIAL ORNITHOLOGY
individual birds and, as is the case in North America,
the farmland/grassland birds have suffered particularly steep declines. Here too though there are
some species that have become more numerous and
the researchers have determined that these tend to
be those species that already have small population
sizes, i.e. the birds most likely to have been the subject of direct conservation efforts.
Key references
Carson, R. (1962) Silent Spring. Houghton Mifflin,
Boston.
Rosenberg, K.V., Dokter, A.M., Blancher, P.J., et al.
(2019) Decline of North American Avifauna. Science
336(6461), 120–4.
Inger, R., Gregory, R., Duffy, J.P., et al. (2015)
Common European birds are declining rapidly while
less abundant species’ numbers are rising. Ecology
Letters 18, 28–36.
State of Nature Partnership (2019) State of Nature
2019 https://nbn.org.uk/stateofnature2019/
A similar situation exists in the UK where the State
of Nature Partnership have recently published a
sobering report suggesting that although the numbers of birds of 171 species for which data exists
have increased over the longer term (the last 50 to 30
years), these increases are driven by colonization
and range expansion of species from mainland
Europe and by increases in numbers of birds that
had become extremely rare but have benefited from
conservation efforts. These increases mask a significant decline in once common and widespread species and it is estimated that some 44 million birds
have been lost from the UK. Once again it is farmland birds that have suffered a particularly dramatic
decline (54 per cent) and so perhaps it is time for us
to review once more our agricultural and wider land
use practices. It is now almost 50 years since Rachel
Carson brought to the attention of the world the
threat of a ‘silent spring’. We may not have solved
the problem yet—but by working together we are
inching closer to doing so. That is why it is important that those of us who have a love for birds, and
for the wider environment, should continue to learn
all that we can and to take all possible positive action
to ensure a bird-filled world for future generations.
Summary
The life history strategies of individual species
influence their population size, as do numerous
environmental pressures both natural and anthropogenic. Communities of birds are able to coexist
because the species within them exhibit niche separation and competition avoidance. Many of the
world’s birds are threatened as a result primarily of
human activity, but by working together species
can be saved from the brink of extinction.
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Index
adaptive radiation 10, 146, 148
accessory optic system 43
air sacs 38–9
alarm calls 133–5
Albatross (Diomedeidae)
Gray-headed 49–50
Tasmanian Shy 48–9
Wandering 49
albatrosses
and longlining 49–50
conservation 49–50
foraging 121–2
flight 33–4
migration 48–50
reproduction 77
albumen 74–7
alien species 16, 142–3
altricial development 86, 91–93, 113
ansiodactyl feet 7–8
anisogamy 96–7
Anseriformes 7
anting 28
Apodidae see Swifts
Archaeopteryx 1–7, 45–6
Auk (Alcidae), Great 150
Babbler (Timaliidae), Pied 135
BDNF 106
beaks see bills
begging 113–14
bills
Darwin’s finches 12–14
diversity 10
morphology 10
Blackbird (Turdidae) 52
Red-winged 102–4
Blackcap (Sylviidae) 13, 31, 53–7, 69
BMP4 13
bone morphometric protein 13
Booby (Sulidae), Masked 77
bout length, song 109
broken wing display 133
brood parasites 82–84
brood patch 88
brood reduction 114–5
Bustard (Otididae)
Houbara 98
Little 99
Buzzard (Accipitridae) 36
calls
alarm 133–6
mobbing 136–7
calmodulin 13
CaM 13
camouflage 10, 131–2
eggs 81
cannibalism 22
carrying capacity 116–117
central place foraging theory 127
Chaffinch (Fringillidae) 106
chalaza 76
character conservation 7
Charidriiformes 10, 147
Chickadee (Paridae), Black-capped
66, 134, 136
chicks 78, 83–4, 87, 91–92 133, 138
begging 113–15
tonic immobility 133
Chiffchaff (Sylviidae) 31, 111
chorioallantois 76
classification 5
cloaca 74–75
clock shift 68
clutch size 77–80, 99, 103
Cockatiel (Psittacidae) 41–2
collision avoidance 42–3
colonial breeding 22, 70–72, 82, 86,
110, 136–8
see also flocks
colour
of eggshells 81–2, 84
of feathers 26–7, 132
communities 144–9
dynamics of 143
ecological network 140, 145
extinction 145, 150–2
immigration 145
patch size 146–7
species richness 145–6
community stability 145–6
competition 10–11, 115, 147–9, 153
competitive exclusion principle 148
Condor (Cathartidae),
Californian 140–1
Confuciusornis 6
confusion effect 139
Conservation 16–17, 43–4, 49–51, 113,
116–7, 138, 150–4
contact zone 14–5
contour feathers 22–26, 88, 113
convergence 7–8
cooperative breeding 116–7
cooperative feeding 124–5
copraphagy 87
copulation 75, 95–6, 100, 113
retaliatory 95–6, 100
coracoids 34, 37
in archaeopteryx 4
corticosterone 58–9
courtship 21, 26, 37, 42, 99–110
Cowbird (Icteridae)
Brown-headed 83
Shiny 84
crèches 138
cross-fostering 53
Crow (Corvidae)
Carrion 14
Hooded 14
Northwestern 125–6
crows
hybrid zone 14
optimal foraging 125–6
Cuckoo (Cuclidae)
Common 82
Diederik 82
Curlew (Scolopiacidae)
Eurasian 10
Darwin’s finches 10–14, 147
dawn chorus 110
delayed maturation 140
diapsid reptiles 1–2
Diclofenac 90
differential allocation 115
155
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INDEX
dinosaurs 4, 6
theropods 17
thecodonts 2
Dipper (Cinclidae), Brown 147–8
directional selection 11–13
disease 130, 141–3
dishonest signal 82, 136
displays
broken-wing 133
courtship 98, 101
disruptive selection 11–12
DNA 8–9, 11
Dodo (Raphidae) 150
Dove (Columbidae)
Barbary 41
Collared 145
down, feathers 21–6, 113
Drongo (Dicruridae)
Fork-tailed 134–6
Duck (Anatidae)
American Black 16
Black-headed 82
Eider 138
European Mallard 16
Ruddy 16–17
White-headed 16–17
ducks, hybridisation 16–17
Dunnock (Prunellidae) 101
dunnocks, mating system 104–5
ecological isolation 11
ecological network 145
ecological release 148
ecological role 150
egg dumping 82
egg recognition 82–4
egg white see albumen
egg yolk see yolks
eggs 75–77
and agricultural chemicals 89–90
camouflage 81
clutch size 77–80
formation 73–7
hatching 91
incubation 85–88
internal structure 75–7
mimicry 82
recognition 82
quality 84–5
eggshells
colouration and pattern 81–5
effects of pesticides 89–90
quality 84–5
Eider (Anatidae)
Common 138
Steller’s 29
embryo 76–77, 91
equilibrium theory 145
evolution
adaptive radiation 10–13
from dinosaurs 5–10
natural selection 11–13
of flight and flightlessness 45–47
of migration 51–6
evolutionary tree see phylogenies
extinction 6, 16, 145, 150–4
extra-pair copulation (EPC) 95–6,
100, 105
faecal pellets 87
Falcon (Falconidae)
Eleonora’s 51
Peregrine 89, 138–9
fat reserves
for migration 57–62
fault bars 28–9
feather tracts 24–5
feather
of Archaeopteryx 1
colour 26
contour 22–26, 88, 113
damage 26–7
down 21–6, 113
filoplume 22
follicle 25
growth 26, 28
maintenance 27–8
pennaceous 6, 22, 45
plumulaceous 6, 22
primary 23, 26, 29
secondary 23, 29
semiplume 22
structure 24
wear see feather damage
see also moult
feeding
differential allocation 115
niche 10, 147–8
territory 126–7
see also foraging
feet
toe arrangement 5, 7–8
claw curvature 5
female preference 98–9
Finch (Estrildidae)
Bengalese 118
Zebra 35–6, 77, 94–6, 106–7,
110, 118
Finch (Fringilliade)
Chaffinch 130
Goldfinch 88, 129–30
Greenfinch 25, 130
House 87, 130, 142–3, 151
Finch (Thraupidae)
Galapagos see Darwin’s finches
Cactus 14
Large Cactus 14
Large Ground 14
Medium Ground 12–4
flight
adaptations for 34
aerodynamics 29, 34, 36, 41
respiration 38–40
wing morphology 23, 30, 33–35
energetics 38–40
evolution of 45–47
flapping 33–8, 41, 45–6
gliding and soaring 33–36,
40–1, 45
speeds 33, 35–7, 41–2
flightlessness
evolution of 45–7
flocks 29, 40, 57, 123–4, 126, 130, 134,
136, 139, 143–4, 147
Flycatcher (Tyrannidae)
Collared 109, 118
Pied 58, 84, 109
food storage 66
foraging 49–51, 63, 66, 120–131
and risk 130–1
and spatial memory 66
cooperation 123–4, 125
flocks 123–5, 127
optimal 125–6
see also feeding
Forktail (Turdidae)
Little 147–8
Spotted 147–8
formation flying 40–1
funnel cage 52,68–9
furcula 1, 2, 4, 34, 37
Archaeopteryx 4
Galapagos Islands 10, 12
genetic swamping 14, 16
gliding see flight
Godwit (Scolopacidae)
Bar-tailed 62
Goose (Anatidae)
Brent 124
Pink Footed 40
Grassquit (Thraupodae)
Dull-coloured 11
Grebe (Podicipedidae)
Atitlan 150
ground nesting 81, 85, 132–3
Grouse (Phasianidae)
Greater Sage 99
Guillemot (Alcidae) 85
egg recognition 82
Gull (Laridae)
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INDEX
Black-headed 123
Glaucous 31
Herring 53, 114
Ivory 31
Laughing 114
Lesser Black-backed 53
gulls
begging 114
cannibalism 22
migration 53
moult strategies 31
hallux 4, 5
harems 101–2
Hatching, eggs 91–2
Hawk (Accipitridae)
Harris 123–5
helpers 116–17
herbivores 125
Hesperornithiformes 6
high vocal centre (HVC) 106–7
hippocampus 65–6
hormones 58–9, 88, 106
hot-shots 98
hot-spots 98
Hummingbird (Trochillidae)
Anna’s 42
Ruby-throated 37, 59
hummingbirds
fat reserves 59
feathers 26
flight 36–7, 42
physiology 40–1, 59
song 105
hybrid zone 14–5
hybridization 14–6
hyperphagia 57, 62, 70
Icthyornithiformes 6
immunocompetence 84, 109, 112, 143
imprinting 118
incubation 86–8, 91
information transfer hypothesis
122–3
infundibulum 74–5
invasive species see alien species
Jackdaw (Corvidae) 28
Jay (Corvidae), Blue 8, 23
Junco (Emberizidae), Dark-eyed 54,
109, 131
K/T boundary 6
keratin 28
kin selection 98–9
Kittiwake (Laridae) 92
Kiwi (Apterygidae), Brown 75
foraging 121
kleptoparasitism 135
last male precedence 95
learning to sing 106–7
leks 98–9
life history strategy 51
light pollution 64–5
lungs 38–9
Macaw, Lears 152–3
magnetic field 69–70
magneto-receptor 70
Magpie (Corvidae), Black-billed 41,
78, 114–5
Mallard (Anatidae), European 16
Manakin (Pipridae), Bluecrowned 98
Manx Shearwater (Procellariidae),
flight 35
mate choice see courtship
mate sharing 101
mating systems 97
megapodes
incubation 86
superprecocial chicks 91
melanins 26–7, 33–4
melatonin 58
meloxicam 90
Merlin (Falconidae) 90
Microraptor gui 6, 45–6
migration 48–65
and fat reserves 58–61
and stable isotopes 55–6
and weather 63
control of 51–4, 58–60
disruption 60–1, 64
ecology of 51–2
evolution of 51–7
genetics 52–7
navigation 68–72
stopover sites 62
migratory orientation 68
migratory restlessness 52–3, 58, 68–9
mimicry, egg 82
mobbing 136–7
monogamy 97, 103–5
moult 28–32
fault-bars 28–9
in gulls 31
minimizing impact of 29–30
strategies 30–2
movement, categories of 48
Murre, thick-billed 127
nXIIts 105
natural selection 10–13, 30, 54, 83
157
see also evolution
directional selection 11–13
disruptive selection 11–12
stabilizing selection 11–12
navigation 65–72
visual landmarks 65
celestial cues 68–9
magnetic-field 69–70
sun compass 68–9
scent-based 70–2
vector-based 67–8
Neornithes 4
neonicotinoids 60–61
nests 85–7
niche 10, 147–9
divergence 147–8
shifts 148–9
bill diversity 10
Nightingale (Turdidae) 110–11
noise pollution 111–3
nuptial gift 100–1
Nuthatch (Sittidae), Red-breasted 134
optimal clutch size 78–9
optimal foraging 125–6
organochlorines 89–90
Ornithomimus 1
Osprey (Pandionidae) 8, 123, 150
Ostrich (Struthionidae) 25
ovaries 74–5
oviduct 74–5
ovum 74–5, 94
Owl (Strigidae)
Great Horned 134
Northern Pygmy 134
Pygmy 130, 144, 149
Tawny 99
Oystercatcher (Haematopodidae),
Eurasian 10, 81, 88, 125
parasites 87, 130
Parrot (Psiticidae), Swift 50
partial migrant 53
passerines 7, 79–80
feather tracts 25
pathogens 87, 130
Peafowl (Phasianidae), Indian
21, 99
pectoralis 34, 37, 41
Pelican (Pelecanidae), Great
White 40–1
pelicans, formation flying 40–1
penguins (Speniscidae) 25, 47
incubation 87
perceptual sharpening 114
pesticides 60–61, 89–90
photoperiod 58
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INDEX
phylogeny 7–10, 17–20
biomolecular 8–10
consensus 9
morphological 8–9
Pigeon (Columbidae), Passenger
7, 150
pigeons, navigation 65, 69–70
piloting 65
pipping, see hatching
place cells see hippocampal cells
placode see feather follicle
plastic pollution 121–2
Plover (Charadriidae)
Little Ringed 10,
Ringed 131
plovers, broken wing display 132–3
plumage
camouflage 30, 131–2
cryptic 29
eclipse 30
nuptial 30
polyandry 97, 104–5
polygamy 102–4
polygynandry 97, 104–5
polygyny 97, 102–5, 117
polygyny threshold model
(PTM) 103–4, 117
population change 142–4
populations 11–13, 16, 142–144
see also communities
porphyrins 26,
precocial 77, 82, 91–92, 103, 113
predation 77–80, 82–3, 92–3, 130–8
predator avoidance 131–8
preen gland 7, 28
prolactin, and incubation 88
Ptarmigan (Phasianidae) 30
pterylae, see feather tracts
pyrazine 121–2
Quelea (Ploceidae), Red-billed 140
rachis 22
Razorbill (Alcidae) 85
Redpoll (Fringillidae) 22
Redshank (Scolopacidae) 10, 137–9
Redstart (Muscicapidae)
Black 115
Common 27, 115
Plumbeous Water 147–8
White-capped Water 147–8
Redstart (Parulidae)
American 98
refuelling, during migration 52,
57–62
resource availability 79
resource defence 105, 126
resource provision 99–101
retricies, see feathers, tail
Robin (Turdidae)
American 120
European 29, 70, 134–5
Sanderling (Scolopacidae) 10, 126–7
Sandpiper (Scolopacidae)
Semipalmated 65
Spotted 77, 103
sensitive period 106–7
sensorimotor phase 106–7
sensory bias 101
sensory acquisition phase 106–7
sentinels 134–5
sex chromosomes 73–5
sex-linked genes 75, 82
sexual conflict 104–5
sexual selection 97, 101
sexy sons hypothesis 98
shell dropping behaviour 125–6
shells, see eggshells
Shrike (Laniidae)
Great Grey 100
Lesser Grey 101
Red-backed 69
silent phase 106–7
Silvereye (Zosteropidae) 69–70
singing rate 109–10
Sinosauropteryx 1
Snipe (Charadriidae), Great 98
social monogamy 97
song 74, 105–113
and noise pollution 112–3
bout length 109
courtship 106–7
functions of 107–13
learning 106–7
sonograms 135
Sparrow (Passerellidae)
Savannah 107
White-crowned 60–1
Sparrow (Passeridae)
House 5, 87, 106, 112–3, 142–3
Sparrowhawk (Accipitridae) 47, 132,
138–9
spatial memory 65–66
speciation 10–13
species
biological concept 11
richness 145
sperm 7, 73, 75, 94–6, 103
storage tubules 95
sperm competition 95–6
stabilising selection 11–2
stable isotopes 55–6
Starling (Sturnidae)
European 29, 37–8, 67–8, 108, 141
Spotless 115
sternum 1, 4, 34, 37, 42
stitching 121
Strigidae 8
sun compass 69
Sunbird (Nectariniidae)
Double-collared 127
Golden-winged 127
Malachite 127
Palastine 86
superprecocial development 91
supracoracoideus 34, 37
Swift (Apopidae) 8, 33, 57
synapsid reptiles 2
Sinosauropteryx prima 6
syrinx 105–6
tail feathers 22, 26, 28–9
tectofugal pathway 43
Tern (Laridae), Arctic 92
Territory
and song 108–9, 111
breeding 78–9, 99–104, 116–7
feeding 126–7
testes 75
testosterone
and bird song 107
and incubation 88
and migration 58
thalamofugal pathway 43
thecodonts 2
theropod dinosaurs 17, 45
Tit (Paridae)
Blue 66, 77, 84–5, 98, 129, 144
Coal 130, 144, 149
Crested 130, 149
Great 30, 84, 91, 144
Marsh 66, 129
Willow 144, 149
toe arrangement 4, 7–8
tonic immobility 133
trachoesyringeal motor nucleus 105
trkB 106
turacous (Musophagidae), feather
colour 26
uropygial gland, see preen gland
uterus 74–5, 95
vagina 74–5, 95
vector navigation 68
vigilance behaviour 134–5, 137
Vireo (Vireonidae), yellow-green 57–8
Vulture (Cathartidae)
Griffon 44
White-backed 90
OUP CORRECTED PROOF – FINAL, 18/08/20, SPi
INDEX
Vultures
collisions 44
pollution 90
vision 44
W sex chromosome 73, 82
wading birds, foraging
10, 121
Warbler (Parulidae)
Bachman’s 151
Black-throated Green 149
Blue-winged 14–15
Brewsters 15
Golden-winged 14–15
Lawrences 15
Prothonatory 83
Red-faced 79
Yellow 86
Yellow-rumped 149
Warbler (Sylviidae)
Aquatic 75
Chiffchaff 31
Garden 31
Greenish 31
Reed 106
Sedge 51
Seychelles 116–17, 150
Willow 31, 55–6, 106
Whitethroat 26–7, 106
weather, and migration 63
Weaver (Ploceidae), Village 82
weavers
egg recognition 84
nest 86
Widowbird (Ploceidae)
Long-tailed 101–2
Red-shouldered 101–2
wing 33–36
wishbone, see furcula
yolk 75–7
yolk sac 76
Z sex chromosome 73
zoonotic disease 142
zugunrhue, see migratory
restlessness
zygodactyl feet 7
159