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Why Birds Matter: From Economic Ornithology to Ecosystem Services
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J Ornithol
DOI 10.1007/s10336-015-1229-y
REVIEW
Why birds matter: from economic ornithology to ecosystem
services
Christopher J. Whelan1 • Çağan H. Şekercioğlu2,3 • Daniel G. Wenny4
Received: 1 January 2015 / Revised: 16 April 2015 / Accepted: 21 April 2015
Dt. Ornithologen-Gesellschaft e.V. 2015
Abstract Birds are conspicuous in many habitats, occur
worldwide, are ecologically diverse, and are better known
than other vertebrate groups. Birds devour pests, pollinate
flowers, disperse seeds, scavenge carrion, cycle nutrients,
and modify the environment in ways that benefit other
species. Investigation of these ecosystem functions directly
as ecosystem services has grown immensely over the last
two decades and the ecological relevance of birds is well
established. Birds are also observed, fed, and used as
artistic and spiritual inspiration by millions of people
around the globe. Yet the economic relevance of birds is
not widely appreciated and the economic relevance to
human society of birds’ ecological roles is even less understood. Quantifying the services provided by birds is
crucial to understand their importance for ecosystems and
for the people that benefit from them. In this paper, we
briefly review the rise and fall of economic ornithology and
call for a new economic ornithology with heightened
Communicated by E. Matthysen.
& Daniel G. Wenny
dandroica@gmail.com
Christopher J. Whelan
whelanc@uic.edu
Çağan H. Şekercioğlu
c.s@utah.edu
1
Illinois Natural History Survey, c/o University of Illinois at
Chicago, Chicago, IL, USA
2
University of Utah, Salt Lake City, UT, USA
3
College of Sciences, Koç University, Rumelifeneri, Sariyer,
Istanbul 34450, Turkey
4
University of California-Berkeley, Museum of Vertebrate
Zoology, Berkeley, CA, USA
standards and a holistic focus within the ecosystem services approach. Birds’ ecological roles, and therefore,
ecosystem services, are critical to the health of many
ecosystems and to human well-being. By understanding
and valuing bird services and disservices through careful
natural history research, we can better assess the environmental consequences of bird declines and extinctions and
communicate these findings to the public and policy
makers, thereby increasing public support for the conservation of birds and their habitats.
Keywords Ecosystem services Pest control Pollination Ecological economics Economic
ornithology Disservices Natural history Seed dispersal Scavenging Predation
Introduction
‘Nature conservation’ is often thought as something that
happens ‘‘out there’’ in reserves rather than something integral to daily life. This view reinforces the misconception
that people are apart from the natural world, leading to
many of the environmental issues we face today. However,
protecting biodiversity and ecosystems is essential for human society, and therefore should be incorporated more
directly into public policy, development plans, and daily
life (Hackett 2011; Kareiva et al. 2011; Lovins et al. 1999;
Whelan et al. 2010), which means we must understand the
value of biodiversity for human society. In this paper, we
outline a framework for investigating and assessing the
value of birds for human society.
One of the earliest examples of such an effort was in the
USA, when the United States Department of Agriculture
(USDA) started to assess the economic impact of birds and
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mammals on agriculture in the late 1800s (see below).
These efforts dwindled by the 1930s, as most species were
found to be beneficial or not harmful. Since then, most
economic aspects of wild animal ecology have been ignored, a problem exacerbated by the decline in funding for,
and instruction in, natural history and organismal ecology
(Tewksbury et al. 2014). More recently, growing awareness of the importance of ecosystem function to human
society (ecosystem services, ES) has led to a renewed effort
to assess the ecological and economic value of biodiversity
and ecosystems (Hocking and Babbitt 2014; Losey and
Vaughan 2006; Muscarella and Fleming 2007; Sekercioglu
2010; Wenny et al. 2011; Whelan et al. 2008). Here, we
describe the roots of ES in economic ornithology of the late
nineteenth and early twentieth centuries, outline the recent
work on understanding ES provided by birds, and provide a
framework for the redevelopment of economic ornithology
research within the field of ecosystem services.
Ecosystem services are defined as ‘‘the set of ecosystem
functions that are useful to humans’’ (Kremen 2005). The
history of ecosystem services has been explored in depth
elsewhere (e.g., Daily 1997; Gomez-Baggethun et al.
2010). The number of scientific papers on ecosystem services has increased dramatically in the past two decades.
The Millennium Ecosystem Assessment (MEA 2005)
brought ecosystem services to the attention of governments
(Gomez-Baggethun et al. 2010). The MEA (2005) aimed to
evaluate the potential consequences of ecosystem change
from a human well-being perspective and with an emphasis
on ecosystem services, and identified four classes of
ecosystem services: provisioning services, cultural services, regulating services, and supporting services.
Birds contribute all four types of ecosystem services
(Sekercioglu 2006a; Whelan et al. 2008). Provisioning
services are provided by both domesticated (poultry) and
non-domesticated species. Birds have long been important
components of human diets for subsistence, consumption,
and sport (Moss and Bowers 2007), particularly waterfowl
(Anatidae) and terrestrial fowl (Galliformes; Peres 2001;
Peres and Palacios 2007). Bird feathers provide bedding,
insulation, and ornamentation (Green and Elmberg 2014).
Through their unique salience for humans, birds offer a
significant focus for studies of cultural services within the
ES paradigm, and this is the field of ethno-ornithology
(Cocker and Tipling 2013; Podulka et al. 2004; Tidemann
and Gosler 2010). Bird-watching is one of the most popular
outdoor recreational activities in the United States and
around the world (Kronenberg 2014a; Ma et al. 2013;
Sekercioglu 2002; White et al. 2014), and has direct economic benefits as well as indirect benefits through numerous citizen science programs involving bird-watchers
(Greenwood 2007). Numerous bird species contribute
regulating and supporting services via their foraging
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ecology. These services include scavenging carcasses, nutrient cycling, seed dispersal, pollination, and pest control
(Sekercioglu 2006a; Whelan et al. 2008). Here, we focus
on regulating and supporting services because the benefits
of these services are often transmitted indirectly to humans,
and are thus poorly understood in terms of their contribution to human well-being.
Many of the ecosystem services provided by birds arise
through their ecological functions. Estimating their value
thus necessitates sound knowledge of the natural history of
the species involved (Sekercioglu 2006a, b; Wenny et al.
2011; Whelan et al. 2008). Most regulating and supporting
services arise via top-down effects of resource consumption. With over 10,000 bird species on earth, birds consume
a wide variety of resources in terrestrial, aquatic, and aerial
environments. Sometimes the consumed resource is a pest
of agricultural crops or forests. In other cases, bird resource
consumption facilitates pollination or seed dispersal, promoting successful plant reproduction in thousands of plant
species. For economically or culturally significant plants,
these services benefit humans, who also benefit indirectly
from the myriad ES provided by forests and other plants.
Through these services, birds have a large, global, but
rarely quantified impact on ecosystems. We urgently need
to develop methods to quantify avian functions, services
and their values, based on a thorough understanding of
their natural history particularly habitat requirements, reproductive ecology, resource exploitation, and interactions
with competitors, predators, and parasites.
The rise and fall of economic ornithology
Early efforts to understand bird impacts focused predominantly on direct interactions as crop pests or game
species. Although not recognized formally as ecosystem
services, the notion that humans may gain benefits from
nature was accepted by students of natural history. In the
US, early studies on food habits of native fauna and systematic expeditions cataloging wildlife and flora in North
America and around the world grew into a burgeoning
discipline known as ‘‘economic ornithology.’’ Embraced
enthusiastically by naturalists at the end of the nineteenth
century, economic ornithology experienced first a meteoric
rise that was matched by a rapid demise. For ornithologists,
important lessons can be gleaned from this history.
Until fairly recently, birds and other wildlife were
largely viewed in economic terms as pests, food, or irrelevant. Even today, agricultural birds are often viewed as
pests, whether or not they cause any measurable impact
(Lindell et al. 2012). Interest in positive and negative roles
of birds spurred the US Congress to appropriate $5000.00
to the USDA to establish a section of economic ornithology
J Ornithol
in 1885 to investigate the diet, movements and other habits
of birds in relation to both insects and plants. The section
grew quickly, graduating into the Division of Biological
Survey in 1896 and the Bureau of Biological Survey in
1905.
Early work concentrated on bird-agriculture relationships, with an emphasis on agricultural production. A
goal of the division was to supply the growing agricultural industry with useful information. Consequently,
initial work concentrated on food habits of birds believed to be injurious or beneficial to agriculture. Similar
efforts in the UK started at the same time (Kronenberg
2014b).
Between 1885 and 1929, Bureau of Biological Survey
researchers contributed hundreds of publications intended
for a wide audience (Fisher 2011). Although the Bureau’s
early work was generally received enthusiastically, criticism of methods and skepticism regarding conclusions
grew. Three important flaws contributed to the eventual
decline of economic ornithology within the Biological
Survey. First, when Bureau scientists assessed diet through
analysis of stomach contents, they mostly used the
volumetric method to describe importance of the different
components of the diet. In this method, relative bulk representation determines the importance of any component
within the diet. The alternative numeric method, which
ultimately gained favor in the larger ecological community,
instead determined importance of items by frequency of
occurrence. Second, a conclusion that a particular bird
species (or group of species) was beneficial to agriculture
was seldom followed up with practical advice promoting
strategies aimed at enhancing the positive bird effects
through some practical manipulation that farmers could
implement (Evenden 1995). Third, and most importantly,
presence of a prey species (arthropod or rodent) in the diet
does not indicate how this affects the population dynamics
of that species. Consumption of a pest by a bird consumer
does not demonstrate avian control of that pest, leading
some entomologists to contend that economic ornithologists over-stated the importance of birds as control
agents. Paradoxically, coincident with the fall of economic
ornithology and the rise of synthetic organic pesticides,
studies from the 1940s through the 1960s that examined
birds in relation to agriculture emphasized birds’ potential
roles as pests rather than as pest control agents (Evenden
1995).
As reviewed by Bruns (1960), interest in the economic importance of birds in Europe developed during
the 1920s, and appears to have followed a somewhat
different trajectory from that in the US. Motivated by an
interest in economic bird protection, a variety of investigations sought to quantify food habits of birds. Investigators focused particularly on the relative
consumption of beneficial versus detrimental insects,
what quantities they consumed, and the relation of insect
consumption to insect abundance. Additional work examined the ability to increase bird density through
provisioning of nest boxes. A key difference in these
European investigations from the earlier North American
studies was a greater attempt to relate consumption to
abundance.
The many studies summarized by Bruns (1960) revealed
that birds often consume a large percentage of available
insects when insect densities are low, but that during insect
irruptions the proportion consumed may be miniscule. In
contrast to earlier views, Tinbergen (1949, in Bruns 1960)
and others found that many insect-consuming forest bird
species exhibit pronounced selectivities for certain insects.
Moreover, many species besides cuckoos were found to
consume hairy caterpillars, and one study (Koroljkowa
1956, as reported in Bruns 1960) found that birds preferentially consume caterpillars of the gypsy moth (Lymantria
dispar) that were unparasitized. Some studies that provisioned areas with nest boxes led to surprising increases in
density of some hole-nesting species, even when those
areas were at already high densities. Areas with increased
bird densities in response to nest box provisioning in turn
were found to have decreased densities of harmful insects.
Taken as a whole, Bruns (1960) concluded that the role of
forest birds in ‘‘forest hygiene’’ is most effective at maintaining harmful insects at benign densities: ‘‘The birds
generally are not able to break down an insect plague, but
their function lies in preventing insect plagues. It is our
duty to preserve birds from aesthetic as well as economic
reasons…the wood is still able to defend itself biologically
against insect plagues. It is our duty to further these biological forces (birds, bats, wood ants, parasites) and to
conserve or create a rich and diverse community. By such a
prophylactic, carrying out of ‘hygiene’ before a possible
outbreak of an insect pest, the forests will be better protected than by any other means.’’
Interest in birds’ ecological roles increased again in the
1970s, owing to comprehensive studies of ecosystem energetics. Although notable investigations (Holmes and
Sturges 1975; Sturges et al. 1974; Wiens 1973) suggested
that birds may contribute little to overall ecosystem energy
flux, exclosure studies demonstrated that bird predation
significantly affected population densities (and, presumably, population dynamics) of arthropods, including some
pests (Askenmo et al. 1977; Holmes et al. 1979; Solomon
et al. 1977).
Subsequent studies determined that predation of insectivorous birds on herbivorous insects positively affected
plant performance (Atlegrim 1989; Marquis and Whelan
1994). In contrast to the methods of economic ornithology,
these studies explicitly examined the trophic interactions
123
J Ornithol
from the plant’s perspective, addressing whether bird predation on insect herbivores increased plant performance or
fitness. These studies also ushered in renewed interest in
birds as potential biological control agents in both natural
and agro-ecosystems. Investigators today typically focus
data collection on a direct or indirect assessment of plant
performance, fitness, and in some circumstances, economic
consequences for humans. For instance, Mols and Visser
(2002) investigated effects of bird control of herbivorous
insects in Dutch apple orchards, and reported that increasing bird density through deployment of nest boxes led
to a 50 % reduction in apple damage and an increase of
about 60 % in total apple crop yield. Koh (2008) attributed
bird pest control to prevention of 9–26 % fruit loss in oil
palm (Elaeis guineensis). Johnson et al. (2009) found birds
significantly reduced damage by coffee berry-borer beetles
(Hypothenemus hampei), with higher coffee yields resulting in increased income from US$44 to US$310/ha.
Avian ecosystem services: a modern economic
ornithology
In light of modern approaches to avian ecology and renewed interest in avian ecological function and ecosystem
services, economic ornithology deserves further development, with both a broader focus and more rigorous
methodologies. The need for reliable quantitative assessment of bird-caused losses of agricultural production is
necessary to assure that costs of damage prevention do not
actually exceed the costs resulting from reduction in crop
yield. In addition, potential disservices associated with
provision of a service need to be more fully incorporated
into modern ecosystem service research (Table 1). To date,
most ES research has focused on the benefits provided and
has ignored disservices (Kronenberg 2014b). Finally,
quantifying the services and disservices is just one component of ES valuation. As we show below, some of the ES
provided by birds have no direct market value, and even
those that can be monetized may have additional nonmarket value. Reliance on market value to justify conservation policy is risky, because markets can change quickly,
as seen when the development of pesticides appeared more
effective than birds in pest control. On the other hand,
attempts to assess non-market value are often ignored or
criticized precisely because they do not have traditional
assessment for market value (Johnson and Hackett 2016).
Keeping in mind Bruns’ (1960) admonition that we must
preserve birds for aesthetic as well as economic reasons
can help guide holistic approaches to avian conservation
that recognize birds as more than simple pawns of economic cost-benefit assessments.
123
Pest control
A pest species decreases fitness, population size, growth
rate, or economic value of a human resource, such as an
agricultural crop. Many bird species may be observed in
gardens and agricultural fields, leading to a perception that
these species are raiding our gardens or crops as pests. For
such a species to function as a pest, however, it must not
only consume the crop, its consumption must be sufficiently large to reduce the resource’s value. This reduction
may be quantified in a variety of ways, from the yield and/
or the monetary value earned from harvest, to the number
of calories delivered to potential consumers.
Pest control reduces the effect of a pest, thereby increasing fitness, population size, growth rate, or economic
value of a resource important to humans. Pest control results from a direct negative effect of a pest control agent on
the pest, producing a positive indirect effect on the resource consumed by the pest to an extent that is economically important to humans.
Insects
More than 50 % of bird species are predominately insectivorous, and nearly 75 % eat invertebrates at least occasionally (Sekercioglu 2006b; Wenny et al. 2011). Many
studies have now examined top-down effects of birds on
invertebrates in a wide variety of natural and agro-ecosystems (Whelan et al. 2008). Most, though not all, of
these investigations have found that birds reduce population densities of invertebrates. Of these studies, many
found that the top-down effects on invertebrates cascade to
the level of the plants (Mantyla et al. 2011; Whelan et al.
2008).
Small mammals
Less studied are the potential roles of birds of prey as pest
control agents of small mammals such as rodents and
rabbits, and granivorous birds as pest control agents of
agricultural weeds (Whelan et al. 2008). Although few
studies since the early work of the Biological Survey have
examined the potential of birds of prey to contribute pest
control services in agro-ecosystems, current information
suggests a strong potential. Birds of prey affect population
dynamics of various rodent and other small mammal species in a variety of ecosystems around the world (Korpimaki and Krebs 1996), and many raptor species inhabit
agricultural ecosystems (Williams et al. 2000). Furthermore, the very presence of predators in an ecosystem reduces the activity of prey species as a result of the creation
of a ‘‘landscape of fear.’’ This effect has been shown to
J Ornithol
Table 1 Framework for ecosystem services research from an ecological perspective
Ecosystem service
Functional group
Potential disservices
Pest control (invertebrates)
Insectivores
Prey upon beneficial insects
Pest control (small mammals and birds)
Carnivores (raptors)
Prey upon poultry and game species
Weed seed control
Granivores
Crop damage
Seed dispersal (fleshy fruits)
Frugivores
Spread invasive species
Seed dispersal (aquatic)
Waterbirds
Spread invasive species
Seed dispersal (nuts)
Seed-caching birds
Crop damage
Pollination
Nectarivores
Pollinate invasive plants and help their spread
Nutrient cycling
Piscivores
Prey upon game fish
Plant damage in breeding or roosting colonies
Waste removal
Scavengers
Dispersal of weed seeds
Fruit crop damage
Habitat damage (tundra)
Eutrophication of aquatic habitats
Spread disease
Nutrient cycling
Disease control
Most previous research has focused on the positive benefits of ecosystem services (left column), but potential costs (right column) of the service
should also be studied
reduce rodent activities when barn owls are present
(Abramsky et al. 1996). Deployment of hunting perches
boosts populations and/or activity-density of various hawks
and owls (Kay et al. 1994; Sheffield et al. 2001; Wolff et al.
1999), leading, in some cases, to decreased rodent
population density (Kay et al. 1994). Existing evidence
thus suggests that birds of prey have the potential to provide pest control services in agro-ecosystems, and the deployment of perches and nesting structures facilitates
recruitment of those services.
Agricultural weeds
Since the studies of Judd (1901, 1902), almost no effort has
been made to assess the role of granivorous birds in the
abundance and distribution of herbaceous agricultural
weeds (Holmes and Froud-Williams 2005; White et al.
2007). Numerous bird species around the globe are seasonally granivorous, and many of these species consume
seeds of native forb and grass species, some of which are
weeds in agro-ecosystems. Barrows (1889) and Judd (1901,
1902) suggested that native avian granivores in the U.S.
may preferentially consume seeds of native herbs and forbs,
even as the non-native house sparrow (Passer domesticus)
prefers seeds of commercial cereal grains. This is an area
that deserves careful, quantitative research. Given that
many of the passerine granivores are seasonally insectivorous (during their breeding seasons) or granivorous
(non-breeding season), they potentially could serve as both
insect and weed seed pest control agents (e.g., Ndang’ang’a
et al. 2013). Various impact studies could be usefully implemented. For instance, some bird species, such as the
American goldfinch (Spinus tristis) in North America, often
forage on seeds before dispersal (pre-dispersal seed predation), while others seem to forage on seeds post-dispersal.
What is the relative magnitude of seed losses of these two
processes? Are they additive or compensatory? Can we
manipulate agricultural landscapes in ways that might encourage granivorous bird species’ habitat use without sacrificing agricultural yield and efficiency and/or facilitate
their effectiveness as granivores (as has been demonstrated
for granivorous insects—see Landis et al. 2010)?
Disservices: crop damage
Crop damage by birds is arguably their most recognized
ecosystem disservice, but the economic losses resulting
from birds are not well quantified. Frequently the perceived
extent of crop loss or damage, as indicated by opinion
surveys, is much greater than the actual losses measured in
the field (Gebhardt et al. 2011). Similarly, the perception
that bird presence in an agricultural field indicates crop
damage by those species is often incorrect (Greene et al.
2010; Lindell et al. 2012). For instance, based on energetics and population size estimates, Weatherhead et al.
(1982) estimated that damage to corn based on subjective
governmental surveys over-estimated crop losses astronomically (10009). Energetics estimates were well
within empirically based, replicated field estimates
(Weatherhead et al.: 0.41 % of crop damaged; field
123
J Ornithol
estimates: 0.25–0.80 % crop damaged). Basili and Temple
(1999) estimated comparable magnitudes of regional losses
of sorghum (0.37 %) and rice (0.73 %) crops owing to
dickcissel (Spiza americana) wintering flocks in
Venezuela, contrasting with the subjective impression
among area farmers of an average loss of 25 % of either
crop. Subjective impressions and estimates of crop loss are
easily exaggerated due to the size of wintering bird flocks,
their conspicuousness and highly localized concentrations.
Overall, crop losses due to birds are probably fairly low,
especially when compared with damage caused by rodents
and insects. Similarly, the red-billed quelea (Quelea quelea), an abundant granivorous species widely considered a
crop pest in Africa, may cause high crop damage locally,
but cause \1 % loss of continental production (Elliott and
Lenton 1989).
For example, red-winged blackbirds (Agelaius phoeniceus) feed on pre-harvest corn kernels for a short period in
the fall, causing some crop loss (Dolbeer 1990; McNicol
et al. 1982). However, measured crop damage was \1 %,
far below government estimates of about 20 % crop damage (Weatherhead et al. 1982), and was primarily in fields
near wetlands and blackbird fall roosting sites. Most importantly, blackbirds eat substantial amounts of invertebrates, especially during the breeding season when corn
kernels are developing. These invertebrates include corn
insect pests that cause far more crop damage than blackbirds (Bendell et al. 1981; Tremblay et al. 2001). In the 30
years since these studies, less palatable corn varieties have
been developed that likely reduce blackbird damage to corn
even further, and anthraquinone-based repellent reduced
blackbird damage to corn by 28 % (Carlson et al. 2013). A
recent study in North Dakota showed that a mean of 0.2 %
of the corn crop in randomly selected plots was damaged
by blackbirds in 2009–2010 (Klosterman et al. 2013).
Similar results have been found for other crops. For example, blackbirds had no effect on stink bugs on rice and
caused damage themselves, but this did not result meaningful reduction in crop yield (Borkhataria et al. 2012).
Nevertheless, some parts of fields can have [10 % damage
(Conover 1984), and in some cases, even slight damage can
prevent corn from being sold for human consumption
(Dolbeer 1990).
A critical research need is to examine in detail the entire
life cycle of key ‘‘avian pest’’ species, quantifying both the
negative and positive effects of their habit use and foraging
behavior on agricultural crops. Such studies also need to
account for the economic and ecological costs of avian and
non-avian pest control measures. Such detailed analyses
may well demonstrate that the cost of avian pests is usually
less than what farmers perceive (e.g., Basili and Temple
1999), and that avian ‘‘pests’’ in fact provide benefits to the
farmer. Furthermore, the invertebrates likely cause far
123
greater damage to crops than do birds, so attempts to
control perceived avian pests may backfire and lead to
greater crop damage by invertebrates (Becker 1996).
Studies should also examine the costs and consequences of
controlling the pest species. For example, efforts to control
queleas with lethal means may have a short-term benefit for
local crop production, but longer-term negative consequences (both direct and indirect) on non-target bird species and even on humans (Jaeger and Elliott 1989;
McWilliam and Cheke 2004; Meinzingen et al. 1989).
Disservices: birds feeding on beneficial insects
Not all bird-insect interactions are beneficial for farmers.
Insect pest populations may also increase as a result of
birds feeding on predaceous insects and parasitoids (Sekercioglu 2006a). However, Hooks et al. (2003) found that
excluding birds did not increase spider predation of herbivorous insects. Actually, birds alone were significantly
better at controlling insects and reducing plant damage than
spiders alone, with 18 % of plants showing extensive defoliation with only spiders versus 0 % with only birds.
Although birds may reduce numbers of insect parasitoids
(Tscharntke 1992) by feeding on infected insects, various
lepidopteran parasitoids only emerge from the pupal stage
and thus cannot prevent defoliation by the caterpillars
(Hooks et al. 2003). Parasites may actually lead to increased foliage consumption (Coleman 1999). Various bird
species often complement other natural enemies by selecting for non-parasitized individuals (Otvos 1979) and
facilitating the spread of viruses (Takekawa et al. 1982).
On the other hand, bell miners (Manorina melanophrys)
are an unusual species that causes infestations of an insect
herbivore (Loyn et al. 1983). These highly territorial birds
mostly feeds on the nymphs, sugary exudates, and lerps
(protective carbohydrate covers) of psyllid homopterans,
the birds often being careful only to remove the lerps with
their tongues without disturbing the nymph (Loyn et al.
1983). This ‘‘tending’’ behaviour, combined with bell
miners’ aggressive group territorial defense, can result in
psylid infestations of Eucalyptus trees, sometimes resulting
in their defoliation and death (Loyn et al. 1983).
Seed dispersal
At least 33 % of bird species disperse seeds, primarily
through fruit consumption, but also through herbivory and
granivory by waterbirds, and scatter-hoarding of nuts and
conifer seed crops by seed-caching birds (Sekercioglu
2006b; Whelan et al. 2008). With the exception of birds
dispersing mistletoes, most bird dispersers interact with
most plant species in a generalized or diffuse manner. A
J Ornithol
single bird species consumes fruits of many plant species,
and the fruit of a single plant species is consumed by many
bird species. The number of plant species dispersed by
birds is not precisely known, but our working estimate is
80,000 (*30 %) species of angiosperms and 650 (*60 %)
of gymnosperms (Green et al. 2016; Tomback 2016;
Wenny et al. 2016).
Fleshy fruits
Birds are ideal seed dispersers. Frugivorous species
typically swallow fruits and seeds intact. Birds are highly
mobile and many migrate long distances. Birds occur
nearly everywhere and provide mobile links within and
among habitats. In most cases, seeds cannot germinate
from within an intact fruit. An additional and frequently
overlooked benefit of endozoochory is the removal of fruit
skin and pulp from the seeds during the interaction (Samuels and Levey 2005; Traveset and Verdu 2002). Consequently, any bird–plant interaction involving seed
handling or ingestion potentially benefits the plant.
Some frugivorous bird species are considered pests of
fruit crops, including grapes (Vitis), blueberries (Vaccinium), strawberries (Fragaria), among others (De Grazio
1978; Greig-Smith 1987). Other frugivorous bird species
disperse invasive plant species. Like granivorous species,
however, many frugivore species also eat many invertebrates during the breeding season. The relative costs and
benefits of such diet switching have not been evaluated for
any species in an ecosystem services context.
Aquatic plants
Although the role of waterfowl as seed dispersers was
recognized decades ago (Ridley 1930), only recently has
the ecology of this interaction been studied. Waterfowl
(Anatidae; *150 species) occur worldwide, are migratory
or otherwise capable of long-distance movements, and
many species are largely vegetarian. Thus, waterfowl can
be highly effective mobile links within and among wetland
habitats (Green and Elmberg 2014).
Seed caching
Approximately 20 species of pines (Pinus) are dispersed by
jays and nutcrackers (Corvidae; Tomback and Linhart
1990). These pines occur in western North America and
across Eurasia and are distinguished from the primarily
wind-dispersed species by having large seeds that lack a
well-developed winged appendage for wind dispersal and
cones that require seed removal by animals (Tomback and
Linhart 1990). Corvids also disperse oaks and beeches
(Fagaceae) by scatterhoarding. Although the presumed
mutual adaptations in these species are less clear than for
nutcrackers and pines, many seeds are cached in suitable
sites for germination and establishment.
Disservices: seed predation and dispersal of invasive
species
Some granivorous birds, such as finches and parrots, can be
significant seed predators (Sekercioglu 2006a). Red crossbills (Loxia curvirostra) in Spain consume more than 80 %
of the ripening seeds of relict Scots pines, whose regeneration is limited by the high rate of seed predation (Castro
et al. 1999). Avian seed predation may increase in tropical
forest fragments, since many tropical granivorous birds are
more common in forest fragments and outside forests than
in extensive forest (Bregman et al. 2014; Sekercioglu
2012). In the forest fragments of southeast Brazil, where
rodent seed predators have declined and granivorous birds
have increased, birds have become important, if not the
main seed predators of Croton priscus (Euphorbiaceae)
(Pizo 1997). As detailed above, although birds can be crop
pests, damage estimates are often exaggerated and not
collected scientifically (Weatherhead et al. 1982).
Introductions of non-native species can turn avian seed
dispersal service into a disservice. Avian seed dispersers
can contribute to the spread of invasive species with generalized dispersal mechanisms (Renne et al. 2002). In the
Usambara Mountains of Tanzania, silvery-cheeked hornbills (Ceratogymna brevis) are effective long-distance (up
to four km) dispersers of the exotic Maesopsis eminii
(Rhamnaceae) (Cordeiro et al. 2004), and significantly
contribute to the rapid invasion of this West African species, which is also dispersed by Ceratogymna hornbills in
its native habitat (Holbrook and Smith 2000).
Pollination
Over 920 species of birds pollinate plants, including
hummingbirds (Trochilidae) in the Americas, sunbirds
(Nectarinidae) in Africa, false-sunbirds (Philepittidae) in
Madagascar, flowerpeckers (Dicaeidae) and white-eyes
(Zosteropidae) in southern Asia, Honeyeaters (Melphagidae) lories (Loridae) in Australasia, and Hawaiian honeycreepers (Drepanididae) in Hawaii (Stiles 1981). In
contrast to seed dispersal, birds pollinate a relatively small
percentage of plant species (Sekercioglu 2006a; Whelan
et al. 2008). However, in some parts of the world like
Australia and certain oceanic islands, avian pollination
reaches important levels and can exceed 15 % of the plant
species in a community (Anderson et al. 2016). Compared
to seed dispersal limitation, there have been far fewer
studies of the importance of avian pollination limitation,
123
J Ornithol
which can result in reduced seed set and long-term
population declines, especially in island communities with
a high proportion of avian pollinators, such as New Zealand (Kelly et al. 2010), Bahamas (Rathcke 2000) or Hawaii
(Sekercioglu 2006a).
Disservices: pollination of invasive species
and nectar robbing
As is the case with seed dispersal, some birds help spread
invasive plant species by pollinating them, especially in
places like Hawaii where there are many introduced bird
and plant species. Furthermore, some ‘‘nectar robbers’’ can
access nectar without pollinating the plants (Proctor et al.
1996; Sekercioglu 2006a). The quality of an avian pollinator is often correlated with its bill length. Some of the
shortest billed hummingbird species, such as the thornbills
(genus Chalcostigma) and fiery-tailed awlbill (Avocettula
recurvirostris), as well as passerine flowerpiercers (genus
Diglossa), are mainly nectar robbers, using their sharp bills
to pierce flower corollas and consume nectar without providing any pollination in return. Interestingly, nectar robbing may sometimes have little to no negative effect on
plant fitness, and may even result in some pollination (see
Sekercioglu 2006a for references).
Scavenging
The ecological importance of scavenging birds is often
underappreciated. Despite the common assumption that
decomposers (i.e., microbes and insects) are primarily responsible for recycling carrion biomass, DeVault et al.
(2003) demonstrated that vultures and other vertebrate
scavengers usually consume most available carcasses in
terrestrial ecosystems. Although vultures are one of the
most recognizable types of birds to non-ornithologists, this
familiarity is often not accompanied by appreciation of the
services they provide. By scavenging, vultures and other
carnivorous vertebrates contribute to waste removal, disease regulation, and nutrient cycling (DeVault et al. 2003;
Houston 1979).
Disservices: spreading disease
Although avian scavengers are generally found to decrease
disease propagation, in some circumstances they may instead have the opposite effect (see Jennelle et al. 2009). For
instance, the survival of scrapie prions of passage through
the digestive system of American crows (Corvus
brachyrhynchos) may facilitate proliferation of prion diseases (VerCauteren et al. 2012). However, relatively little
is known about how avian scavengers influence disease
123
ecology of both humans and wildlife, and additional research in this area is critically needed.
Nutrient cycling
Birds contribute to nutrient cycling in all habitats, but most
impressively where aquatic birds nest colonially on islands
(Anderson and Polis 1999; Polis and Hurd 1996). Seabirds
often nest in dense colonies both in coastal areas and on
islands, processing large amounts of food in small areas.
The result is significant input of nutrients from the aquatic
zone to the terrestrial zone. Such large inputs of phosphaterich guano can influence the structure and composition of
plant communities (Ellis 2005), and guano has historically
been of great economic value both as a fertilizer and in
manufacture of munitions. Because phosphorous has no
gaseous form at ambient temperatures, it does not move
from aquatic to terrestrial ecosystems through atmospheric
processes, and transport via piscivorous birds is thus critical over short time horizons.
Disservices: eutrophication
Avian nutrient transport can sometimes affect ecosystems
negatively (Sekercioglu 2006a). Aquatic systems, especially ponds and wetlands, and small lakes, may experience
eutrophication owing to massive inputs of nitrogen and
phosphorus from bird excrement (Kerbes et al. 1990;
Manny et al. 1994; Post et al. 1998). Excessive terrestrial
nutrient deposition can inhibit plant growth (Gillham 1960)
and even cause plant death. Abundance and species richness of invasive plant species may increase in areas of
greatest intensity of bird colonies (Vidal et al. 2003), since
these plants often have high disturbance tolerance and
colonizing capacity. Large concentrations of ducks and
geese can add excessive amounts of nutrients to wetlands,
parks, and other open areas, reducing water quality, destroying vegetation, creating pollution, and even causing
disease outbreaks (Post et al. 1998). Manny et al. (1994)
calculated that of all outside nutrients that entered Michigan’s Wintergreen Lake, waterfowl added 69 % of carbon,
27 % of nitrogen, and 70 % of phosphorous, the last two of
which can lead to eutrophication.
Conclusions
Keeping in mind the decline of Economic Ornithology in
the early twentieth century, efforts to modernize the field
today must ensure that the approach is rigorous, repeatable,
and focused on tangible measures of the direct and indirect
benefits to human society (Kronenberg 2014b; Whelan
J Ornithol
et al. 2008). Bird contributions to ecosystem service and
disservice with respect to the replacement of the service by
human labor or technology may be compared with costbenefit analysis (e.g., bird predation versus pesticides for
pest control). Investigations or methods that permit scaling
up from experimental plots to entire ecosystems (Rogers
et al. 2012; Whelan et al. 2008) are critical.
We have made considerable progress in building conceptual frameworks for economics of ecosystem services.
Important considerations include whether the bird species
responsible for the service is unique or part of a redundant
network (Power et al. 1996). Regardless of redundancies,
several studies indicate the importance of species richness
for delivery of ecosystem services, implying that, even
with redundancies, each species counts (Barbaro et al.
2014; Cordeiro and Howe 2003; Garcia and Martinez 2012;
Kelly et al. 2010). Also critical is the temporal and spatial
scale over which any potential service is generated (Chee
2004). Ecosystem service accounting needs to consider the
intrinsic variability inherent in the production of any
ecosystem service. Ecosystem processes naturally vary
over time. Understanding natural variability is thus critical
to the proper accounting of ecosystem services (MEA
2005).
Avian ecologists have made great strides in understanding and documenting the many ecosystem services
provided by birds, yet knowledge gaps persist and need
filling. We know appreciably more about how birds function as consumers of arthropods and fruits than as consumers of nectar. We thus know more about how birds
function as pest control agents of herbivorous insects and
as seed dispersers, respectively, than as pollinators. Additional research regarding which plant species are pollinated
by which bird species, and the effectiveness of birds relative to other pollinators, is critical. More research on avian
granivory in agro-ecosystems, particularly with respect to
seasonal switching of diet between seeds and arthropods, is
also needed.
When birds contribute multiple ecosystem services (e.g.,
reduction of weed seed in nonbreeding season and insect
pest control in breeding season), we must determine the
relative demographic impacts of each service. The same
holds when different co-occurring species contribute such
different ecosystem functions and services. Rarely if ever
do we know the demographic contribution of birds for any
one of these roles, let alone their synergistic (or antagonistic) effects. Cost–benefit analysis should be applied
when alternative ecosystem ‘‘components’’ might be
available (use of pesticides versus encouragement of bird
predation).
Rapidly changing climate and other types of global
change are forcing shifts in the distributions of birds,
plants, and other species, resulting in new ecological
interactions, particularly in the understudied tropics that
host most of the world’s bird species (Sekercioglu et al.
2012; Sodhi et al. 2011; Wormworth and Sekercioglu
2011). Ecologically specialized bird species are substantially more threatened with extinction and we still know
little about the ecological consequences of bird extinctions.
A better understanding of birds’ ecological functions and
services is urgently needed for conserving bird populations
and their ecological contributions.
Conflict of interest
of interest.
The authors declare that they have no conflict
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