Nest Predation and Nest Sites
Thomas E. Martin
BioScience, Vol. 43, No. 8. (Sep., 1993), pp. 523-532.
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Fri Sep 21 11:01:59 2007
Nest Predation and Nest Sites
New perspectives on old patterns
Thomas E. Martin
I
dentifying causes of general patterns of habitat selection, species
coexistence, and life-history traits
are central issues in evolutionary ecology. Many organisms have been studied to address these issues, but no
group has had a greater influence on
current perspectives than birds
(Konishi et al. 1989).
Rapid advances came a few decades ago with work by Lack (1948,
1954),Hutchinson (1957,1959), and
MacArthur (1958, 1972) and his associates (Cody and Diamond 1975).
These investigators argued that
competition and food limitation were
the major underlying influences of
habitat selection, species coexistence,
and life-history traits among birds (reviewed in Martin 1986, 1987). In recent years, the ubiquity and importance of competition and food
limitation have been debated (Salt
1983, Wiens 1989).
Nonetheless, although the competition paradigm has been challenged,
alternative explanations are rarely
explored for birds. New hypotheses
need to be developed and examined,
and they need to be directed at old and
long-standing patterns that have been
interpreted in the conventional perThomas E. Martin is an associate professor and assistant unit leader at the US
Fish and Wildlife Service, Arkansas Cooperative Fish and Wildlife Research Unit,
Department of Biological Sciences, University of Arkansas, Fayetteville, AR
72701. His current address is the Montana Cooperative Wildlife Research Unit,
Department of Biological Sciences, University of Montana, Missoula, M T
59812.
September 1 993
Nesting season can be a
critical period for
maintenance of bird
populations
Habitat selection and
species coexistence
More t h a n three decades ago,
MacArthur (1958) published a study,
widely cited in general biology textbooks, showing that five coexisting
warbler species differed in their foraging locations and methods (Figure la).
This partitioning of resources among
coexisting species is an old and wellstudied pattern that has long been
considered necessary for coexistence
(reviewed in Schoener 1974, 1986).
MacArthur and others also showed
spectives of competition and food limitation.
In this article, I focus on nest predation as a process and nest sites as a
resource. Predation is considered an
important process in many systems
(e.g., aquatic systems), but it has been
neglected as an evolutionary process
in avian systems (Martin 1988c,
1992b, Sih et a1 1985).This neglect of
nest predation as an evolutionary force
is surprising because population studies indicate that nest predation is pervasive; nest predation has been observed to be the primary source-ofnest
losses across a wide diversity of species, habitats, and geographic locations, accounting for 80% of nest
losses on average (Martin 1992a,
1993, Ricklefs 1969). Natural selection should favor birds that choose
habitats, communities, and life-history traits that reduce the negative
effects of nest predation given the
importance of reproductive success to
fitness. I will show how nest predation and nest sites can provide viable
alternative hypotheses for long-standing patterns of habitat selection, spe- The colors of this female orange-crowned
cies coexistence, and life-history traits warbler, as it stands on the edge of a nest
that traditionally have been attrib- under a maple stem, are similar to the
uted to food limitation and competi- colors of the plants and litter surroundtion.
ing the nest site. Photos: Thomas E. Martin.
Birds are often inconspicuous in their nests in the sites they choose for nrs~1115.lhis
female orange-crowned warbler (center of photo) has nested in a site without woody
vegetation.
that numbers of coexisting bird species increase with vegetation density
and spatial heterogeneity (Karr and
Roth 1971, MacArthur et al. 1962,
Willson 1974), a pattern that exists in
many other animal foraging systems,
including lizards, mammals, freshwater fish, and marine intertidal organisms.
These two well-documented patterns generate two questions: Why is
foliage density important to choice of
habitats? Why do increasing numbers
of species coexist in habitats with
more foliage and greater structural
heterogeneity? Historically, these
questions have been explained in terms
of food limitation and competition:
birds were thought to choose habitats
with greater foliage density because
more foliage provided more food, and
more species were thought to coexist
in habitats with greater structural heterogeneity because there were more
types of foraging sites to partition to
minimize competition (MacArthur
1958, 1972, MacArthur et al. 1962;
see Martin 1986). Yet, evidence of
competition and food limitation was
indirect or absent, and other processes
were not examined.
Habitat selection. Dense foliage and
increased structural heterogeneity can
affect habitat choice by reducing risk
of predation in aquatic systems (e.g.,
Sihet al. 1985, Werner and Hall 1988).
Birds may similarly choose habitats
with dense vegetation to reduce the
probability of nest predation. Foliage
next to the nest can reduce the probability of predation by concealing the
nest. Indeed, predation rates were
lower at nests with greater concealment in 29 of 36 studies (Martin
1992a). At a larger spatial scale, foliage in the patch (5-meter radius circle)
surrounding the nest may also influence predation risk; dense and complex vegetation may impede the ability of mobile predators to locate
sedentary prey (e.g., nests), even when
the prey are poorly concealed. The
latter result is expected primarily if
predators are searching vegetation
randomly. However, bird species (and
sedentary organisms) usually specialize on individual plant species for
nesting and, thus, do not use vegetation randomly. In such cases, predators waste time and effort if vegetation is searched randomly. Instead,
predators should only search substrate
types that represent potential sites for
encountering prey.
As a result, pfedation risk and patch
choice may be influenced by numbers
of potential prey sites rather than
foliage density per se, thereby creating two mechanistic hypotheses. The
total-foliage hypothesis states that
reda at ion risk decreaseswith increases
in total vegetation in the nest patch
because greater foliage density inhibits transmission of visual, chemical,
or auditory cues by prey. The potential-prey-site hypothesis states that
increases in the density of plants of the
type used by prey reduces the probability of predation because it increases
the number of potential prey sites that
must be searched and can cause the
predator to give up before finding the
occupied site.
I tested the response of predators to
numbers of unoccupied and occupied
sites using artificial nests baited with
quail (Coturnix coturnix) eggs (Martin 1988b). I put out seven nests per
patch and varied the number of eggcontaining nests in each patch (one,
three, or seven of the seven nests contained eggs). Each of the three experimental treatments was represented by
ten patches. Predation rates for any
nest in a ~ a t c hdecreased with increases in ;he number of nests that
were unoccupied (Martin 1988b).Such
results show that predators can respond to numbers of unoccupied and
occupied prey sites, at least in an
artificial setting.
Potential prey sites are represented
in a natural setting by plants of the
species and size used for nesting. Nest
predation should decrease with increased number of these ~ l a n t under
s
one of the simplest situations of the
potential-prey-site hypothesis. Under
the total-foliage hypothesis, predation should decrease with increases in
numbers of total stems rather than the
subset of stems of the type used for
nesting. These predictions were tested
on study sites in high-elevation snowmelt drainages in Arizona (Martin
1988a) by counting the number of
stems in a 5-meter-radius circle surrounding nests. Analyses of hermit
thrushes (Catharus guttatus) and
MacGillivray's warblers (Oporomis
tolmiei) support the potential-preysite hypothesis; nest predation was
reduced when the nest patch contained more potential nest sites (FigBioScience Vol. 43 No. 8
ure 2). The total foliage hypothesis
was rejected for both species; predation rates were not reduced at nests
surrounded by more total vegetation
stems (Figure2; also Martin and Roper
1988).
predation risk is not necessarily
always high in small patches (few
potential prey sites);if birds only used
large patches, then predators should
ignore small patches in the same way
they ignore unused substrate types,
and anv bird that used a small ~ a t c h
would escape predation. Of course,
predators would learn to explore small
patches as numbers of prey using them
increased. and vredation rates would
quickly ekala& because of the low
search time in small patches. This
arms race should ultimatelv level off
with birds using patches in proportion
to their relative abundance and the
amount of time it takes the predator
to search them. Thus, some birds (conspecifics or a different species) should
use small patches; in Arizona, greentailed towhees (Pioilo chlorurus)
choose small patchei of firs, whereaH
hermit thrushes and MacGillivray7s
warblers mostly choose large patches.
If birds select nesting patches that
reduce predation risk, then they should
choose patches with greater numbers
of ~otentialnest sites in situations in
wgich these are the patches with the
least risk of predation (e.g., hermit
thrush and MacGillivray's warbler).
Patches used for nestine were compared to unused patches :entered on a
stem of the same type used for the nest
(nonuse patches). These comparisons
showed that patches used for nesting
by MacGillivray7swarblers and hermit thrushes did indeed have more
potential prey sites, but not more total
vegetation, than nonuse patches (Martin and Roper 1988).' Such choices
minimize predation risk given the patterns of predation found for these two
species (i.e., Figure 2). Moreover, some
species, such as the hermit thrush, do
not forage in vegetation of the type
used for nesting, so abundance of
foraging sites can be eliminated as a
basis for these nest patch choices (see
Martin and Roper 1988). Thus, birds
choose nest sites and patches with
reduced risk of nest predation.
Predation risk can increase with
prey density (Martin 1 9 8 8 ~but
) ~such
'T.E. Martin, 1993, unpublished data.
September 1993
The colors of this female red-faced warbler, sitting on its nest, match some df the
colors of the general area-even the orange color of the bird's face resembles the color
of some leaf elements in the surrounding litter. The color and brightness of this site
contrasts with that of the orange-crowned warbler (see photo page 523).
effects could be offset by greater numbers of potential prey sites, given that
the latter apparently reduce predation
risk. Consequently, numbers of individuals and species may increase with
foliage density due to increasing numbers of potential nest sites (Martin
1988a), rather than the historical argument of greater .numbers of foraging sites (e.g., MacArthur 1972,
MacArthur et al. 1962).
I tested this possibility by reanalyzing a classic study by Willson
(1974); she showed that bird species
numbers increased with the addition
of shrub and tree layers, but she questioned the importance of foragingsubstrates to this result. I reanalyzed her
data by classifying species based on
nesting versus foraging sites and found
that more of the species that were
added with shrub and tree foliage
layers were species that nested in those
layers than species that foraged in
them (Martin 1988a). Moreover, examination of the correlation between
number of species and density of foliage in these above-ground layers
showed that almost 20% more of the
variation in species numbers was explained based on nesting preferences
than on foraging preferences.
Similar results were obtained for
my sites in Arizona (Martin 1988a).
Thus, availability of nest sites with
low risk of predation provides a strong
alternative explanation for the long-
standing relationship between bird
species numbers and foliage profiles.
Of course, such effects do not eliminate the possibility that food limitation and competition are also operating, but the results challenge the
priority of the latter processes and
show that they certainly are not the
only explanations for these patterns.
Coexistence of species. Nest predation may also affect the types of species that successfully coexist, based
on similarity of their nest sites. When
different species use the same site for
nesting, then density of potential prey
sites is held constant but prey density
for that site is increased by coexistence (Figure 3b). If predation risk
increases with cumulative prey density, then predation risk should increase for all species using similar nest
sites and thus exert negative selection
on coexistence (Martin 1988c; also
see Holt 1977,1984). If these species
use different nesting sites, then the
predator must search more substrates,
thereby reducing search efficiency and
reducing the cost of coexistence (Figure 3a). When nest site differences are
sufficiently large to make searching
both sites too costly to the predator,
then coexistence should not affect
predation rates. Such effects can favor
coexistence of species that use different nest sites (Martin 1988b,c). These
nest site differences can occur in two
horizontal nesting space. The 12 species on the Arizona sites were dispersed vertically, with four species
nesting on the ground, three species
nesting in the shrub layer, two species
nesting in the subcanopy, and three
species in the ~ a n o p y .Data
~
from
other avian communities also showed
that birds were, moreover, dispersed
vertically based on their nesting sites
than on their foraging sites (Martin
1988~).
species within a vegetation layer
differed in nest substrates and microhabitats along a short moisture gradient in the Arizona snow-melt drainages (Figure lb). Each of the four
ground-nesting species places nests at
the base of different plant species (Figure 5) that occur at different abunA red squirrel (Tamiasciurushudsonicus) dances along the moisture gradient
robs a bird nest. This photo was taken by (Figure lb). The three shrub-nesting
an automated camera.
species overlap in substrate use (all
use small firs), but they chose these
spatial dimensions: vertical (i.e., firs in different microhabitats along
among vegetation layers) and hori- the moisture gradient; green-tailed
zontal (i.e., among substrates or mi- towhees chose small firs in drier sites
crohabitats in the same vegetation where New Mexican locust was more
layer).
abundant. whereas MacGillivrav's
I used artificial nests to experimen- warblers chose small firs in patc6es
tally test the prediction that predation with more maple, and hermit thrushes
favors nest site differences among co- chose small firs in patches with more
existing species (Martin 1988b). Nests small firs than the other two specie^.^
were placed in positions that simu- These differences in nest site use among
lated nesting locations of four species coexisting species are greater than for
occurring on the study sites in Ari- foraging sites because birds specialize
zona. Nests were divided among the (use a site more than 60% of the time)
sites of these four species in one treat- on nest sites that differ among species
ment to simulate coexistence of four (e.g., Figure 5), whereas birds are
species that use different nest sites much less specialized and overlapmore
(Figure 3a). In a second treatment, based on foraging sites (Figure la).
nests were placed at the same total
If nest predation favors this use of
density but were placed in only one of different nest sites by coexisting spethe four sites to simulate all four spe- cies (or favors coexistence of species
cies using the same site (Figure 3b). that already use different sites based
Predation rates were ~redictedto in- on their evolutionary histories), precrease when cumulative density of dation rates should be greater for spenests increased in a particular nest site cies that use nest sites that are similar
due to overlapping use by coexisting to those used by other species. Indeed,
species (Martin 1 9 8 8 ~ )Indeed,
.
nest predation rates were greater for guilds
predation rates were much greater (shrub nesters) and species within a
when the simulated species used the guild that placed a greater proportion
same site than when they used differ- of their nests in sites that were similar
ent nest sites (Figure 4). Thus, these to other coexisting species.'
The cost of using nest sites that are
experiments indicate that nest predators exhibit behaviors that can favor similar to other coexisting species is
nest site differences among coexisting clearly shown by MacGillivray's warblers. They place their nests in small
species.
Examination of nest site use by
birds on my Arizona sites indicated =Seefootnote 1.
that they do in fact differ in where 'See footnote 1.
they place their nests in vertical and 'See footnote 1.
firs or short maple thickets. Small firs
are also used as nest sites bv hermit
thrushes and green-tailed {owhees,
whereas MacGillivray's warbler is the
only species that uses the short maple
thickets on these sites. As a result,
cumulative nest density in small firs is
slightly more than four times as great
as in the maple. If predators respond
to cumulative densities, predation
rates should be greater for MacGillivrav's warblers nests in small firs
than thbse in maple. ~ndeed,daily
mortality rates were significantly
greater in firs than in maple (Figure
6), and total percentage of nests lost to
predation was substantially greater in
firs (78.3%) than in maple (39.0%).
Moreover, experiments with artificial
nests showed that this trend could be
reversed by increasing the cumulative
density of nests in maple compared
with small firs: when nests in m a ~ l e
were four times as dense as nests in
small firs, daily mortality rates of
nests in maple were much higher than
for nests in small firs (compare striped
bar of maple with open bar of fir in
Figure 4). Such results show that differences in reda at ion rates between
these substrites are from differences
in density of nests rather than differences in the substrates.
In summary, artificial and real nests
show that risk of nest predation increases with overlap in nest site use
among coexisting species and thereby
provides a strong alternative hypothesis to food-based competition for
resource partitioning among coexisting species. Indeed, partitioning of
microhabitats among coexisting species is much greater when based on
nest sites (Figures 1b and 5) than on
foraging sites (Figure 1a). Moreover,
the results show a direct fitness cost
(i.e., increased nest predation) with
overlap in nest site use among coexisting species, whereas fitness costs of
overlap in foraging sites are largely
undocumented.
Constraints of evolved nest
placement on local success
Predation may favor nest site specialization within species because use of
new sites may either overlap sites already used by other coexisting species
or because species may not be adapted
to new sites in terms of, for example,
cryptic coloration or physiological
BioScience Vol. 43 No. 8
Cape May
warbler
Blackburnian
warbler
Black-throated
green warbler
Bay-breasted
warbler
Myrtle warbler
,Green-tailed towhee
Giilivray's warbler
Hermit thrush
Figure 1. a. Foraging locations of five species of warblers coexisting in northeastern
spruce woods (modified from MacArthur 1958). The diagram indicates six vertical
and three horizontal zones in trees that are most frequently used by each warbler
species. The zones of most concentrated activity are shaded such that at least 60%
of the observed foraging attempts are in the shaded zones (MacArthur only shaded
to 50% in his original article). Numbers are the percentage of observed foraging
attempts in shaded zones. Note that any zone of concentrated activity in the top three
vertical layers (only the myrtle warbler uses lower zones) is usually used as a zone of
concentrated activity by at least three species. In fact, the cumulative percentage of
time spent in any zone by all species combined is greater than for any individual
species that concentrates activity in that zone. In short, species overlap markedly in
their use of any foraging zone even when only considering the zones that comprise
60% of the foraging activity. b. Schematic drawing of vegetation and bird distribution
along a moisture gradient in snow-melt drainages in Arizona (unpublished data). The
lower parts of drainages are moist and characterized by plant species such as canyon
maple (Acer grandidentatum) and quaking aspen (Populus tremoloides). The upper
sides of drainages are drier and typified by xeric-tolerant plant species such as New
Mexican locust (Robinia neomexicana). Small white firs lAbies concolor) were
distributed throighout the entire gradient. These gradieAts (i.e., hillsides) are
generally only 35-70 m in length. The four ground-nesting bird species (identified
underneath the gradient) nest at the base of different plant species that occur at
different points along the gradients. When the plant species that comprise 60% of the
nest substrates for a species are examined, almost no overlap in nest substrate use
occurs among species (see Figure 5 ) . The three shrub-nesting bird species (identified
above the gradient) all use small firs but use the firs in different parts of the gradient
such that the microhabitat conditions surrounding the firs differ.
tolerance to the microclimatic condi- strate type; e.g., Figure 5 ) .Moreover,
tions. Indeed, data from Arizona show a review of the literature also revealed
nest predation is greater in less fre- that most species are specialized in
quently used nest sites,j and most their nesting ~ u b s t r a t e This
. ~ specialspecies were substrate specialists ization contrasts with foraging sites
(more than 6 0 % of nests in one sub- where species are much less special'See footnote 1.
September 1993
6T.E. Martin, 1993, manuscript in preparation.
ized and overlap more (Figure l a ) .
Specialization may also lead to stereotypy in nest placement. Nest heights
of 1 7 warbler species were compared
over latitudes differing by as much as
14", and only 4 species shifted heights
significantly despite geographic
changes in vegetation structure and
types of coexisting species (Martin
1 9 8 8 ~ )Moreover,
.
in many cases, all
or most bird species within a genus
use the same vegetation layer or general substrate type for nesting. Such
results suggest that nest placement
often is evolutionarily conservative.
Nest placement may be set for a
species over a large geographic area
based on events during speciation or
their evolutionary history. Stereotypy
in nest placement could result in poor
re~roductivesuccess in some habitats
and even select against occupation of
those habitats, potentially providing
a mechanism for favoring coexistence
of species that differ in nest placement. For example, hermit thrushes
are subject to more intense predation
than any other species on my study
sites in Arizona. This intensity of predation is closely related to the use of
small firs for nesting.
Given that nestinr! is so unsuccessful in small firs, i h y choose such
sites? Hermit thrushes may be immigrating t o my sites from other sites
where small firs are an appropriate
choice for nesting. Firs may elicit a
settling response when encountered
by dispersing birds, because firs are an
appropriate proximate cue over the
larger range of the population. Indeed. the race of hermit thrush that
occurs on my sites usually uses small
conifers for nesting throughout its
western range (Harrison 1979). Such
sites may be appropriate over most of
the range, but inappropriate on my
study areas.
My study sites are drainages that
are located within 8 km of the edge of
the Mogollon Rim, an abrupt cliff
that represents the southern extension
of the Colorado Plateau. The edge of
the rim has a narrow band of moist
vegetation (e.g., maple) associated
with greater precipitation formed by
the u ~ w a r ddeflection of air at the rim
face. My study sites are in this narrow
band of moist vegetation. Red squirrel distribution and densities are associated with maple on these sites (Uphoff 1990). Photos from automated
527
MacGillivray's warbler poses a
similar problem: Given that nesting
success is so much greater in maple
thickets (Figure 6), why use firs?
MacGillivray's warbler usually places
only approximately one third of nests
in small firs (Table 1). This use of
conifers again reflects a common pattern throughout their range.s However, small firs may be used when
short maple thickets are not available.
Many of the territories where small
firs are used have less short maple.9
Ma&~ll~vrays warbler
0.100.00..
0.06.0.04.0)
C
0.02-
.2
1
0.00-
E
om-
S
Herrntt thrush
.-%
--
--
-
--
W e s t e r n Foundation of Vertebrate Zoology,
1993, Los hngeles, C h , unpublished data.
ySee footnote 1.
0.05 Moreover, annual differences in
nest sites also suggest that availability
is important. In the four years before
1988 and 1989, maples were used for
approximately two thirds of the nests.
In 1988 and 1989, late freezes and a
drought, respectively, inhibited leaf
development in maples, and MacGillivray's warblers placed two thirds
of their nests in small firs (Table 1 ) .
The increased use of small firs by
MacGillivray's warblers in 1988 and
1989 was associated with significantly
greater nest predation in these two
years compared with the four previous years. Moreover, predation rates
were correlated with the proportion
-.-Few Many
Few Many
Potential
nest sites
Total stems
Figure 2. Daily mortality rate (rate at
which nests are lost to predators per day)
and its standard error for nests in patches
with less (few) or more (many) than the
median number of stems that represent
potential nest sites or total vegetation
(total stems). Z-values were calculated
using the z-test of Hensler and Nichols
(1981). For the MacGillivray's warbler,
62 nests were observed. For potential
nest sites, z = 2.5 (p = 0.006); for total
stems, z = 0.9 ( p = 0.19). For the hermit
thrush, 109 nests were observed. For
potential nest sites, z = 2.5, p = 0.006; for
total stems, z < 0, p > 0.5.
cameras at artificial nests showed that
red squirrels are the major predators
on nests and account for more than
80% of nest predation events (Martin
1988b).'Moreover, these maple habitats contain MacGillivray's warblers
and green-tailed towhees, both of
which use small firs as nest sites and
thereby overlap hermit thrushes and
increase the cumulative density of nests
in firs.
If the low nesting success of hermit
thrushes in maple drainages is due to
the high density of red squirrels and
high cumulative density of nests in
small firs, then nesting success should
be higher in the same nest sites (small
firs) in other habitat conditions without coexisting species. Indeed, success
of hermit thrush nests in small firs in
nearby drainages that d o not contain
maple or the other two coexisting
species was markedly higher than in
maple drainages (Figure 7).
--
'See footnote 1.
528
Case a
Case b
Figure 3. Schematic drawing of substrate and prey distribution for two experimental
nest treatments. In both cases, four types of nest sites are represented by four open
symbols. Four bird species are represented by four solid symbols. In the first treatment
(case a), each species occupies a different nest site. In the second treatment (case b),
density is the same as in case a, but all species occupy the same nest site. The result
is that cumulative density in a nest site (e.g., circles) is four times greater when species
use the same nest site (case b ) than when each species uses a different nest site (case
a). Note that almost all circles are occupied in case b, rewarding predators to continue
searching the substrate type but to ignore other substrate types because they are
empty. This situation increases predation rates on all species using the substrate type.
In contrast, in case a, the predator must search all substrates to encounter the same
number of prey, and the increased encounters with unoccupied sites may cause the
predator to give up before finding a prey, thereby reducing the cost of coexistence.
BioScience Vol. 43 No. 8
an influence on nest-site selection may
also indirectly affect other traits (e.g.,
life-history traits) that are affected by
nest sites (Martin 1988d).
Life-history traits
Maple
(1 m)
Ground Fir
Maple
(3m)
Nest position
Figure 4. Mean (and standard error) in
daily mortality rates (rate at which nests
are lost to predators per day) for artificial
nests when nests were placed among four
different types of sites (open bars, case a
of Figure 3 ) and when nests were all
placed in the same type of sites (striped
bars, case b of Figure 3). Density of nests
was held constant between the two treatments. A total of 480 nests were used
among three replicate sites and over two
temporal replicates. The situation of nests
placed in the same type of sites was not
tested for the 3-meter maple. Data from
Martin (1988b).
of nests placed in small firs by
MacGillivray's warblers among years.
Thus, availability of suitable nest sites
apparently can influence the success
of a population within a habitat by
influencing predation risk.
In summary, nest predation represents a potentially strong selection
pressure and forms a viable alternative hypothesis to food limitation and
competition for general patterns such
as the increase in numbers of species
with foliage density and dispersion,
differences in microhabitat use among
coexisting species, and differences in
nesting success of populations among
habitats. The role of nest predation as
Orange-crowned warbler
0Virginia's warbler
Q)
v,
2
Life-history studies represent one area
in which nest reda at ion has not been
totally ignored. Yet, food limitation is
still thought to be the most important
influence on life-history traits (Lack
1948, 1954, reviews in Martin 1987,
1992b)and, ironically, the most widely
touted example of nest predation effects (large clutch size of cavity-nesting birds) may be incorrect. The large
clutch sizes of cavity-nesting birds
compared with open-nesting birds
have long been considered a consequence of reduced nest predation o n
cavity nesters (Lack 1948,1954, Lima
1987, Slagsvold 1982). Nest predation is indeed generally less for cavitynesting than open-nesting birds (Martin and Li 1992; but see Nilsson 1986),
but nest ~ r e d a t i o nhas not been directly testkd as the cause of the clutch
size pattern. Here, I examine nest
predation and two other hypotheses.
Recent inters~ecificanalvses demonstrate that adult survival varies inversely with fecundity in both Europe
(Bennett and Harvey 1988, Szther
1988) and North America (Martin in
press a). This inverse relationship may
occur because fecundity derives from
adult mortality (e.g., Law 1979),
which allows one hypothesis for the
clutch size differences between cavity-nesting and open-nesting birds. The
winter mortality hypothesis states that
a greater proportion of cavity nesters
Red-faced warbler
Dark-eyed junco
0 %
E 0.5
3
u
2
U.
0.0
Firs
Maple
Locust
Nesting substrate
Open
Figure 5. Frequency that ground nests were placed below the indicated plant species
by the four ground-nesting species. Orange-crowned warbler (Vermivora celata; n =
90; black bars), Virginia's warbler (Vermivora virginiae; n = 27; open bars), red-faced
warbler (Cardellina rubrifrons; n = 30; shaded bar), and dark-eyed junco (Junco
hyemalis; n = 55; cross-hatched bar).
September 1993
Percentage of
nests built in
Year
Percentage of nests lost to
predation
Firs
Maple
1984
55
0.33
0.67
u
C
Q)
Table 1. Annual variation in nest predation as a function of variation in use of
nesting substrates by MacGillivray's warblers. The increased use of firs in 1988
and 1989 was associated with significantly greater nest predation than in the
previous four years (X2 = 6.95, p =
0.008, multiple comparison test of Sauer
and Williams 1989). Predation rates were
correlated with proportion of nests built
in firs (r = 0.89, p < 0.05).
than open nesters are residents, and
winter mortality is thought to be
greater for residents than migrants
(Greenberg 1980, von Haartman
1957,1968). Thus, larger clutch sizes
of cavity nesters may be a byproduct
of greater adult mortality caused by
residency habits.
Reproductive traits may not derive
from adult survival, however. Instead,
adult survival may derive from differences in reproductive output (Charnov
and Krebs 1974, Williams 1966), affecting two hypotheses. The nest predation hypothesis states that reduced
nest predation is thought t o allow
more young to be fed over a longer
nestling period (Lack 1948, 1954) or
more energy to be invested in a single
nesting attempt rather than several
(e.g., Slagsvold 1982). As a result,
reduced nest predation is thought to
favor larger clutch size (Lack 1948,
1954, Law 1979, Lima 1987, Slagsvold
1982), which should cause decreased
or no change in adult survival. The
limited breeding opportunities hypothesis states that when breeding opportunities are limited, birds should invest increased effort in reproduction
(i.e., large clutch size) at the cost of
reduced survival when they get a
chance to breed because they may not
get another chance (Martin 1992b, in
press b). Hence, cavity nesters whose
breeding opportunities are limited by
availability of nest holes should have
larger clutch sizes, causing lower survival, than open-nesting birds.
Greenberg (1980) concluded that
residents suffered higher adult mortality than migrants (represented by
529
Fir
Maple
Nest substrate type
Figure 6 . Daily mortality rates (and standard errors) for nests of MacGillivray's
warblers in small white firs and canyon
maple. Daily mortality rates were much
greater ( z = 2.85, p = 0.0022) for nests in
firs than for nests in maple. There were
30 nests in firs and 32 nests in maple.
the combined data in Figure 8). However, he confounded migrant classification and nest type. I reanalyzed the
data and separated nest type from
migration habits. Analysis of variance
showed that adult survival did not
differ between migrants and residents
within a nest type (i.e., open nesters;
Figure 8). O n the other hand, survival
differed between nest types (open nesters versus cavity nesters) within residents.
The same results are obtained when
based on a larger data set with even
finer division in migration habits (Figure 9); survival does not differ among
migration classifications within a nest
type, but it does differ between nest
types within a migration classification when body mass effects are controlled through two-factor analysis of
covariance.
The similar adult survival of residents and migrants when nest type is
controlled (i.e., within open nesters
and nonexcavators) falsifies the winter-mortality hypothesis, which predicts that residents suffer greater adult
mortality than migrants. Moreover,
not all resident cavitv nesters suffer
greater adult mortality than open nesters; resident cavity-nesting species that
excavate their own nest holes (excavators) have adult survival rates that
are greater (0.65 2 .028 [standard
error], n = 5 ) than for either resident
nonexcavators (species that do not
excavate but instead use existing holes)
or resident open nesters (Figure 9 )
with body mass controlled (ANCOVA,
F = 12.73, p < 0.0001).
The evidence also favors rejection
of the nest-predation hypothesis. Nest
530
mortality predictably averages much
,,,
less for excavators (13% of nests are
,
lost) than nonexcavators (36% loss;
5
Martin and Li 1992). Yet, excavators 7 0.55
have smaller clutches (Martin and Li 2
1992) and greater adult survival (Fig- - o.,5
ure 9) than nonexcavators, counter to 4
the nest-predation hypothesis, which a 0.35
predicts that excavators with reduced
Combined
Open
Cavity
nest predation should have larger
Nest type
clutch size and lower or similar adult
survival c o m p a r e d w i t h nonex- Figure 8. Annual adult survival for resicavators. Moreover, analysis of life- dent (open bars) versus migrant birds
history traits for 110 species of North (shaded bars) when nest type is combined
American birds shows that clutch sizes or separated. Data are from Greenberg
of nonexcavators are outliers for their (1980). Numbers in parentheses reprenest predation rates (Martin in press sent numbers of species. Midpoints were
used for data presented with ranges. Cava). Such results indicate that the large
"
clutch sizes of nonexcavating cavity ity nesters include only species that do
not excavate their own cavities. Data for
nesters cannot be explained by the blue tit (Parus caeruleus) on Canary Isnest predation hypothesis. Plus, the land were excluded because island DODUpatterns are not explained by phylo- lations are known to exhibit higher surgenetic effects (Martin in press b, vival than mainland populations. Data
Martin and Li 1992).
for brown-headed cowbird (Molothrus
The data are consistent with the ater) also were excluded because this
limited-breeding-opportunities hy- species lays its eggs in the nests of other
pothesis. Nest sites are much more species. Analysis of variance showed that
limited for cavity-nesting birds that adult survival did not differ (F = 0.98,
L
L p > 0.10) between migrants and residents
within a nest type (i.e., open nesters). On
the other hand, survival differed (F =
13.14, p = 0.002) between nest types
(open nesters versus cavity nesters) within
residents.an influence on nest-site selection may also indirectly affect other traits
(e.g., life-history traits) that are affected
by nest sites (Martin 1988d).
depend on finding an existing hole
(nonexcavators) than for open nesters
Maple
Maple
Nonmaple
(Martin and Li 1992, von Haartman
(1989, 1991) (1989, 1991)
(All years)
1957,1968), and nonexcavators have
Drainage type
larger clutches and lower adult surFigure 7. Nesting success of hermit vival than open nesters, as predicted
thrushes in maple drainages pooled across by the limited-breeding-opportunities
eight years (1984-1991) and in two years hypothesis. In addition, nest sites are
(1989, 1991) when both maple and also more limited for nonexcavators
nonmaple drainages were studied. Maple than excavators, because excavators
drainages are the snow-melt drainages
can create their own cavities (Westhat have been the focus of my studies in
Arizona. Nonmaple drainages are nearby olowski 1983)andnonexcavators have
drainages that have small firs but do not larger clutches and lower adult surcontain maple. Total nesting success (per- vival than excavators, again as precentage of nests that fledge at least one dicted by the hypothesis. Thus, comyoung) was 8.0% (out of 195 nests) for p a r i s o n of a d u l t m o r t a l i t y for
maple drainages in 1984-1991; 8.7% nonexcavators versus both open nest(out of 103 nests) for maple drainages in ers and excavators supports the lim1989 and 1991; and 38.9% (out of 1 7 ited-breeding-opportunities hypothnests) for nonmaple drainages in 1989 esis and rejects the two alternative
and 1991. The success of nests in
hypotheses.
nonmaples drainages was markedly higher
Excavators as a group provide adthan in maple drainages either in the
ditional
support for the hypothesis.
same study years (X2= 10.9, p = 0.001) or
compared to nest success pooled across Excavators vary in their abilities to
excavate holes because of morphoyears (X2= 15.2, p = 0.0001).
BioScience Vol. 43 No. 8
logical differences, and species with
weaker excavating morphology depend on existing holes more; such
species potentially are more limited in
their nesting opportunities, and clutch
sizes increase with this dependence on
existing holes as expected under the
limited-breeding-opportunities hypothesis (Martin in press b). Moreover, excavators that use old holes
apparently suffer greater nest predation (Nilsson et al. 1989j, and, hence,
the larger clutch sizes of these species
is further evidence against the traditional nest predation hypothesis. Predation may contribute to clutch size
differences indirectly by influencing
nest site preferences, nest size, or number of broods (Lima 1987, Martin
1988d, in press a, Martin and Li 1992,
Moller 1987, 1989, Slagsvold 1982).
However, nest site attributes apparently are more important to differences in clutch size and adult survival
among cavity-nesting bird species than
are differences in nest predation or
food limitation (Martin and Li 1992,
Martin in Dress bj.
These risults emphasize the importance of examining new hypotheses
rather than blindly accepting longstanding dogmas. Indeed, although
nest predation appears t o be less important to life histories of cavity-nesting birds, nest predation apparently
influences life-history traits among
many groups of birds for which food
limitation traditionally has been considered to be more important (Kulesza
1990, Martin 1993, in press a).
Conservation implications
The pervasive nature of nest predation and the influence of nest sites on
oredation risk indicates that nest sites
are important habitat components and
that the nesting season can be a critical veriod for maintenance of bird
populations. Conservation of species
depends on knowing their breeding
biology and identifying and preserving the habitat features that affect
breeding productivity and survival
(Martin 1992a). Yet, insufficient information is available for most suecies with regard to their habitat neehs,
reproduction, and survival.
Nest predation has gained considerable attention in conservation studies because nest predation can increase with fragmentation (e.g.,
u
September 1993
nest site preferences, and these preferences may be fixed. Habitat fragAll estimation methods
mentation can cause direct loss of
O.=T
habitat features needed by some species and thereby cause loss of those
species (Martin 1992a).
Even in large forest tracts without
edge problems, alteration of conditions by grazing, lumber production,
or other anthropogenic activities can
potentially cause loss of necessary
habitat conditions for some species.
m, esf
Jolly-Seber methods
Moreover, habitat degradation may
reduce the diversity of nesting sites
available and cause increased predation on species that still use such habitats because they are forced to use
similar (overlapping) nest sites and
increase cumulative nest density, or
because species are forced to use poorquality nest sites.
Residents
SD
LD
migrants migrants
Such effects added to increased predation
along edges (Wilcove 1985)
Figure 9. Annual survival rate for North
American bird species separated by mi- may cause many populations to regration habits and nest type (open nests, produce well below levels necessary
open bars; cavity nests, shaded bars). for maintaining populations. Indeed,
Numbers in parentheses are numbers of a number of bird species are showing
species. Data are from Martin and Li alarming population declines (Robbins
(1991). Cavity nesters include only et al. 1989). Correction of such popunonexcavators. Four methods of estimat- lation problems will depend on detering adult survival, all based on recapture1 mining the habitat features that allow
recovery, were used by the studies. The successful reproduction by a variety
Jolly-Seber method is the most rigorous
estimation method; it is separated to test of species on their breeding grounds,
any potential bias due to differences In as well as habitats needed for survival
estimation methods. The patterns for the on the wintering grounds. Given the
Jolly-Seber estimates are identical to the importance of nest predation and nest
patterns for all methods combined. Sur- sites to nest success, much greater
vival does not differ among migration attention is needed for these issues,
2
V)
-
classifications within a nest type (F =
0.72, p > 0.10) but does differ between
nest types within a migration classification (F = 15.32, p c 0,0001) when body
mass effects are controlled through twofactor analysis of covariance.
Wilcove 1985) and potentially cause
loss of species (local extinction) from
fragments. Such effects have been considered primarily in terms of the increase in predators along edges of
habitat fragments (Wilcove 1985 and
many others). Yet, nest predation cannot fully explain losses of species from
fragments (see Martin 1992a), and
some assumptions regarding vulnerability of species t o nest predation are
incorrect (Martin 1993j.
Other ecological requirements of
species are undoubtedly important to
their loss. For example, the arguments
and evidence presented here suggest
that species commonly differ in their
Acknowledgments
I appreciate comments and thoughts
on this manuscript by E. Bokman, W.
Etges, S. Foster, S. Garner, R. L. Hutto,
M. Newton, L. Petit, and anonymous
reviewers. I thank a large number of
field assistants for help in finding and
monitoring nests. I thank the Blue
Ridge Ranger Station of the US Forest
Service for their support and permission to work on their forest. My work
has been supported by grants from the
National Science Foundation (BSR8614598 and BSR-906320).
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BioScience Vol. 43 No. 8
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Nest Predation and Nest Sites
Thomas E. Martin
BioScience, Vol. 43, No. 8. (Sep., 1993), pp. 523-532.
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G. E. Hutchinson
The American Naturalist, Vol. 93, No. 870. (May - Jun., 1959), pp. 145-159.
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On the Advantage of Being Different: Nest Predation and the Coexistence of Bird Species
Thomas E. Martin
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Nest Predation Among Vegetation Layers and Habitat Types: Revising the Dogmas
Thomas E. Martin
The American Naturalist, Vol. 141, No. 6. (Jun., 1993), pp. 897-913.
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Evolutionary Determinants of Clutch Size in Cavity-Nesting Birds: Nest Predation or Limited
Breeding Opportunities?
Thomas E. Martin
The American Naturalist, Vol. 142, No. 6. (Dec., 1993), pp. 937-946.
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Life History Traits of Open- vs. Cavity-Nesting Birds
Thomas E. Martin; Pingjun Li
Ecology, Vol. 73, No. 2. (Apr., 1992), pp. 579-592.
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Nest Predation and Nest-Site Selection of a Western Population of the Hermit Thrush
Thomas E. Martin; James J. Roper
The Condor, Vol. 90, No. 1. (Feb., 1988), pp. 51-57.
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Sources, Sinks, and Population Regulation
H. Ronald Pulliam
The American Naturalist, Vol. 132, No. 5. (Nov., 1988), pp. 652-661.
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Population Declines in North American Birds that Migrate to the Neotropics
Chandler S. Robbins; John R. Sauer; Russell S. Greenberg; Sam Droege
Proceedings of the National Academy of Sciences of the United States of America, Vol. 86, No. 19.
(Oct. 1, 1989), pp. 7658-7662.
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Resource Partitioning in Ecological Communities
Thomas W. Schoener
Science, New Series, Vol. 185, No. 4145. (Jul. 5, 1974), pp. 27-39.
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Predation, Competition, and Prey Communities: A Review of Field Experiments
Andrew Sih; Philip Crowley; Mark McPeek; James Petranka; Kevin Strohmeier
Annual Review of Ecology and Systematics, Vol. 16. (1985), pp. 269-311.
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Adaptation in Hole-Nesting Birds
Lars von Haartman
Evolution, Vol. 11, No. 3. (Sep., 1957), pp. 339-347.
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Ontogenetic Habitat Shifts in Bluegill: The Foraging Rate-Predation Risk Trade-off
Earl E. Werner; Donald J. Hall
Ecology, Vol. 69, No. 5. (Oct., 1988), pp. 1352-1366.
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Nest Predation in Forest Tracts and the Decline of Migratory Songbirds
David S. Wilcove
Ecology, Vol. 66, No. 4. (Aug., 1985), pp. 1211-1214.
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Natural Selection, the Costs of Reproduction, and a Refinement of Lack's Principle
George C. Williams
The American Naturalist, Vol. 100, No. 916. (Nov. - Dec., 1966), pp. 687-690.
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Avian Community Organization and Habitat Structure
Mary F. Willson
Ecology, Vol. 55, No. 5. (Late Summer, 1974), pp. 1017-1029.
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