On the Advantage of Being Different: Nest Predation and the Coexistence of Bird Species
Thomas E. Martin
PNAS 1988;85;2196-2199
doi:10.1073/pnas.85.7.2196
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Proc. Nati. Acad. Sci. USA
Vol. 85, pp. 21%-2199, April 1988
Ecology
On the advantage of being different: Nest predation and the
coexistence of bird species
(community structure/density-dependent predation/resource partitioning/search images)
THOMAS E. MARTIN
Department of Zoology, Arizona State University, Tempe, AZ 85287-1501
Communicated by Jared M. Diamond, December 23, 1987
tors will increase for individual species with the cumulative
density of all similar species (ref. 17; also see refs. 23 and 24).
Thus, such behavioral responses by the predators, if they
exist, can favor coexistence of species that use different
nesting sites (partitioning of resources, where nest sites are
the resource) to minimize cumulative density effects (17).
Here, I report experiments that support the premise that
predator search intensity increases with the frequency of
occupied nest sites (reward rate). I then show that, for a
given density of nests, nest predation is reduced when those
nests are placed in sites that differ (partitioned nesting space)
than when placed in similar sites (unpartitioned space).
A long-standing debate in ecology centers on
ABSTRACT
identifying the processes that determine which species coexist
in a local community. Partitioning of resources, where species
differ in resource use, is often thought to reflect the primary
role of competition in determining coexistence of species. However, in theory predation can favor similar patterns. This
theory premises that predators increase their search intensity
with increasing density of prey. One set of experiments reported
here supports this premise based on predators that search for
bird nests. A second set of experiments documents that preda.
tion rates are lower when nest sites are partitioned among
different sites than when the same number of nests are placed in
similar sites. Moreover, predation rates on experimental nests
are more similar to rates on real nests when experimental nests
are partitioned among different sites. These results provide
support for a hypothesis that nest predation is a process that can
favor coexistence of bird species that partition resources, where
nest sites are the resources.
STUDY AREA AND METHODS
Study Area. Experiments were conducted in four mixedconifer drainages in central Arizona at -2300-m elevation.
These drainages were of the same vegetation type and
general location as other sites on which I have been studying
nest predation (25, 26). Nest predators were identified using
cameras outfitted with infrared light beams that trigger the
camera when the beam is broken. Ten cameras were set up
at artificial nests that were in the same drainages as experimental nests but which were not included in the results
presented here. Preliminary results based on 11 pictures
indicated that the nest predators were red squirrels (Tamiasciurus hudsonicus) and gray-neck chipmunks (Tamias cinereicollis). These results coincide with my impressions on
these sites from observations of birds chasing these two
predators. However, other predators are also on the sites
[e.g., long-tailed weasels (Mustelafrenata) and Steller's jays
(Cyanocitta stelleri)] and undoubtedly account for some nest
losses.
Experiments used artificial wicker nests baited with quail
(Coturnix coturnix) eggs. Artificial nests have been successfully used in other studies to examine predation rates (27,
28). Moreover, I previously tested potential biases associated with using artificial nests in the habitats studied here
and found that nests that simulate the appearance and
position of real nests can elicit predation responses that
reflect real trends (29).
Experiment 1. This experiment tested the response of
predators to reward frequency by modifying the frequency
of egg-occupied nests in three treatments. In all treatments a
constant number of nests (seven) was placed in small white
firs (Abies concolor) in 10-m-diameter circles (referred to as
clumps). Ten clumps were used in each treatment and placed
about 25 m apart. Treatments were separated by 100 m. One,
three, and all seven nests in each clump contained eggs in
treatments one, two, and three, respectively. Thus, this design used 70 nests per treatment with 10, 30, and 70 nests
containing eggs in treatments one, two, and three, respectively.
Experiment 2. This experiment tested the effect of nest
space partitioning on predation rates. Four species were
simulated. One nest type simulated an orange-crowned
warbler (Vermivora celata) and was placed in a small de-
Local processes determine the number and types of species
that coexist in a local'community, within regional and historical constraints on availability of species (1). Competition is
an example of a local process. In fact, resource partitioningi.e., differences among coexisting species in their use of
resources-is commonly observed and often thought to reflect the primary role of competition in determining coexistence of species (2-5). However, the importance of competition has been hotly debated, creating a need to examine
alternative processes (6-9). Predation is an alternative process that can affect coexistence of species by mediating competitive interactions or by eliminating species (10-14). More
importantly, theory suggests that predation can also favor
resource partitioning similar to competition (15-17). Thus,
this theory provides an alternative explanation for a common
pattern (i.e., resource partitioning). Here, I test whether nest
predators exhibit the behaviors that can favor resource partitioning among coexisting bird species.
Nest predation is probably an important agent of natural
selection for birds because such predation commonly is a
primary limit on reproductive succes's (18). However, the
effect of predators depends on their searching behavior (17).
Predators, in searching for bird nests, must examine some
potential nest sites that are not occupied by eggs (no
reward). Increased reward frequency should reinforce
search behavior. Consequently, both search intensity and
the proportion of nests lost to predators should increase with
the frequency or density of occupied nest sites (reward rate).
Moreover, predators can enhance their search efficiency by
specializing on prey types and learning search images
(19-22). If predators do not discriminate among species with
similar nest sites, then the proportion of nests lost to predaThe publication costs of this article were defrayed in part by page charge
payment. This article must therefore be hereby marked "advertisement"
in accordance with 18 U.S.C. §1734 solely to indicate this fact.
2196
Proc. Natl. Acad. Sci. USA 85 (1988)
Ecology: Martin
pression in the ground under the stem of a deciduous shrub
(usually big-toothed maple-Acer grandidentatum) (termed
ground species). The second nest type simulated a hermit
thrush (Catharus guttatus); it was covered with moss and
placed about 1 m above ground in a small white fir (termed
fir species). The third type was unmodified and placed 1 m
above ground in maple [termed maple (1m) species], simulating a MacGillivray's warbler (Oporornis tolmiei). The
fourth type was placed 3 m above ground in maple [termed
maple (3m) species] simulating a black-headed grosbeak
(Pheucticus melanocephalus).
Nests were placed at =10-m intervals along two parallel
transects (long continuous strips of sample area) that were a
minimum of 25 m apart; exact distance between transects
and among nests on a transect varied depending on the
availability of a suitable nest site. The same spacing was
used in both of two treatments (to be described) to maintain
constant density between treatments. Both treatments were
included in each of three spatial replicates. Treatments were
separated by 100 m in each replicate, and spatial replicates
were separated by 3-5 km. Experiments in all three spatial
replicates were initiated at the end of May when egg-laying
activity peaks. The experiments were then repeated in late
June when many birds were renesting. This design used 80
nests per spatial replicate (40/treatment) or 240 nests per
temporal replicate, with 480 nests used overall.
Treatment one simulated a four-species assemblage (partitioned nesting sites). The four nest types were alternated
sequentially along the two transects in each replicate, using
40 nests per replicate. Treatment two simulated a singlespecies assemblage (unpartitioned sites); 20 nests of one
species were placed along the transects followed by a 100-m
buffer and then a second set of 20 nests of a different species
for a total of 40 nests in this treatment. This design, which
only tested two single species per temporal replicate, was
used to maintain constant sample size (40 nests) between
treatments and because of time and space constraints on
putting out additional nests. The ground species was tested
in both temporal replicates to test for any temporal biases.
The other single species tested in the first and second
temporal replicates were the fir and maple (1m) species,
respectively. Thus, three of the four species were tested as
2197
-J
0
6
12
9
15
DAYS EXPOSED
FIG. 1. Predation rate as a function of the ratio of egg-occupied
nests to total nests in a clump. The three treatments include one,
three, and seven nests containing eggs in each clump. (a) Percentage
of clumps remaining without any nests in the clump losing eggs to
predators. (b) Percentage of intact nests remaining (no egg loss to
predators).
arguably reflect an increasing probability of random encounacross treatments. However, the risk to individual nests is shown by the percentage of intact nests (no
egg loss) that were remaining at each nest check; the results
show that even individual nests had a greater rate of predation (F = 6.08, P < 0.02) with increases in reward frequency
(Fig. lb).
Experiment 2. Predation rates were greater (F = 515.89, P
< 0.03) in the single-species treatment across all spatial and
temporal replicates (Fig. 2). The higher predation rates could
ters of nests
Temporal Replicate 1
Temporal Replicate 2
0-O Multiple species
1 00*@-4 Single species
z
0
single species.
Statistical Tests. Predation rates on artificial nests were
measured by examining loss of eggs from nests every 3 days
during 15 days of exposure to predators. Differences among
treatments were examined by comparing the percentage of
nests remaining without having lost any eggs to predators.
These data were arcsine-transformed and analyzed by one-,
two-, or three-way, repeated measures, analysis of variance
(ANOVA). One-way analyses were used for the first experiment. Two-way analyses were used in the second experiment for those comparisons that did not include temporal
replications. Otherwise, three-way analyses were used.
Two- and three-way interactions with treatment effects were
not significant (P > 0.10 in all cases).
Predation rates on real nests of the four species being
simulated were measured by examining loss of eggs every
3-4 days and using the Mayfield method, which measures
the proportion of nests that are lost to predators per day (30,
31). Differences in these daily mortality rates between artificial and real nests were tested with the z test (31).
0~
0
m
z
z
Lii
z
LAO
w
0( 0
io10
W
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-
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RESULTS
Experiment 1. Predation rates increased (F - 10.07, P <
0.01) with increased reward frequency when based on the
percentage of clumps remaining without any nests losing
eggs to predators (Fig. la). Given that the number of nests at
risk increased across treatments, then such results may
3
6 9 12 15 0 3 6 9 12
DAYS EXPOSED TO PREDATORS
1
FIG. 2. Percentage of nests that lose no eggs to predators. Each
column is a temporal replicate, and each row is a spatial replicate.
The multiple species treatment represents the combined predation
rate for four species; the single-species treatment combines two sets
of single species in each temporal replicate.
2198
Ecology: Martin
z
0
Proc. Natl. Acad. Sci. USA 85 (1988)
a
Ground Species
1 00t
Temporal Replicate 1
0--O Multiple species
b
Fir Species
Temporal Replicate 1
1 0op-
Multiple species
Maple (1 m) Species
Temporal Replicate 2
-@ Single species
!R
0
w
0A
0-0-
0-I
0
3:
Iz
z
801 0K
601 \
w
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20
IC)
--
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w
z
. =-
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00.~
0
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ol
z
w
4
w
2
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ol
0 1-.~
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EL
3
3
6 9 12 15
6 9 12 15
DAYS EXPOSED TO PREDATORS
3
6 9 12 15 0 3 6 9 12 15
DAYS EXPOSED TO PREDATORS
FIG. 3. Percentage of nests that lose no eggs to predators. Each column is a temporal replicate, and each row is a spatial replicate. (a) Data
in each treatment are based only on the nests that simulated the ground species in all spatial and temporal replicates. (b) Data from both
treatments are based only on the nests that simulated the fir species for the first temporal replicate and the maple (im) species for the second
temporal replicate.
have occurred because the species used in this treatment have
containing eggs. These results complement other data showgenerally higher predation rates than those in the multipleing that predation rates on real hermit thrush nests are lower
species sample; this hypothesis is unlikely because three of
when greater numbers of white firs (unoccupied potential
the four species were tested in the single-species treatment.
nest sites) surround the nests (26). Thus, data from both real
However, comparison of predation rates for the individual
and artificial nests support the premise that predators modify
species used in both treatments allows direct examination of
their search behavior in response to the frequency of occuthis potential bias. Such comparisons show that predation
pied nests that they encounter.
rates are unequivocally greater in the single-species treatment
The second set of experiments documents that predators
(Fig. 3); predation rates were higher (F = 30.06, P < 0.04) for
can exhibit the behaviors necessary to favor partitioning of
the ground-nesting species in both temporal replicates (Fig.
nesting space; predation rates were reduced when nests
3a) and for the fir species (F = 52.43, P < 0.02) and maple
were partitioned among different sites. These results do not
=
<
(im) species (F 18.83, P 0.05) in temporal replicates 1
seem to be an abnormal response of predators to artificially
and 2, respectively (Fig. 3b). Moreover, predation rates in the
nest densities given that predation rates in the multiplehigh
multiple-species treatment were much more similar to predaspecies treatment were similar to predation rates on real
tion rates on real nests than in the single-species treatment
nests (Table 1). The lower predation rates in the multiple(Table 1). Predation rates can differ among years (unpubspecies treatment as compared with single-species treatment
lished data), but such fluctuations should not influence the
may arise because the four nest types were so different that
general pattern documented here because the results are
different predator species specialized on each nest type; these
based on controlled treatments.
predators may then have simply responded to the different
DISCUSSION
densities of individual nest types in the two treatments.
Photographs of predators at the two nest types (fir and
The first experiment documents that predators can increase
ground) monitored with cameras suggest this to be an unlikely
their searching intensity with increasing frequency of nests
Table 1. Mean ± variance in predation rates, measured as daily mortality rates, for the artificial
nests in the multiple- and single-species treatments and for real nests of the four species
simulated in the treatments
Daily mortality rate, nests lost to predators per da-y
Multiple-species
Single-species
treatment
Real nests
0.210 ± 0.0004
0.027 ± 0.0002 (17)t
**
0.168 ± 0.0004
0.047 ± 0.0002 (22)
**
0.154 ± 0.0004
0.081 ± 0.0005 (19)
*
0.012 ± 0.0001 (8)
only on nests monitored during the same season as
experiments (1987) and only during the egg stage. *, P < 0.02 and **, P < 0.001 in comparisons
between adjacent numbers.
tSample size in parentheses, which equals the number of nests observed.
treatment
0.075 ± 0.0001
*
Ground
0.050 ± 0.0001
Maple (im)
0.068 ± 0.0001
Fir
0.035 ± 0.0001
Maple (3m)
Predation rates on real nests are based
Ecology: Martin
explanation; both red squirrels and chipmunks were detected
taking eggs at both nest types (unpublished data). In addition,
observations suggest that these same predators also take eggs
from the other two nest types (personal observation). The
lower predation rate in the multiple-species treatment may
instead occur because multiple prey types inhibit development of search images and thereby reduce foraging efficiency
(17, 21, 22). Separation of these two possibilites will require
more photographic data and additional experiments. Nonetheless, these experimental results show that there can indeed
be an advantage to being different; nest predation is significantly reduced when nest sites differ.
The two major predator species, or their sibling species,
are widespread throughout forested North America (32),
providing a basis for expecting the behavior documented
here to be widespread. Moreover, because nest predation is
commonly the primary source of nesting failure in avian
systems (18), the predation behavior documented here may
represent a process that commonly favors coexistence of
species that partition nesting sites. Some evidence does
indeed indicate that partitioning of nesting space may be
common (17). Such patterns are supported by analogous
arguments and evidence that predation may favor coexistence of species that differ in appearances or escape behaviors (23, 24).
Other processes clearly may be acting concurrently with
predation, and the relative importance of these processes
will vary over time and among habitats and areas. However,
the results documented here suggest that predation may
provide an alternative explanation for some patterns of
resource partitioning. Moreover, previous work on predation has focused on the loss of independent juveniles and/or
adults, even though reproductive success is an important
component of fitness. This study emphasizes that predation
on eggs and dependent young can constitute another important level of selection. These points are underscored by
demonstrating them on birds because predation effects have
been ignored in birds more than any other taxonomic group
(11). Indeed, studies of birds provided much of the original
impetus for the long-held view that resource partitioning
induced by competition was a primary and widespread cause
of species coexistence. Finally, some data show that birds
are relatively invariant in their nesting heights among geographic regions (17). This evidence indicates that nest site
differences among coexisting species do not necessarily
reflect local coevolution. Instead, the differences may reflect
selection for coexistence of species with nest sites that
Proc. Natl. Acad. Sci. USA 85 (1988)
2199
already differ due to differences in their individual evolutionary histories (17). Such effects emphasize the importance of
considering historical and regional processes in the structuring of communities (1, 17).
I thank J. Connell, J. Diamond, D. Levey, M. Douglas, T. A.
Markow, M. A. Newton, R. E. Ricklefs, J. J. Roper, T. W.
Schoener, and D. Simberloff for helpful comments on earlier drafts.
K. Donohue, M. Godwin, T. McCarthey, and J. Soliday provided
able assistance in putting out and monitoring the artificial nests. This
work was supported by Whitehall Foundation, Inc., and National
Science Foundation (BSR-8614598).
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