Global Change Biology (2013) 19, 411–419, doi: 10.1111/gcb.12062
Climate change has indirect effects on resource use and
overlap among coexisting bird species with negative
consequences for their reproductive success
S O N Y A K . A U E R * and T H O M A S E . M A R T I N †
*Montana Cooperative Wildlife Research Unit, 205 Natural Science, University of Montana, Missoula, MT 59812, USA,
†U.S. Geological Survey, Montana Cooperative Wildlife Research Unit, 205 Natural Science, University of Montana, Missoula,
MT 59812, USA
Abstract
Climate change can modify ecological interactions, but whether it can have cascading effects throughout ecological
networks of multiple interacting species remains poorly studied. Climate-driven alterations in the intensity of plant–
herbivore interactions may have particularly profound effects on the larger community because plants provide habitat for a wide diversity of organisms. Here we show that changes in vegetation over the last 21 years, due to climate
effects on plant–herbivore interactions, have consequences for songbird nest site overlap and breeding success.
Browsing-induced reductions in the availability of preferred nesting sites for two of three ground nesting songbirds
led to increasing overlap in nest site characteristics among all three bird species with increasingly negative consequences for reproductive success over the long term. These results demonstrate that changes in the vegetation
community from effects of climate change on plant–herbivore interactions can cause subtle shifts in ecological
interactions that have critical demographic ramifications for other species in the larger community.
Keywords: climate change, habitat selection, nest predation, plant populations, trophic interactions, ungulate browsing
Received 7 August 2012 and accepted 1 October 2012
Introduction
With the earth’s climate changing at a rapid rate (Kerr,
2004; Meehl et al., 2007; Loarie et al., 2009), ecologists
face the challenging task of understanding species’
responses to shifting environments and their demographic consequences. Species within a community can
differ widely in how they respond to climate change
(e.g., shifts in phenology or spatial distribution), the
rate at which they respond, and to which aspects of climate they are most sensitive (Visser & Holleman, 2001;
Voigt et al., 2003; Le Roux & McGeoch, 2008). Climate
may also have cascading effects within ecological networks of multiple interacting species through alteration
of interactions (Post, 2013), but the potential for climate
change to have such indirect effects remains poorly
studied (Zarnetske et al., 2012).
Climate-driven alterations in the intensity of plant
–herbivore interactions may have particularly far reaching effects on the larger community because plants
provide habitat for a wide diversity of organisms (Martin
& Maron, 2012). Heterogeneity in plant community
Correspondence: Sonya K. Auer, Department of Environmental
Conservation, University of Massachusetts, 201 Holdsworth Hall,
160 Holdsworth Way, Amherst, MA 01003, USA, tel. + (949) 680
0208, fax + (413) 545-4358, e-mail: myioborus@yahoo.com
© 2012 Blackwell Publishing Ltd
structure and function on local and regional scales allows
animal species to avoid competition and predation by
partitioning niche space and thereby facilitates the coexistence of multiple species (Martin, 1988; Tews et al., 2004).
However, recent studies demonstrate that climate change
can lead to an increase in herbivory and a concomitant
decline in plant diversity and abundance (Roy et al.,
2004; Tylianakis et al., 2008; O’Connor, 2009; Wookey
et al., 2009; Massad & Dyer, 2010; Li et al., 2011; Brodie
et al., 2012). These changes in the plant community may
decrease opportunities to partition niche space and
thereby lead to increased overlap in resource use among
coexisting species. Increased overlap may then have
negative consequences for the persistence of populations,
biodiversity, community stability, and ecosystem functioning and services (Worm et al., 2006; Mooney et al., 2009;
Wardle et al., 2011). However, impacts of climate-driven
changes in plant–herbivore interactions on resource
partitioning of coexisting species are not yet known.
We investigated whether climate change intensification of herbivore impacts on a high-elevation plant
community in north-central Arizona, USA, over the last
21 years has affected nest site overlap and breeding
success in three ground-nesting songbirds–Orangecrowned Warbler (Oreothlypis celata), Virginia’s Warbler
(Oreothlypis virginiae), and Red-faced Warbler (Cardellina
rubrifrons). As temperatures have increased, snowpack
411
412 S . K . A U E R & T . E . M A R T I N
levels have decreased over time in this high-elevation
site (Martin & Maron, 2012). In turn, elk (Cervis canadensis), the dominant herbivore in the system, that previously migrated to lower elevations when deep snow
levels precluded access to forage and increased the energetic cost of movement, are now more frequently opting
to remain at these high-elevation sites during the winter
(Sweeney & Steinhoff, 1976; Brown, 1994). Increased
browsing pressure has subsequently impacted the
recruitment of woody plants and led to precipitous
declines in the abundance of deciduous tree species in
this and other areas (Martin, 2007; Brodie et al., 2012;
Martin & Maron, 2012). Bird abundance has also
declined over time in parallel with these changes in the
plant community (Martin, 2007; Martin & Maron, 2012).
Declines in the abundance of deciduous tree species
may impact nest site choice and nesting success in multiple different ways. The three warblers previously partitioned their nest sites among patches dominated by
different woody plant species (Martin, 1998). Both
observational and experimental studies show that partitioning of nest sites reduces risk of nest predation, the
primary source of nest mortality, in this (Martin, 1996,
1998) and other systems (e.g., Hoi & Winkler, 1994;
Schmidt & Whelan, 1998). Thus, the decline in deciduous trees may reduce the availability of preferred nest
sites, force the three species to select increasingly similar sites, and thereby suffer increased nest predation
and reduced reproductive success. Alternatively, if the
decline in the density of breeding birds and their nests
causes predators to shift focus to other, more abundant,
prey types (Martin, 1996), then the decline in deciduous
trees may lead to increased overlap in nest site use, but
have no consequence for nesting success. Third, overlap in nest site use may not increase at all as the total
abundance of the three bird species and thus their
demand for preferred nest sites is declining over time.
Finally, changes in the total stem densities or the vegetation composition at nest sites of the three bird species,
rather than overlap per se, may increase rates of nest
predation if they increase the visibility of nests to predators or lead to detrimental changes in abiotic factors
such as microclimate. We evaluated these alternate
hypotheses by measuring temporal changes in the
availability of preferred nest sites, changes in nest site
choice, and the consequences of nest site choice for nest
site overlap and breeding success.
Materials and methods
Arizona. The vegetation in these shallow drainages is characterized by a mix of deciduous and coniferous tree species–
namely canyon maple (Acer grandidentatum), quaking aspen
(Populus tremuloides), New Mexican locust (Robinia neomexicana), Gambel’s oak (Quercus gambellii), white fir (Abies concolor),
and Douglas fir (Pseudotsuga menziesii)–that are segregated
along a distinct microclimate gradient from the wetter, cooler
drainage bottoms up to the drier, warmer ridges (Martin,
1998). Maples and aspens are found primarily at the bottom of
the drainages, whereas locust and oak are typically more
abundant higher on the slopes (Martin, 1998). These drainages
stand in contrast to the surrounding drier forest dominated by
an open canopy of ponderosa pine (Pinus ponderosa) and white
pine (Pinus strobiformis) with Gambel’s oak in the subcanopy.
Stellar’s Jays (Cyanocitta stelleri) and House Wrens (Troglodytes
aedon) are the primary avian nest predators, whereas mammalian predators include red squirrels (Tamiasciurus hudsonicus),
gray-necked chipmunks (Eutamias cinereicollis), and long-tailed
weasels (Mustela frenata).
Bird species
Orange-crowned, Virginia’s and Red-faced Warblers are
ecologically similar, closely related passerines in the wood
warbler family Parulidae. They nest on the ground, usually at
the base of a small sapling, and select and defend overlapping
territories that span the entire microclimate gradient in these
drainages. Past studies show that the three species partitioned
their use of nest sites by nesting in patches dominated by different woody plant species: Orange-crowned Warbler showed
a strong preference for sites dominated by maple whereas
Virginia’s Warbler and Red-faced Warbler preferred sites that
were dominated by locust and fir, respectively, but also
included maple (Martin, 1998).
Vegetation sampling
We measured the densities of the dominant woody plant species at stratified random sites and at nest sites each year from
1989 to 2009 to determine how the availability of nest sites and
nest site selection of the three bird species changed through
time. Due to a lapse in funding, data were not collected in
1990. Stratified random sites were selected at three positions
along the slope (bottom, middle, and upper third) and every
50 m down the length of each drainage. The specific locations
of these sites within the bottom, middle, and upper third of
the slopes were selected at random (Martin, 1998). Plant densities at nest sites were measured in a sampling plot centered on
the nest. At both random and nest sites, trees were counted
within a 5-m radius circular plot and separately by species
and size classes: diameter at breast height < 2.5 cm, 2.5–8 cm,
8–23 cm, and >23 cm. Small conifers were grouped by height
classes: <1 m, 1–3 m, and 3–5 m tall (Martin, 1998).
Study area
Nest searching and monitoring
Study sites were 20 high-elevation (~2400 m above sea level)
snow melt drainages along the Mogollon Rim of central
We searched the study drainages for nests of the three bird
species each year from 1989 to 2009 (with the exception of
© 2012 Blackwell Publishing Ltd, Global Change Biology, 19, 411–419
C L I M A T E C H A N G E E F F E C T S O N R E S O U R C E O V E R L A P 413
1990) and located nests using adult behavioral cues, as
described by Martin and Geupel (1993). Once located, nests
were monitored every 3–4 days until offspring fledged or
were depredated. Nests were considered successful if they
fledged at least one young. Young were determined as having
fledged if they disappeared from the nest within 2 days of
their predicted fledging date, or if we observed fledglings
nearby or adults carrying food in close proximity to the nest.
Nests were considered depredated if eggs or young nestlings
disappeared.
Statistical analyses
We first examined how the vegetation community changed
from 1989 to 2009. Specifically, we used correlation analyses to
determine whether the mean annual densities of the different
woody plant species–maple, locust, oak, aspen, and fir–changed across years at random sites. Densities of different size
classes of the same plant species were positively correlated, so
size classes were therefore lumped together by species. Likewise, white fir vs. Douglas fir showed positive correlations
and were therefore lumped together as fir. We used mean
annual estimates to eliminate the extensive pseudoreplication
within seasons and provide a conservative approach to change
across time. We also examined whether the relative abundance of preferred nest sites of each species changed across
years. A site was considered preferred by Orange-crowned,
Virginia’s, and Red-faced Warblers if it was dominated by
maple (>50%), locust (>40%), and fir (>40%), respectively, as
quantified in Martin (1998). We then investigated whether
vegetation composition at nest sites of the three bird species
had changed from 1989 to 2009.
We used discriminant function analysis (DFA) to examine
whether overlap in vegetation composition among species’
nest sites changed across the 21 years. Densities of maple,
locust, oak, aspen, and fir as well as the species of plant the
nest was placed under were entered as predictor variables,
and bird species identity served as the grouping variable. Nest
site overlap between the three species was computed for each
year along each discriminant function as
d2
2 2
overlap ¼ e2ðs1 þs1 Þ
where d is the distance between the two species’ centroids
along a discriminant function, s1 and s2 are the standard deviations of discriminant scores for each species (Maurer, 1982;
Finch, 1989). Total overlap between a pair of bird species was
computed as the product of overlap values for the two discriminant functions characterizing habitat use (May, 1975). Overlap values range from 0, where no overlap occurs, to 1 where
nest sites are completely overlapping. We then used correlation analysis to test whether overlap in nest site characteristics
among species pairs changed across years.
Finally, we examined whether average nest site overlap
between a given bird species and the two other species had
consequences for the rate of nest predation. Daily rates of
nest predation were determined following Mayfield (1975),
Johnson (1979), and Hensler & Nichols (1981) as some nests
were found after the onset of incubation. Rather than overlap
© 2012 Blackwell Publishing Ltd, Global Change Biology, 19, 411–419
per se, nest predation may be influenced by other aspects of
the habitat that are correlated with temporal changes in nest
site overlap. Specifically, declines in overall density of woody
stems, simplification in the composition of woody plant species at nest sites, or other unmeasured factors correlated with
year could also explain patterns of nest predation. Thus, we
evaluated whether year, the mean total stem density at nest
sites and at random sites, and each bird species’ mean position
(centroid) along each discriminant function had any effects on
daily nest predation rates. The explanatory powers of total
stem density at nest sites, total stem density at random sites,
and centroid position were evaluated alone as well as through
separate models in combination with nest site overlap. We
used backward stepwise elimination regression to determine
which variables, if any, were the best predictors of nest predation rates. Predictors with the lowest t value were removed
until all predictors in the model were significant. Year was
highly correlated with nest site overlap (see results), so we
evaluated its effects on nest predation separately to avoid
problems associated with multicollinearity.
Analyses were performed on data from 698 Orangecrowned Warbler nests, 510 Virginia’s Warbler nests, 476 Redfaced Warbler nests, and 10,532 random sites across 21 years.
The mean number of sites per year (±1 SE) for each species
was as follows: 38.4 ± 3.5 Orange-crowned Warbler nests,
28.1 ± 3.0 Virginia’s Warbler nests, 27.0 ± 2.4 Red-faced
Warbler nests, and 478.7 ± 29.8 random sites. All analyses
were performed using SPSS (version 11.5).
Results
Temporal changes in woody plant densities
Analyses of random sites showed that stem densities of
maple, locust, and firs declined across years, whereas
oak and aspen remained relatively constant at very low
densities (Table 1, Fig. 1a). Densities of maple and
locust also declined over time at nest sites of all three
species whereas densities of oak and aspen again
showed no trend (Table 1, Fig. 1). Densities of fir
decreased at Red-faced Warbler nests, but showed no
Table 1 Correlation coefficients of densities of five woody
plant species with year (1989–2009) for random sites and nest
sites of three ground-nesting songbird species
Plant
species
Nest sites
Random Orange-crowned
sites
Warbler
Virginia’s
Warbler
Red-faced
Warbler
Maple
Locust
Oak
Aspen
Fir
0.93*
0.94*
0.37
0.22
0.48*
0.72*
0.81*
0.42
0.41
0.22
0.74*
0.72*
0.37
0.21
0.76*
*P < 0.05
0.92*
0.73*
0.23
0.06
0.19
414 S . K . A U E R & T . E . M A R T I N
(a)
(b)
(c)
(d)
Fig. 1 Temporal change in densities of dominant woody plant species at random sites (a), and at nest sites of Orange-crowned Warbler
(b), Virginia’s Warbler (c), and Red-faced Warbler (d) in the Coconino National Forest, AZ, USA.
temporal trend at Orange-crowned Warbler and
Virginia’s Warbler nests (Table 1, Fig. 1).
Temporal changes in nest site selection
Fig. 2 Temporal change in relative abundances of nest sites preferred by Orange-crowned Warbler, Virginia’s, and Red-faced
Warblers. A nest site was considered preferred by Orangecrowned, Virginia’s, and Red-faced Warblers if it was dominated by canyon maple (>50%), New Mexican locust (>40%),
and white and Douglas fir (>40%), respectively, as quantified in
Martin (1998).
Decreased stem densities of maple and locust across
years led to a subsequent decrease in the relative abundance of available nest sites preferred by Orangecrowned Warbler (sites with maple >50%; r = 0.95,
P < 0.001; Fig. 2) and Virginia’s Warbler (sites with
locust >40%; r = 0.61, P < 0.01; Fig. 2), respectively.
In contrast, the faster decrease in maples and locusts
relative to firs led to an increase over time in the availability of nest sites preferred by Red-faced Warblers
(sites with >40% fir; r = 0.91, P < 0.001; Fig. 2). These
changes in vegetation and nest sites led to an increase
in overlap among nest site characteristics across years
(Fig. 3) between Orange-crowned Warbler and
Virginia’s Warbler (r = 0.50, P = 0.02), Orange-crowned
Warbler and Red-faced Warbler (r = 0.47, P = 0.03),
and Virginia’s Warbler and Red-faced Warbler
(r = 0.70, P = 0.001). This increase in overlap was due
to all three bird species progressively nesting in sites
characterized by an increasing density of firs compared
with maple, locust, oak, and aspen (Fig. 4).
© 2012 Blackwell Publishing Ltd, Global Change Biology, 19, 411–419
C L I M A T E C H A N G E E F F E C T S O N R E S O U R C E O V E R L A P 415
(a)
(b)
Fig. 4 Multidimensional habitat use among Orange-crowned,
Virginia’s, and Red-faced Warblers during years 1989–2009. Nest
site choices were differentiated along the first canonical discriminant axis (x-axis) by the abundance of firs and maples (v2 = 253.4,
df = 12, P < 0.001) and along the second axis (y-axis) by the
abundance of aspen, locust, and oak (v2 = 113.6, df = 5,
P < 0.001). Estimates are centroids for each bird species from
each year and are derived from discriminant function scores of
woody plant species at nest sites of the three bird species.
Consequences of nest site overlap for nest predation
(c)
Fig. 3 Temporal change in nest site overlap between (a) Orangecrowned Warbler and Virginia’s Warbler, (b) Orange-crowned
Warbler and Red-faced Warbler, and (c) Virginia’s Warbler and
Red-faced Warbler. Indices of overlap were derived from discriminant function scores of woody plant species at nest sites of the
three bird species. Overlap is based on the distance between and
variance within centroids among the three pairs of species, where
an overlap value of 1 signifies complete overlap among nest sites
in the abundances of the five different woody plant species
including canyon maple, New Mexican locust, Gambel’s oak,
quaking aspen, and white and Douglas fir.
© 2012 Blackwell Publishing Ltd, Global Change Biology, 19, 411–419
Year did not explain variation in nest predation
rates for any of the three species: Orange-crowned
Warbler (t = 1.32, P = 0.21), Virginia’s Warbler
(t = 1.77, P = 0.09), and Red-faced Warbler (t = 1.38,
P = 0.19). Thus, variation in nest predation was not a
simple function of general factors correlated with time.
The mean total stem density at nest sites, or and at random sites, were not good predictors of nest predation
rates for two species: Orange-crowned Warbler (nest:
t = 1.41, P = 0.17; random: t = 1.10, P = 0.30) and
Red-faced Warbler (nest: t = 1.05, P = 0.31, random:
t = 1.48, P = 0.16). Mean total stem density was marginally related to nest predation for Virginia’s Warbler
(nest: t = 2.05, P = 0.06, random: t = 1.81, P = 0.09).
Likewise, woody plant composition at nest sites,
calculated from each species’ centroid position on each
discriminant axis each year, was not a significant predictor of nest predation across years for any of the three
species: Orange-crowned Warbler (function 1: t =
1.48, P = 0.16; function 2: t = 0.23, P = 0.83),
Virginia’s Warbler (function 1: t = 1.83, P = 0.08;
function 2: t = 1.04, P = 0.31), and Red-faced Warbler
(function 1: t = 0.71, P = 0.49; function 2: t = 0.06,
P = 0.96). Thus, simple changes in plant densities and
composition over time did not predict predation rates.
416 S . K . A U E R & T . E . M A R T I N
Greater overlap among nest sites of the three bird species was associated with an increase in daily nest predation rates for all three species (Fig. 5): Orange-crowned
Warbler (b (±1 SE) = 0.05 ± 0.02, t = 2.14, P = 0.04),
Virginia’s Warbler (b = 0.07 ± 0.03, t = 2.47, P = 0.02),
and Red-faced Warbler (b = 0.04 ± 0.02, t = 2.16, P = 0.04).
Total stem density and woody plant composition at nest
sites, when each was evaluated together with nest site
overlap, were again not significant predictors of nest
predation for any of the three bird species and were
removed from the models. Ultimately, overlap in plant
species composition at nest sites was the only significant
habitat predictor of nest predation rates.
(a)
(b)
Discussion
Climate change can have direct effects on plant recruitment, growth, and community composition (Wahren
et al., 2005; Kelly & Goulden, 2008; Kreyling et al., 2011;
Elmendorf et al., 2012). However, the physiological,
behavioral, and numerical responses of herbivores to
climate change can also be important determinants of
these plant responses (Roy et al., 2004; Tylianakis et al.,
2008; Wookey et al., 2009; Massad & Dyer, 2010; Li
et al., 2011) and in some cases can have an even greater
impact on plants than warming itself (Post & Pedersen,
2008; Gornall et al., 2009; O’Connor, 2009; Brodie et al.,
2012; Martin & Maron, 2012). Although studies have
focused mainly on climate-driven herbivore impacts on
plant communities (see references above), little if any
research has examined how these impacts may trickle
down to effect the animal species that rely on plants for
nonconsumptive purposes (but see Martin & Maron,
2012). Our study demonstrates that herbivore responses
to climate change can exert a strong influence on plant
abundance and community composition but also that
these changes in the plant community can then have
important consequences for resource use and overlap
of coexisting bird species that use plant species for nesting sites. These cascading effects of climate and elk on
plants and birds are congruent with predictions that
responses of apex predators and herbivores to climate
change will have profound rippling effects throughout
the larger ecosystem (Wilmers & Post, 2006; Wilmers
et al., 2007; Zarnetske et al., 2012). Top consumers can
have disproportionate effects on the larger community
(Borer et al., 2006), and in many cases appear to be
more sensitive to climate change than species from
other trophic levels (Voigt et al., 2003; MacLennan et al.,
2012), so they are likely to play as important a role in
driving larger ecosystem responses to climate change in
other systems as they are in this one.
Declines in the abundance of three dominant tree
species led to changes in nest site choices among the
(c)
Fig. 5 Nest predation rate as a function of average nest site
overlap for three breeding songbirds: Orange-crowned Warbler
(a), Virginia’s Warbler (b), and Red-faced Warbler (c). Overlap
is based on the distance between and variance within centroids
among the three pairs of species, where an overlap value of 1
signifies complete overlap among nest sites in the abundances
of the five different woody plant species, including canyon
maple, New Mexican locust, Gambel’s oak, quaking aspen, and
white and Douglas fir. Average overlap is computed as the
mean overlap of nest sites of a given bird species with the nest
sites of the two other species in the nesting guild.
three songbird species with negative consequences for
their reproductive success. The mechanisms underlying
this positive association between nest site overlap and
© 2012 Blackwell Publishing Ltd, Global Change Biology, 19, 411–419
C L I M A T E C H A N G E E F F E C T S O N R E S O U R C E O V E R L A P 417
nest predation rates are not clear but likely involve the
disruption of nest site selection responses that historically mitigated the negative effects of both density- and
frequency-dependent predation (Martin, 1988, 1996,
1998). Predation can be an important determinant of
habitat and resource use among coexisting prey species
on both evolutionary and ecological time scales (Holt,
1984; Holt & Lawton, 1994; Wisheu, 1998). In both
aquatic and terrestrial systems, prey species that share
a common predator often partition their use of habitat
(Leibold, 1990; Martin, 1996; Gonzalez & Tessier, 1997;
Wisheu, 1998; Lingle, 2002). When predation is densityand frequency dependent, as it is in many systems
(Johnson, 2006; Middlemas et al., 2006; Lima, 2009),
segregation of prey into different habitat types can
decrease predator searching efficiency by decreasing
the apparent cumulative prey density and thereby
diluting the strength of predation by forcing predators
to search more potential prey sites, and by inhibiting
the development of predator search images (Persson,
1985; Martin, 1988, 1996; Dukas & Kamil, 2001; Ishii &
Shimada, 2010). In our system, experiments with artificial nests and observations of occupied natural nests
show that nest predation is density dependent, that
nest predation rates are reduced when nest sites are
partitioned among different sites, and that overlap in
nest site characteristics among species can lead to
increased nest predation rates (Martin, 1988, 1996,
1998). Convergence toward a single nest site type may
therefore have increased the cumulative density and
frequency of a single prey type and thereby strengthened the impact of density- and frequency-dependent
nest predation.
Nest predation is the leading cause of nesting mortality in birds (Ricklefs, 1969; Martin, 1992) and accounts
for greater than 90% of nesting failures at our study site
(Martin, 2001). Nest predation nearly tripled over the
21-year period as nest site overlap increased from
around 0.6 to almost 1.0 among the three species, signifying almost complete overlap among nest sites.
Increased predation associated with overlap among
nest sites may provide a mechanistic link between the
temporal changes in habitat and bird abundance
observed at this study site. Densities of breeding pairs
of Orange-crowned and Virginia’s Warblers have
declined over the last 25 years, whereas Red-faced
Warbler exhibits a weak but not significant decline
(Martin, 2007; unpublished data from more recent
years). Annual abundance at our site is determined by
effects of nest predation on recruitment the previous
year, but also by habitat selection choices of birds in early
spring prior to settling (Martin, 2007). Thus, declines in
the densities of Orange-crowned and Virginia’s
Warblers may be driven in part by the recruitment of
© 2012 Blackwell Publishing Ltd, Global Change Biology, 19, 411–419
fewer offspring due to increasing overlap among nest
sites and associated nest predation. Alternatively, but
not exclusively, densities of breeding pairs may be
explained by fewer birds opting to settle in areas where
the availability of preferred habitat is increasingly
lower and thus the potential for nest site overlap and
associated nest predation is higher. The lack of change
in Red-faced Warbler densities, on the other hand, is
less clear but may be driven by a decrease in recruitment that is balanced out by the increase in availability
of preferred nest sites.
Observational and experimental studies at this site
provide strong evidence that nest site overlap has negative consequences for reproductive success via its
effects on nest predation (Martin, 1988, 1996, 1998).
Other factors correlated with the observed changes in
habitat may also provide alternate explanations for
changes observed in nest predation rates. Rather than
overlap per se, increased nest predation could be driven by the decline in total stem densities that has
occurred at nest sites of the three species and across the
greater study plots in general if it increases the visibility of nests or parental trips to and from the nest,
thereby leading to higher rates of nest predation by
visually oriented predators. Decreased stem densities
and changes in vegetation composition at nest sites
could also increase nest predation if they alter nest
microclimate and thereby parental behaviors that might
attract predators or interfere with background matching of nesting birds or nest contents. However, stem
densities and vegetation composition did not explain
variation in nest predation rates suggesting that temporal changes in these specific components of habitat are
not driving the patterns we observed here. Alternatively, climate change, alone or in combination with
herbivory, may be influencing predator abundance or
hunting behavior over time by altering predator habitat
availability. Unfortunately, we do not have any data on
predator abundance or behavior over the 21-year period to assess this alternative directly. However, data on
nest predators in fenced and unfenced plots at our
study site provide some evidence that an increase in
predator abundance is not responsible for the patterns
we report in this study. Relative to unfenced plots,
predator abundance is in fact higher but nest predation
risk lower in fenced plots where, after 6 years of elk
exclusion, vegetation has returned to the density, structure, and composition recorded in the early 1990s
(Martin & Maron, 2012). If predator abundance is
directly related to these changes in habitat, then nest
predator abundance in the unfenced plots that we studied is probably lower now than it was in the late 1980s
when we began this study. The lack of direct correlation between nest predation and year also suggests that
418 S . K . A U E R & T . E . M A R T I N
the positive relationship we observed between nest predation and nest site overlap is not a simple function of
temporal changes in climate or habitat that might influence predator abundance or behavior.
Although more research is needed to evaluate these
alternative mechanisms, our results at present demonstrate that, at a minimum, climate-driven changes in
habitat from altered herbivory has direct effects on nest
site use and overlap among coexisting species. These
changes can then have negative consequences for
reproductive success in populations of these three bird
species. Reduced snowpack levels and earlier spring
snow melt times have recently been observed in many
alpine and high-latitude systems around the world
(Stone et al., 2002; Hamlet et al., 2005; Bhutiyani et al.,
2010). Given that declining snowpack can intensify herbivore impacts in this (Martin & Maron, 2012) and
other systems (Post et al., 1999; Brodie et al., 2012),
management of herbivore populations will likely play a
vital role in preserving the processes and interactions
that allow closely related species to coexist and ultimately help to maintain species diversity in the face of
climate change. Moreover, our results suggest that
changes in habitat from climate effects on plant
–herbivore interactions can alter available niche space
and influence interactions to yield critical demographic
impacts for other species within the community. Such
indirect effects of climate are subtle and can be difficult
to detect, but can be important underappreciated ecosystem effects that may exist more broadly than
currently recognized.
Acknowledgements
We would like to thank the numerous research assistants and
graduate students that helped in monitoring nests and measuring
the vegetation characteristics of nest and random sites over the
last 21 years. We also acknowledge the helpful comments and
suggestions of two anonymous reviewers. This research was supported by grants from the U.S. Geological Survey Climate Change
Research Program and the National Science Foundation (DEB0 841 764, DEB-1 241 041) to TEM. This work was conducted
under University of Montana IACUC #059-10TMMCWRU. Any
use of trade names is for descriptive purposes only and does not
imply endorsement by the U.S. Government.
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