Behavioral Ecology Vol. 13 No. 1: 101-108
© 2002 International Society for Behavioral Ecology
Comparative manipulation of predation risk in incubating birds reveals variability in the plasticity of responses
a Montana Cooperative Wildlife Research Unit, Avian Studies Program, University of Montana, Missoula, MT 59812, USA b U.S. Geological Survey, Biological Resources Division, Montana Cooperative Wildlife Research Unit, Avian Studies Program, University of Montana, Missoula, MT 59812, USA
Address correspondence to C.K. Ghalambor, who is now at the Department of Biology, University of California, Riverside, CA 92521, USA. E-mail: camerong{at}citrus.ucr.edu .
Received 23 August 2000; revised 9 April 2001; accepted 15 April 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The evolution of different parental care strategies is thought to result from variation in trade-offs between the costs and benefits associated with providing care. However, changing environmental conditions can alter such fitness trade-offs and favor plasticity in the type or amount of parental care provided. Avian incubation is a form of parental care where parents face changing environmental conditions, including variation in the risk of nest predation. Because parental activity can draw attention to the location of the nest, a reduction in nest visitation rates is a predicted response to an increased, immediate predation risk. Here, we experimentally increased the risk of nest predation using model presentations at nests of five coexisting species that differ in their ambient levels of nest predation. We examined whether individuals detect changes in nest predation risk and respond by reducing visitation to the nest. We also tested whether this behavioral response differs among species relative to differences in their ambient risk of nest predation. We found that males of all species detected the increased predation risk and reduced the rate at which they visited the nest to feed incubating females, and the magnitude of this change was highly correlated with differences in the risk of nest predation across species. Hence, as the vulnerability to nest predation increases, males appear more willing to trade the cost of reduced food delivery to the female against the benefit of reduced predation risk. Our results therefore suggest that nest predators can have differential effects on parental behaviors across species. We discuss how the comparative nature of our results can also provide insight into the evolution of behavioral plasticity.
Key words: Certhia, incubation feeding, nest predation, parental care, phenotypic plasticity, Poecile, Sitta.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The evolution of parental care strategies is thought to result from trade-offs between the fitness costs and benefits associated with providing care (Clutton-Brock, 1991
;
Roff, 1992,
Stearns, 1992). Different
environmental conditions can alter these fitness trade-offs and lead to
variation among species and populations in the amount or type of parental care
provided (e.g., Badyaev and Ghalambor,
2001; Clutton-Brock,
1991). However, environments also tend to be highly variable, such
that no single behavioral phenotype is consistently optimal. Such dynamic
conditions require plasticity in behavior as a means of tracking environmental
change. For example, in response to a perceived risk of predation, individuals
of many species exhibit adaptive changes in behavior that reduce the
probability that they will be predated (e.g.,
Lawler, 1989;
Lima, 1998;
Lima and Dill, 1990;
Sih et al., 1992). Yet, few
studies have considered the plastic behavioral responses of parents providing
care for their offspring, making it important to understand the theoretical
and empirical basis in which parents make behavioral adjustments to changing
environmental conditions (e.g., Brodie,
1989; Carlisle,
1982).
Avian incubation of eggs is a fundamental form of parental care that
requires parents to resolve time and energy trade-offs in response to changing
environmental conditions. In passerine species with uniparental incubation,
females must leave the nest during incubation to feed and meet their own
nutritional requirements, but absences from the nest can negatively affect egg
temperatures and subsequent embryo development, as well as the ability to
protect eggs against predators (e.g., Conway and Martin,
2000a,b;
Haftorn, 1988;
Moreno, 1989;
Weathers and Sullivan, 1989;
White and Kinney, 1974;
Williams, 1996). By feeding
females on the nest (i.e., incubation feeding), males can help ameliorate the
trade-off between time on the nest incubating and time off the nest foraging.
Indeed, the additional food provided by the male has been shown to increase
female nest attentiveness, resulting in shortened incubation periods and
improved hatching success (e.g., Halupka,
1994; Lifjeld and Slagsvold,
1986; Lyon and Montgomerie,
1985; Smith et al.,
1989; von Haartman,
1958). Yet, the benefits of incubation feeding can be offset by
the cost of higher nest predation, which increases with the frequency that
males visit their nests (Lyon and
Montgomerie, 1987; Martin and
Ghalambor, 1999; Martin et al.,
2000a,b;
Skutch, 1949). Thus, parents
incubating eggs must resolve a number of conflicting demands in response to
changing environmental conditions.
Most previous work has examined the extent to which parents modify
incubation behaviors in response to changes in temperature and energetic
demands (Haftorn, 1988;
Weathers and Sullivan, 1989;
White and Kinney, 1974;
Williams, 1996). Yet
incubating parents are also faced with changes in the immediate risk of nest
predation (e.g., the approach of a predator near the nest), which should favor
modifications in behavior that reduce the risk of predation (reviewed in
Lima and Dill, 1990;
Martin, 1992;
Montgomerie and Weatherhead,
1988). Because nest predation can increase with increasing
parental activity near the nest (e.g., Martin et al.,
2000a,b),
parents faced with an increased, immediate risk are predicted to decrease
visitation rates to the nest to reduce drawing attention to the location of
the nest (Ghalambor and Martin,
2000,
2001). We assume that such
behavioral plasticity in response to an immediate predation threat is under
stronger selection in species more vulnerable to nest predation from visually
oriented predators such as corvids and squirrels. For example, when a predator
approaches a nest, species that use vulnerable nest sites (e.g., open-cup
nests) should be under selection to reduce nest visitation rates more relative
to species that use safer nest sites (e.g., cavity nests) because predators
can more easily access the nest (Martin
and Ghalambor, 1999). Thus, the costs of reduced food delivery are
offset by the benefits of reduced predation risk, and differences among
species in the risk of nest predation should alter this cost-benefit
trade-off. Behavioral comparisons of populations or species that differ in
their risk of predation can therefore provide insight into the degree to which
parental decision making evolves.
We experimentally tested whether incubating parents can perceive changes in
predation risk and modify their behavior accordingly. Predation risk was
manipulated using model predator presentations near the nests of five species
that differ in their ambient nest predation risk. We tested two predictions
within and across species. First, we tested whether species exhibit adaptive
plasticity in their incubation behaviors when faced with increased, immediate
predation risk; male incubation feeding should decrease when the perceived
risk of predation increases as a strategy to minimize drawing the attention of
the predator to the nest (see above; see also
Martin and Ghalambor, 1999).
Second, we tested whether the change in incubation feeding rates in response
to predator presentations is greater in species with higher ambient risk of
nest predation, which presumably reflects greater selection intensity on
phenotypically plastic traits (e.g.,
Doughty, 1995;
Giles and Huntingford, 1984;
Gotthard and Nylin, 1995).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study species and study site
We focused on five coexisting species that are ecologically similar (i.e., hole-nesting, insectivorous, socially monogamous, with similar body mass and behavioral repertoires) and closely related phylogenetically (Harrap and Quinn, 1995
;
Sibley and Ahlquist, 1990):
pygmy nuthatch (Sitta pygmaea; Sittidae), red-breasted nuthatch
(Sitta canadensis; Sittidae), white-breasted nuthatch (Sitta
carolinensis; Sittidae), mountain chickadee (Poecile gambeli;
Paridae), and brown creeper (Certhia americana; Certhidae). Long-term
research on these five species reveals that they experience different levels
of ambient nest predation, and these differences appear to be related to
variation in nest-site characteristics
(Martin and Ghalambor, 1999,
unpublished data; Martin and Li,
1992). These species also exhibit a wide range of variation in
incubation feeding rate, which is also tightly correlated with their nest
predation rates (Figure 1; Martin and Ghalambor, 1999).
Thus, these species provide an ideal system to experimentally test whether the
correlation between nest predation and incubation feeding reflects
causality.
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Study sites were high-elevation (2600 m) snow-melt drainages on the
Mogollon Rim, Arizona, USA. A detailed description of the vegetation is
provided in Martin (1998). We
searched study sites for nests of the five focal species from May through late
June 1994-1998. All nests were in natural cavities and were intensively
monitored to assess breeding stage (i.e., egg laying, incubation, nestling). A
total of 52 natural nests were found for use in experiments (n = 11,
Sitta pygmaea; n = 13, S. canadensis; n =
11, S. carolinensis; n = 8 Poecile gambeli;
n = 9 Certhia americana), and all experiments were carried
out between days 6 and 11 of the incubation period. The majority of males and
females were uniquely color banded, and we had no indication that the same
birds were resampled in subsequent years. In addition, each experiment was
carried out on a different territory to minimize any potential territory
quality effects.
Experimental manipulation of predation risk
To test effects of predation risk on incubation behavior, we presented a
taxidermic model of a common nest predator. The goal of model presentations
was to increase the perceived risk of nest predation near the nest site
without eliciting nest defense behavior, such that males would continue to
feed incubating females. We chose to present a taxidermic model of a mammalian
predator, the red squirrel (Tamiasciurus hudsonicus), because it is
the most common nest predator of the five focal species in this study and has
been observed using parental activity as a cue to finding nests
(Martin, 1993, unpublished
data; Martin and Li, 1992).
Response to the predator model was compared to a control model of the largely
granivorous bird, the dark-eyed junco (Junco hyemalis), which
represents no predation threat. Depending on the composition of the
understory, mounts were attached to nearby tree saplings (either a quaking
aspen, Populus tremuloides, or canyon maple, Acer
grandidentatum) and placed 6-8 m from the nest tree, with the location
held constant for each model. In addition, we played taped vocalizations of
either squirrels or juncos from a cassette player placed at the base of the
sapling where the model was perched to increase detectability of the models.
To simulate the movements of a real squirrel and junco, a thin twine was
attached to the base of the sapling and used to sway the sapling during
presentations in an effort to give the impression that the model was moving.
Use of vocalizations with the moving model is particularly effective in
preventing habituation to the model alone (Ghalambor and Martin,
2000,
2001).
Experimental design and behavioral observations
We compared behavioral responses of the five bird species to squirrel and
junco models that were presented in a stratified random order on consecutive
days for each nest. Time of day and ambient temperature are highly correlated
with each other, and both are in turn correlated with incubation behaviors in
these species (Ghalambor,
1998, unpublished data). Therefore, we started all observations at
the same time each day (0600 h) to control for any possible effects of time or
temperature on parental behavior. The design consisted of an initial control
period of 90 min followed by a 90-min model presentation period of either the
predator or the control. We measured two behaviors in response to model
presentations. First, we measured the change in male incubation feeding rate
between the pre-presentation control period and the model presentation period.
Second, because the food delivered to the female can increase her time on the
nest (e.g., Martin and Ghalambor,
1999) and females may increase attentiveness in response to
increased predation risk (e.g., Beissinger
et al., 1998; Thompson and
Raveling, 1987), we also measured changes in female nest
attentiveness (% time on nest). The change in incubation feeding and nest
attentiveness between the pre-presentation and model presentation periods
represents the magnitude of change in each species and allows for a
standardized comparison across species.
Data analysis
We plotted the behavioral response of each species using standard plots of
the behavioral means against the pre-presentation and model presentation time
periods. Before analysis, incubation feeding rate was log-transformed and
percent nest attentiveness was arcsine transformed to normalize the data. We
first tested whether male incubation feeding rates were correlated with female
nest attentiveness within the five species to assess independence of the two
variables. We tested this using an ANCOVA with nest attentiveness as the
dependent variable, incubation feeding rate as a covariate, and species as a
grouping variable. We repeated this test for both the pre-presentation and
model presentation periods. We then tested for a significant order of
presentation effect (i.e., whether the squirrel or the junco was presented
first) using a repeated-measures ANOVA that tested the effect of order and the
interaction of order and species on incubation feeding rate and nest
attentiveness. All species and the difference in their responses between the
pre-presentation and model presentation time periods for days when a squirrel
or junco were presented were then included in a repeated-measures ANOVA. We
tested whether the difference in incubation feeding rate and nest
attentiveness differed between model types and whether there was an
interaction between these behavioral responses and species. To directly
compare how much each species modified its behavior in response to the
predator model, we compared incubation feeding rates and nest attentiveness
during the pre-presentation and model presentation time periods on days when
only the squirrel was presented. As above, we used a repeated-measures ANOVA
and tested for a significant time effect (pre-presentation versus
presentation) and a time-by-species interaction effect.
The five species exhibit large differences in their baseline rates of incubation feeding (Figure 1). Large differences in baseline rates make comparisons of behavioral plasticity among species complicated because the same absolute change in one species may not be equivalent to the same changes in another. For example, Sitta pygmaea males may feed incubating females more than 10 times per hour, whereas Certhia americana males rarely feed females more than 4 times per hour. Thus, a reduction by 2 feeds per hour in these two species would represent either a 20% or 50% change in food delivery to the female, respectively. We therefore standardized responses across species by converting absolute changes in each behavior to percent changes between the pre-presentation period and the predator presentation time periods. We then tested the relationship across species between response to the predator and variation in the risk of nest predation using a nonparametric Spearman rank correlation test because the small number of species resulted in a non-normal distribution.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We expected to find a close relationship between incubation feeding and nest attentiveness; however, we found no correlation between these traits in any of the five species during the pre-presentation control period (ANCOVA, F = 0.53, df = 1, 47, p =.82) or the model presentation period (ANCOVA, F = 0.009, df = 1, 47, p =.93), and thus we treated these two behaviors as independent variables (see Discussion). We then tested for order effects in presentation experiments and found that the order in which models were presented had no effect on incubation feeding rates (repeated-measures ANOVA; F = 6.05, df = 1, 39, p =.41), and there was no order-by-species interaction effect (repeated-measures ANOVA; F = 11.55, df = 4,39, p =.28). We found the same result for nest attentiveness; there was no order effect (F = 0.824, df = 1, 40, p =.37) or order-by-species effect (F = 1.09, df = 4, 40, p =.37), so we dropped this term from further analyses.
There was a significant effect of model type on male incubation feeding rates when all species were grouped together (repeated-measures ANOVA; F = 39.96, df = 1, 48, p <.0001), reflecting that incubation feeding rates dropped more in the presence of the predator model than in the presence of the control (Figure 2). Indeed, in the presence of the squirrel model, we observed males of all five species arriving in the vicinity of the nest (< 10 m) with food in their bills, then leaving the vicinity of the nest without feeding the female. We never observed this behavior in the presence of the control model, suggesting that males recognized squirrels as a potential threat and were hesitant to visit the nest when a squirrel was present. In no case did we observe males attacking or exhibiting any type of nest defense behavior toward either the predator or control models. In contrast to male incubation feeding rates, female nest attentiveness did not significantly change in response to model presentations (Figure 3; ANOVA, F = 1.99, df = 1, 43, p =.17). During sessions off the nest, females of all species were occasionally observed perching and foraging directly above the squirrel model, but no clear difference in female behavior was observed in response to the predator and control models. In no case were females observed attacking the predator or the control models.
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When only the response to the predator model was considered (Figure 4a), feeding rates significantly differed between the pre-presentation and predator presentation periods for all species (repeated-measures ANOVA, F = 139.05, df = 1, 46, p <.0001). The change in incubation feeding rate significantly differed among species (repeated-measures ANOVA, F = 76.14, df = 4, 46, p <.0001), and there was a significant species by treatment interaction (F = 12.14, df = 4, 46, p <.0001). The significant interaction between species and treatment was primarily driven by differences in incubation feeding rates in the presence of the nest predator, rather than by large differences in initial feeding rate among species (Figure 4a). Thus, slopes measure the extent of change in incubation feeding rates in the presence of a nest predator (Figure 4a). The same analysis for nest attentiveness (Figure 4b) showed no differences in attentiveness between the pre-presentation and predator presentation periods (repeated-measures ANOVA, F = 0.872, df = 4, 45, p =.36). There was, however, a significant species effect (F = 21.53, df = 4, 45, p <.0001), but no species-by-treatment interaction (F = 1.104, df = 4, 45, p =.37), reflecting that species significantly differed in the amount of time spent on the nest but not in their responses to the presentations (Figure 4b). The only species that showed any measurable change in nest attentiveness was Certhia americana, which increased its time on the nest in response to the predator presentation (Figure 4b).
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We predicted that the magnitude of decreases in incubation feeding rates in
response to the predator model should be greater in species with greater risk
of nest predation. We found the magnitude of standardized changes (i.e.,
decreases) in incubation feeding in response to the predator model were,
indeed, larger for species at greater risk of nest predation
(Figure 5a; Spearman 
=
0.90, df = 5, p =.019). Percent change in female nest attentiveness
was not related to risk of nest predation (Spearman = 0.30, df = 5,
p = 0.30; Figure 5b),
and only Certhia americana exhibited a percent change that was
significantly different from zero (Figure
5b).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Studies of phenotypic plasticity have historically been limited to environmentally induced changes in morphology and life histories, while plasticity in behavioral traits has been relatively understudied (Carroll and Corneli, 1999
).
Yet understanding the factors that influence behavioral plasticity may play an
essential role in understanding the selective pressures creating variation in
parental care strategies within and across species. Here we experimentally
tested whether parents of five coexisting, cavity-nesting species were able to
perceive an increase in the risk of nest predation and adjust their behavior
accordingly. We found strong evidence that males of all species recognize a
potential nest predator and respond by reducing their incubation feeding rates
(Figures 2 and
4a). A reduction in incubation
feeding is assumed to be an adaptive strategy that reduces the risk of drawing
the attention of visually oriented predators to the nest (see also Ghalambor
and Martin, 2000,
2001; Martin et al,
2000a,
b). By conducting experiments
in a comparative framework, we were also able to test and demonstrate that the
slope of the behavioral responses (Figure
4a) and the magnitude of change
(Figure 5a) in incubation
feeding rates increased as the risk of nest predation increased across
species. Thus, differences in the risk of nest predation across species
predict variation in both the mean incubation feeding rates
(Figure 1) and plasticity in
incubation feeding rate in the presence of a nest predator (Figures
4a and
5a). These results are
consistent with the previously proposed hypothesis that variation in
incubation feeding rates among species has evolved in response to differences
in the ambient risk of nest predation
(Martin and Ghalambor,
1999). In contrast to male incubation feeding rates, females did not generally modify their time on the nest incubating eggs in response to nest predator presentations, despite a reduction in the amount of food received from the male (Figures 3 and 4b). Below we discuss the implications of these results for our understanding of parental care tactics during incubation and for behavioral plasticity in general.
Response to predation risk within species
Strategic or adaptive changes in behavior that affect fitness often depend
on the ability of an individual to monitor changes in the environment (e.g.,
Moran, 1992). We found
reductions in feeding visits by males in the presence of the squirrel model,
but a lack of response to the control model, indicating that birds are able to
track changes in immediate predation risk
(Figure 2). Males were never
observed attacking the predator model or engaging in other types of behavior
near the nest, suggesting that males trade the benefits of food delivery to
the female against the costs of attracting attention to the nest by reducing
visits to the nest in the presence of a nest predator. Yet, a reduction in
food delivered to females is also predicted to have costs in the form of
reduced female nest attentiveness because females are forced off the nest to
forage for themselves. Numerous studies have found that nest attentiveness by
females is highly responsive to changes in food delivered by males (e.g.,
Lifjeld and Slagsvold, 1986;
Lyon and Montgomerie, 1985;
von Haartman, 1958). Yet only
Certhia americana showed a change in nest attentiveness between days
when a predator and a control model were presented
(Figure 3), and, contrary to
our prediction, attentiveness increased rather than decreased (see also
Figure 4b). We see two possible
explanations for this discrepancy. First, a lack of reduction in female nest
attentiveness may simply reflect the shortterm (90 min) duration of the
presentations, where females were able to maintain nest attentiveness without
compromising their energy balance. Second, females, like males, may perceive
the increased risk of nest predation and maintain nest attentiveness as a
strategy to reduce risk to eggs (Beissinger
et al., 1998; Kleindorfer and
Hoi, 1997; Marzluff,
1985; Thompson and Raveling,
1987). Incubating females of the three nuthatch species are very
effective at deterring squirrels using antipredator displays at the nest (see
Ghalambor and Martin, 1999;
Kingery and Ghalambor, 2001),
but no comparable data are available for the other two species. In response to
both an increased risk of nest predation and a reduction in food from the
males, females may be faced with the conflicting pressures of needing to get
off the nest to forage versus spending time on the nest for defense,
independent of the thermal requirements of the eggs (see also
Beissinger et al., 1998;
Thompson and Raveling, 1987).
Similar experiments to those conducted here on species where males do not feed
females could test the effects of nest predation risk on female behavior
independent of changes in male food delivery.
The observed responses to predator presentations should also be sensitive
to the type of nest predator encountered. We chose to use a squirrel model for
our predator presentations because squirrels are the most common nest predator
of all cavity-nesting birds on our study site
(Martin, 1993;
Martin and Li, 1992) and
because squirrels have been observed using parental activity as a cue to
finding the location of nest sites (Ghalambor and Martin, unpublished data).
However, nest predators may differ in the level of risk they pose and how that
risk is perceived by nesting birds. For example, Steller's jays (Cyancitta
stelleri) are also highly visual and common nest predators at this study
site, but they have difficulty accessing the deeper cavity nests of Sitta
pygmaea and Sitta canadensis (Ghalambor and Kingery, 2001;
Ghalambor and Martin, 1999).
Had we used a Steller's jay model, it is possible that S. pygmaea and
S. canadensis would have not modified their incubation feeding rates.
Indeed, in other experiments we have shown that cavity-nesting species respond
less strongly to a jay model than do coexisting, open-cup—nesting
species (Ghalambor and Martin,
2001). Thus, the type of predator encountered near the nest may
elicit different responses, and future studies should explore how birds alter
their behavior to the suite of predators with which they coexist.
Response to predation risk across species
Differences among species in behavioral responses to the predator model are
most obvious for incubation feeding (Figure
4a). For example, incubation feeding rates drop to almost zero in
the presence of the predator model in Poecile gambeli, a species with
a relatively high risk of predation, whereas feeding rates decrease only
slightly in Sitta pygmaea, the species with lowest risk of nest
predation (Figure 4a). These
differences in behavioral plasticity exist despite presentation of the same
standardized predator stimulus. Such results may reflect that behavioral
plasticity has evolved in response to different predation rates (see below).
Other comparative studies of behavioral plasticity among populations and
species have found similar support for variation in plastic responses as an
adaptation to different environmental conditions
(Blouin, 1992;
Giles and Huntingford, 1984;
Rodd et al., 1997).
Ultimately, however, data on the heritabilities of these behavioral responses
are needed before we can conclude whether the differences in plasticity among
species reflect evolved or learned differences. In contrast to the male
response, the absolute change and the percent change in female nest
attentiveness did not vary among any of the species except Certhia
americana, which increased its nest attentiveness in response to the
predator model (Figures 4b and
5b). Further investigation into
the behavioral changes of incubating females in response to nest predators is
clearly warranted, particularly in the majority of species where females must
resolve the trade-off between time on the nest incubating and time off the
nest foraging without male assistance.
One interesting aspect of our results that warrants discussion is the
relationship between mean incubation feeding rates and associated plasticity.
Increased levels of nest predation are associated with lower mean incubation
feeding rates among species (Figure
1; Martin and Ghalambor,
1999). A consequence of low baseline incubation feeding rates is
that the potential for plasticity is reduced in species at very high risk of
nest predation because males feed females infrequently. This is the case for
Certhia americana, where males feed incubating females at a much
lower rate than the other four species
(Figure 4a). Thus, although in
response to the predator model C. americana males reduced feeding
visits to near zero, the absolute change in feeding was relatively small
compared to the other species (Figure
4a). The slope of change measuring the plastic response in
incubation feeding is therefore more shallow in C. americana than
expected given its risk of nest predation. We attempted to correct for this
effect by converting absolute changes in incubation feeding to percentage
changes in order to standardize the response across species
(Figure 5a). These standardized
responses also show a strong relationship between the magnitude of change and
risk of nest predation that asymptotes as incubation feeding approaches zero
in the presence of the predator (Figure
5a). However, it is important to recognize that the same absolute
change will have a larger standardized effect in species that feed less
frequently, such as C. americana, making even standardized
comparisons across species problematic if large differences exist in baseline
feeding rates. In terms of the costs and benefits associated with incubation
feeding under the risk of predation, what we ultimately need to know is how
much absolute versus relative reductions in food to the female influence both
the probability of nest predation and the female's energetic demands in
different species.
Implications for the evolution of behavioral plasticity
Behavioral traits, like other phenotypic traits, vary as a function of the
interaction between genes and the environment (see
Carroll and Corneli, 1999). The
norm of reaction or set of phenotypes expressed across a range of environments
by a single genotype is the conceptual framework most often used in studies of
plasticity (e.g., Stearns,
1989). However, reaction norms can also be considered properties
of any genetically related group of individuals, such as clones, populations,
or species. To the extent that reaction norms are heritable, comparisons of
the slopes of reaction norms provide insight into the evolution of plastic
traits (e.g., Doughty, 1995;
Gotthard and Nylin, 1995;
Scheiner, 1993). Nonparallel
norms of reaction can be used as evidence for the evolution of phenotypic
plasticity to different selective environments
(Blouin, 1992;
Carroll and Corneli, 1999;
Doughty, 1995;
Gotthard and Nylin, 1995;
Thompson, 1999). In the
present study we found strong evidence for nonparallel norms of reaction among
species with respect to male incubation feeding rate but weak evidence for
female nest attentiveness (Figure
4). Had the slopes for changes in incubation feeding been
parallel, our results would have suggested that, while mean differences exist
in incubation feeding, the behavioral response to a potential predator was
similar among species. The nonparallel slopes we observed suggest that
plasticity associated with incubation feeding has diverged among species, and
this divergence is strongly associated with differences in the risk of nest
predation across species. Because manipulative experiments in behavioral
ecology are typically carried out on single species and within single
populations, the comparative results observed here are rare, yet they may be
highly informative regarding the environmental forces responsible for
variation in behaviors. Had we carried out this study on only S.
pygmaea, we may have concluded that nest predators have a weak to
marginal effect on parental behavior, whereas if we had studied only S.
carolinensis, we would have concluded that predation risk has a very
strong effect. Only by placing these experiments within a comparative context
is the relationship between parental behavior and nest predation revealed.
Indeed, we have recently conducted similar experiments during the nestling
period on 10 species that fall along a nest predation gradient and found
similar results to those presented here
(Ghalambor and Martin, 2001,
unpublished data). Thus, there appears to be a general pattern between how
strongly birds respond to nest predators and their ambient risk of nest
predation.
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ACKNOWLEDGEMENTS |
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We thank Pam Watts, Paul Martin, and Chavez del Agua for help with the predator presentation experiments and many field assistants for help collecting the other field data that made this study possible. We thank the Arizona Game and Fish Agency, Blue Ridge Ranger Station of the Coconino National Forest, and the Apache-Sitgreaves National Forest for their support of this work. This study was supported by grants to T.E.M. from the National Science Foundation (DEB-9407587, DEB-9527318, DEB-9707598), and the BBIRD (Breeding BIology Research and Monitoring Database) program under the Global Change Research Program of the U.S. Biological Resources Division. C.K.G. was supported in part by a doctoral dissertation improvement grant from the National Science Foundation (IBN-9701116). This manuscript was improved by discussions and comments from Farrah Bashey, Alex Badyaev, Scott Carroll, Michael Bryant, Dionna Elder, David Reznick, Paul Martin, Trevor Price, David Westneat, Marlene Zuk, and one anonymous reviewer.
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