THE YEAR IN EVOLUTIONARY BIOLOGY 2009
Predation on Dependent Offspring
A Review of the Consequences for Mean Expression
and Phenotypic Plasticity in Avian Life History Traits
Thomas E. Martina and James V. Briskieb
a
b
United States Geological Survey, Montana Cooperative Wildlife Research Unit,
University of Montana, Missoula, Montana, USA
School of Biological Sciences, University of Canterbury, Christchurch, New Zealand
Predation on dependent offspring (i.e., offspring that depend on parents for care) forms a
critical source of natural selection that may shape a diversity of life history traits. Selection from predation risk on dependent offspring can influence life history strategies of
both offspring and parents. Such selection may act on both the form of plastic responses
(e.g., the shape of norms of reaction) and mean expression of traits. Consideration of
both levels of responses is key to understanding the ecological and evolutionary role of
predation on dependent offspring. Here, we discuss how plastic responses and mean
expression of life history traits may respond to selection from predation on dependent
offspring in nests of birds (i.e., nest predation). We then review the expected effects and
evidence for a diversity of life history traits, including clutch size, egg size, renesting
rates, onset of incubation, parental incubation behavior, development rates and period
lengths, parental feeding behavior, nestling begging, and nest conspicuousness. The evidence demonstrates a broad role of nest predation on both phenotypic plasticity and
mean expression of diverse traits, but evidence remains limited to a few studies on a
limited variety of species for almost all traits, and much broader experimental tests are
needed.
Key words: clutch size; egg size; development rates; life history; tradeoffs; nest predation; parental care; passerines
Introduction
Understanding why species differ in life history traits that strongly influence fitness (i.e.,
fecundity, adult survival, reproductive effort,
development rates, and parental care strategies) remains a major question in evolutionary ecology (Charlesworth 1980; Partridge &
Harvey 1988; Roff 1992; Charnov 1993, 2000;
Martin 1995, 1996, 2004). Offspring predation
strongly influences phenotypic expression of life
history traits in insects and aquatic organisms,
but such studies have focused largely on indepen-
Address for correspondence: Thomas E. Martin, Montana Cooperative Wildlife Research Unit, Natural Science 205, University of Montana,
Missoula, MT 59812. tom.martin@umontana.edu
dent offspring (Reznick & Bryga 1987; Crowl
& Covich 1990; Reznick et al. 1990, 1996;
Roff 1992; Benard 2004). Predation on dependent offspring (i.e., those that depend on parents for care) also can form a powerful source
of natural selection (Martin 1988, 1992a, 1998;
Wiklund 1995, 1996) that can act on both offspring and parental care traits. The neglect of
this source of selection is exemplified by the
book on parental care by Clutton-Brock (1991),
which does not mention the possible influence
of offspring predation on parental care strategies. Nonetheless, evidence has accumulated
for the importance of offspring predation in
the evolution of parental care strategies and
offspring life history traits (Skutch 1949; Martin et al. 2000a, 2006, 2007; Martin 1992b,
2002).
The Year in Evolutionary Biology 2009: Ann. N.Y. Acad. Sci. 1168: 201–217 (2009).
c 2009 New York Academy of Sciences.
doi: 10.1111/j.1749-6632.2009.04577.x 201
202
Dependence on parental care can lead to
different mechanistic pathways of responses to
selection by predation compared with independent offspring. Feeding activity and growth
rates provide one example. Increased predation risk on independent offspring can cause
reduced feeding activity by offspring and yield
slower development in some systems, such as
aquatic vertebrates and invertebrates as well as
terrestrial insects (Van Buskirk 2000; Altwegg
2002; Benard 2004). Increased predation risk
on dependent young of terrestrial vertebrates
can cause parents to reduce the rate that they
feed young (Skutch 1949; Martin et al. 2000a)
and, thereby, also reduce growth rates (e.g.,
Scheuerlein & Gwinner 2006; Thomson et al.
2006). Slower growth from reduced food, therefore, occurs in species with independent and
dependent young, but the mechanistic pathway
differs. Slower growth was caused by reduced
parent feeding in species with dependent offspring and through reduced offspring foraging
in species with independent young. This proximate result is opposite of that expected evolutionarily; populations or species with greater
offspring predation risk are expected to evolve
faster development to more quickly escape risky
stages (Case 1978; Arendt 1997; Martin 2002;
Remeš & Martin 2002; Roff et al. 2005; Martin
et al. 2007). Such differences highlight the importance of considering both proximate plastic responses and evolutionary responses. In
short, predation on dependent offspring can
yield proximate and evolutionary solutions in
both offspring and parental strategies. Here,
we review ideas and evidence of the potential
consequences of this source of natural selection
in birds.
Birds with altricial young provide an excellent system for studying the importance of dependent offspring predation; loss to predation
of offspring in nests (i.e., nest predation) forms a
strong source of natural selection (Martin 1988,
1992a, 1998; Wiklund 1995, 1996) that is suggested to influence many traits (Table 1). Studies of birds have played a major role in shaping
contemporary views of life history evolution,
Annals of the New York Academy of Sciences
but the focus has been on food limitation, rather
than nest predation, as the major driver of
life history strategies (Lack 1954; Martin 1987,
1996, 2004; Partridge & Harvey 1988; Ferretti
et al. 2005). Much life history work in birds
also has focused on north temperate species
nesting in boxes, which might provide a skewed
view of food versus predation; species using nest
boxes have some of the largest clutch sizes of
any passerine species, potentially magnifying
the importance of food, while minimizing the
role of predation because of the safety of boxes
(Martin 2004). Certainly, food can influence life
history traits (see review in Martin 1987) and
food can interact with nest predation to influence outcomes (Martin 1992b; Zanette et al.
2006; Eggers et al. 2008). However, our focus
here is to explore how predation on dependent
offspring can influence trait expression, not to
assess its importance relative to other possible
sources of selection.
Birds provide a practical system for the study
of life history evolution because selection intensity from offspring predation can be readily
estimated (e.g., Martin 1998; Chalfoun & Martin 2009). Nest predation accounts for 70%–
95% of reproductive mortality in most bird
species and thus exerts significant selection
(Martin 1988, 1992a, 1993a, 1995; Wiklund
1995, 1996). Direct estimation of selection intensity can strengthen inferences about the potential evolutionary influence of nest predation,
if traits include quantitative genetic variation.
This assumption is reasonable because quantitative genetic variation has been found for
many of these traits (e.g., Roff & Mousseau
1987; Mousseau & Roff 1987; Houle 1992;
Merila 1996; Kölliker et al. 2000; Sheldon et al.
2003; MacColl & Hatchwell 2003, 2004). Thus,
birds provide an important model for examining the influence of predation on dependent
offspring as a source of natural selection on the
evolution and plasticity of a wide range of offspring and parental traits (Table 1).
Nest predation can influence both phenotypic plasticity and mean expression of traits,
but understanding and consideration of the
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Martin & Briskie: Nest Predation and Life History Strategies
TABLE 1. Traits Hypothesized to be Influenced by Predation on Dependent Offspring, Plus the Hypothesized Direction of Ultimate/proximate (A Single Sign Indicates Direction is the Same for Both) Phenotypic
Changes (Evolved Mean Change and Plastic Responses) to Increased Predation Risk, and References
Theorizing or Demonstrating the Relationships
Trait
Ultimate/
proximate
relationship
Clutch size
−
Egg size
Nos. of broods/renesting rates
−
+
Timing of the onset of incubation
Rates males feed incubating females
−
−
Incubation activity
−
Nest attentiveness (% time on nest)
Biparental (shared) incubation
Parental trips to feed offspring
+
+
−
Prey loading (quantity of food/trip)
Female-only parental care
Development periods
+
+
−
Development rates
+/−
Nestling begging intensity
−
Nest size and conspicuousness
−
References
Skutch 1949; Slagsvold 1982a, 1984, 1989a, 1989b;
Kulesza 1990; Martin 1995; Martin & Clobert 1996;
Julliard et al. 1997; Martin et al. 2000a; Doligez &
Clobert 2003; Ferretti et al. 2005; Eggers et al. 2006;
Zanette et al. 2006; Kleindorfer 2007; Olsen et al. 2008
Martin et al. 2006; Fontaine & Martin 2006a
Slagsvold 1984; Major 1991; Martin 1995; Zanette et al.
2006
Clark & Wilson 1981; Hussell 1985; Briskie & Sealy 1989
Martin & Ghalambor 1999; Ghalambor & Martin 2000,
2002; Fontaine & Martin 2006a
Weathers & Sullivan 1989; Martin & Ghalambor 1999;
Conway & Martin 2000; Ghalambor & Martin 2000,
2002; Ferretti et al. 2005; Kleindorfer 2007; Massaro
et al. 2008; Olsen et al. 2008
Conway & Martin 2000; Fontaine & Martin 2006a
Kleindorfer & Hoi 1997
Skutch 1949; Sargent 1993; Martin et al. 2000a, 2000b;
Fontaine & Martin 2006a; Ferretti et al. 2005; Muchai &
duPlessis 2005; Eggers et al. 2005, 2008; Massaro et al.
2008; Peluc et al. 2008; Olsen et al. 2008; but see Roper
& Goldstein 1997
Martin 1996; Martin et al. 2000a
Willis et al. 1978; Frith et al. 1997; Willis & Oniki 1998
Lack 1948; Nice 1957; Bosque & Bosque 1995; Martin
1995; Remeš & Martin 2002; Martin 2002; Roff et al.
2005; Martin et al. 2007
Case 1978; Bosque & Bosque 1995; Remeš & Martin 2002;
Martin 2002; Ferretti et al. 2005; Scheuerlein & Gwinner
2006; Thomson et al. 2006; Martin et al. 2007
Redondo & Castro 1992; Haskell 1994; Leech & Leonard
1997; Briskie et al. 1999
Lill 1974; Snow 1978; Slagsvold 1982b, 1989a, 1989b;
Oniki 1985; Møller 1990; Galligan & Kleindorfer 2008
consequences at both levels remain rare. Most
attention to evolution of life history traits has
focused on mean expression by populations
or species (e.g., Martin 1995). Yet, phenotypic plasticity can also be under selection and
evolve. Phenotypic plasticity represents proximate phenotypic adjustments to environmental variation, such as nest predation risk, and
the line connecting phenotypic expression of
a genotype among environments (i.e., different levels of nest predation risk) represents
the reaction norm (Schlichting 1986; Scheiner
1993; Schlichting & Pigliucci 1998; Doughty &
Reznick 2004; Pigliucci 2005). Here, we consider phenotypic plasticity in life history traits
that are under behavioral control and therefore
reversible rather than permanent changes that
occur in development. Consideration of both
204
phenotypic plasticity and mean expression is
critical for advancing understanding of the ecological and evolutionary influence of nest predation on life history strategies.
Phenotypic Plasticity and Mean
Expression of Traits
Many studies have documented plastic responses in clutch size, egg size, development
rates, and various parental care behaviors in
relation to variation in nest predation risk
(references in Table 1, also Schmidt et al.
2006). Plasticity clearly is an important phenotypic attribute that can evolve (Schlichting
1986; Scheiner 1993; Schlichting & Pigliucci
1998; Donohue et al. 2001; DeWitt & Scheiner
2004a; Doughty & Reznick 2004; Pigliucci
2005; Nussey et al. 2005). The extent of phenotypic change in response to environmental
variation, or steepness of reaction norms, is one
of the key attributes that can evolve (de Jong
1990; Gibert et al. 1998; Schlichting & Pigliucci
1998; Donohue et al. 2001; Pigliucci 2005). Yet,
tests of differences in extent of plasticity among
species that evolved under different levels of selection are lacking (Donohue et al. 2001; Ghalambor & Martin 2002; Pigliucci 2005). How
the extent of plasticity varies is predicted to depend on the strength and variability of selection
(Schlichting & Pigliucci 1998). Relaxed selection from low predation rates may allow traits
to be more plastic, or traits may become more
canalized because of either benefits from higher
expression or costs of plasticity (DeWitt et al.
1998; Price et al. 2003). Strong but constant
selection may also yield canalization, whereas
strong but variable selection may favor greater
plasticity (Pigliucci 2005), and depending on
the ability to ameliorate selection, plasticity can
influence evolutionary change in mean expression (Price et al. 2003).
Phenotypic plasticity can potentially ameliorate the evolutionary influence of nest predation on mean trait expression when phenotypic
adjustments reduce the strength of selection im-
Annals of the New York Academy of Sciences
posed. For example, the rate that parents feed
their offspring is heritable (Freeman-Gallant &
Rothstein 1999; MacColl & Hatchwell 2003)
and, therefore, subject to evolution from selection by nest predation. Nest predation rates can
increase with the rate that parents visit the nest
to feed offspring (Skutch 1949; Martin et al.
2000a, 2000b; Muchai & DuPlessis 2005; Rastogi et al. 2006), and parents of some species
demonstrate phenotypic plasticity by reducing
feeding rates in environments with greater predation risk (Ghalambor & Martin 2000, 2002;
Eggers et al. 2005, 2008; Fontaine & Martin
2006a). Such plasticity can ameliorate predation risk and thereby reduce selection for evolutionary change in mean trait expression while
favoring increased plasticity.
The extent to which plasticity ameliorates
predation risk among species, however, may
vary and probably does not completely erase
differences in selection intensity among species.
For example, birds that nest in open cups (opennesting species) typically experience higher nest
predation risk than birds that nest in cavities
(Lack 1948; Nice 1957; Martin & Li 1992;
Martin 1995). Selection may have favored reduced parental activity in terms of feeding
visits among open-nesting species compared
with cavity-nesting species to reduce predation
risk (Martin & Ghalambor 1999; Martin et al.
2000a). Nonetheless, even if parental activity is
eliminated, open nests retain a higher ambient
rate and risk of predation than cavity nests because open nests are more accessible (Fontaine
et al. 2007). Thus, reduced parental activity
may be favored to reduce predation risk on
open nests, but it does not eliminate the ambient difference in risk that exists among nest
types. This ambient difference in risk therefore remains as a differentiating selection pressure that influences evolution of reaction norm
slopes and mean expression among species.
In the common cases where plasticity is insufficient to offset the change in risk, mean
expression may change along with plasticity
(Waddington 1961; Price et al. 2003), although
such possibilities are untested. Moreover, the
Martin & Briskie: Nest Predation and Life History Strategies
205
Figure 1. Responses of nest predation and parental feeding rate (number of trips to the
nest/h) to each other. (A) Response of nest predation to changes in parental feeding rate within
two example species that differ in their ambient risk of nest predation. The response lines reflect
the interaction of ambient risk with changes in risk from predator responses to changes in
feeding rates. More vulnerable species, such as open-nesting species, show a steeper increase
in predation risk with increasing feeding rate because nests are vulnerable to predators and
increased activity increases detection of these vulnerable nests by predators. In contrast,
increasing feeding rate in species in safer nests, such as cavity-nesting species, produces
a much shallower increase in predation risk because cavities are difficult for predators to
access, so predation risk increases only slightly even with increased activity. (B) Plasticity of
parental feeding rate to changes in ambient (background levels) nest predation risk. Solid
lines reflect reaction norms in response to changes in ambient predation risk (e.g., different
habitats or changing predator populations) within high risk (i.e., open nesting) versus low
risk (i.e., cavity nesting) species. Reaction norms are steeper in high risk species because
increases in ambient risk increase predation costs faster with increasing feeding rates than
in low-risk species. Moreover, food costs from reduced feeding may more closely approach
or even exceed costs of increased predation risk in low-risk species, thereby further favoring
low slopes in low-risk species. The solid circles are the means of species and indicate that
higher predation risk can favor evolution of lower mean feeding rates, and this evolutionary
relationship among species is reflected by the dashed line. Thus, the mean expressions of
feeding rate, and the reaction norms, should differ among species with changes in ambient
predation risk.
change in both mean expression and reaction
norm can be influenced by the rate at which
the selection pressure changes with phenotypic
adjustment. For example, the rate that predation risk increases with feeding rate might be
expected to differ among species as a function
of their relative vulnerability to nest predation.
Predation risk might be expected to increase
at a faster rate (steeper slope) with increased
feeding rate in vulnerable species, such as an
open-nesting species, than in a species with a
safer nest site, such as a cavity-nesting species
(Fig. 1A). Such differences may be important
because they can affect the relative strength
of selection on mean trait expression and the
shape of the trait’s reaction norm.
The steep increase in predation risk with
feeding rate in species with high ambient levels of nest predation risk (i.e., open nesting)
(Fig. 1A) may favor not only a lower mean
feeding rate but also a steep reaction norm,
where increases in ambient predation risk are
associated with steep decreases in feeding rates
(Fig. 1B). In contrast, in safer cavity-nesting
species the low ambient level of nest predation
risk and mild increase in risk with increasing
feeding rates (Fig. 1A) may favor not only higher
mean feeding rates but also smaller changes
(i.e., lower slope) in response to increases in ambient predation risk (Fig. 1B; also see Ghalambor & Martin 2002). Indeed, in such situations
the cost of not reducing feeding rates in terms of
206
Figure 2. Example of an association in both
slope of reaction norms and mean expression of the
trait among species from data in Ghalambor & Martin (2002). Here, the slope of the response in the
rate that males visit nests to feed incubating females
with experimental differences in nest predation risk is
strongly associated with mean feeding rates across
five species studied in northern Arizona, and both
are strongly related to nest predation risk (see Ghalambor & Martin 2002).
predation could be less than the costs of reducing feeding rates in terms of food loss to young.
Here we expect the slope of the reaction norm
to be inversely related to mean trait expression; species with higher predation risk should
show greater plasticity (steeper slopes) associated with lower mean feeding rates, and data
from Ghalambor & Martin (2002) support this
predicted inverse association between plasticity
and mean trait expression (Fig. 2). Of course,
steepness of the reaction norm can be positively or negatively related to mean expression
depending on direction of selection on each.
Nonetheless, this discussion (Fig. 1) and result
(i.e., Fig. 2) highlights the importance of considering the coevolution of mean expression and
plasticity in considerations of the evolution of
life history traits.
In addition to parental feeding activity, other
traits also may differ in the extent that their
means and/or plasticity evolve in response to
nest predation either from differences in heritability and/or strength of selection. Identification of such variation among traits is needed
Annals of the New York Academy of Sciences
(DeWitt & Scheiner 2004b; Pigliucci 2005), and
the study of multiple traits is important from
several standpoints. First, past work in birds
has commonly focused on a single life history
trait, such as clutch size, whereas life history
strategies include a diversity of traits that can
trade off and influence each other (Roff 1992;
Martin 1992b, 2004). Understanding tradeoffs
is critical to understanding variation in individual traits, such that attention to a broader set of
traits may pay dividends in advancing understanding of life history evolution (Roff 1992;
Charnov 1993; Martin 2004; Ferretti et al.
2005; Martin et al. 2006). Second, examination
of hypothesized effects of nest predation across
multiple traits (e.g., Table 1) increases strength
of inference of the potential role of predation
because the traits serve as a form of replication; demonstrating that many traits evolved in
hypothesized directions concordant with rates
of nest predation provides much stronger inference than demonstrating it for one trait. Finally,
determination of differences among traits in selection differentials and evolutionary responses
in mean expression and plasticity depends on
study of multiple traits. Keeping in mind these
potential interactions and expectations of proximate plastic responses (i.e., reaction norms)
and mean expression of traits in response to
selection from nest predation, we briefly review
the theoretical expectations and evidence for
each of the traits in Table 1.
Review of Individual Traits
Clutch Size
A variety of different mechanisms have been
hypothesized to explain an influence of nest
predation on clutch size (see Skutch 1949; Cody
1966; Slagsvold 1982a; Lima 1987; Martin
1992b, 1995; Martin et al. 2000a). Regardless
of mechanism, these hypotheses by and large
predict that clutch size should be reduced in response to increased nest predation risk whether
as proximate plastic responses or as evolved
Martin & Briskie: Nest Predation and Life History Strategies
mean expression (Table 1). Some studies have
shown plastic responses in clutch size to variation in predation risk (e.g., Julliard et al. 1997;
Doligez & Clobert 2003; Eggers et al. 2006),
whereas other studies of a larger diversity of
species found no plastic response in clutch size,
even when other traits showed strong responses
to nest predation risk (e.g., Fontaine & Martin 2006a; Massaro et al. 2008). These differences suggest that clutch size plasticity may be
limited in response to variation in nest predation risk in some species. Further tests of different forms of nest predation risk (e.g., predator removal, change in nesting cover, predation
on neighbors) in diverse species are needed
to assess differential responses. Nonetheless,
when a plastic response occurs, it results in a
negative relationship (i.e., smaller clutch size
with increased predation risk) as predicted
(Table 1).
Evolved mean expression of clutch size
across populations or species shows a more
consistent negative relationship with nest predation (Slagsvold 1982a; Martin 1995; Martin et al. 2000a; Ferretti et al. 2005; Kleindorfer 2007). However, nest predation does
not explain all significant variation in clutch
size. For example, it does not appear to explain clutch size variation among cavity-nesting
birds or across latitudes, suggesting that other
factors play a stronger role (Martin 1993c;
Martin et al. 2000a). Clutch size is the most
widely studied life history trait among birds
and is clearly an important component of fitness, but with limited plastic responses in many
species, attention to other traits in experimental studies may pay bigger dividends in understanding the influence of nest predation on life
histories.
Egg Size
Egg size has received minimal attention in
terms of both plastic responses and evolved
mean expression in response to selection from
nest predation. This neglect is unfortunate be-
207
cause egg size can be significantly influenced
by maternal effects (i.e., Mousseau & Fox 1998)
through altered investment (i.e., energy per offspring) that may enhance offspring quality (Sinervo 1990; Roff 1992; but see Krist et al. 2004).
Decreased nest predation risk may be expected
to favor increased investment in offspring that
have a higher probability of surviving the nest
attempt, and one form of increased investment
is through larger eggs (see Martin et al. 2006).
Plastic responses in egg mass to different levels of nest predation risk have not been examined except by Fontaine and Martin (2006a),
who found increases in egg mass across eight
species in response to experimentally reduced
nest predation risk, as predicted. This same
set of species did not show plastic responses
in clutch size (Fontaine & Martin 2006a), indicating that egg size may be more plastic and
responsive to variation in nest predation risk
than clutch size in at least some species. Kleindorfer (2007), however, found that clutch size
changed, whereas egg size did not differ, between two populations of Geospiza fuliginosa that
differed in nest predation risk. These contrasting results emphasize that responses in egg size
can be complicated by potential tradeoffs between egg size and clutch size (Smith & Fretwell
1974; Bernardo 1996; Martin et al. 2006; Martin 2008). These differences in responses of egg
size to predation risk suggest that the tradeoff between parental investment (egg size) and
offspring number (clutch size) is important to
study under different predation and environmental conditions.
The influence of nest predation on mean
egg size across species also has been ignored
and can be influenced by the egg size–clutch
size tradeoff (Martin et al. 2006). Examination
of species in four geographic regions found a
possible effect across regions, but not among
species within regions, although clutch size variation complicated results (Martin et al. 2006).
The possible influence of nest predation on the
interaction between egg size and egg number
within and across species needs considerably
more study.
208
Annals of the New York Academy of Sciences
Numbers of Broods and
Renesting Attempts
One potential influence of increased nest
predation risk is to favor reduced investment
in the current attempt (i.e., smaller clutch
sizes and/or eggs) to save energy to apportion among future attempts both within and
among seasons (Slagsvold 1982a, 1984; Major
1991; Martin 1995; also see Petrie & Møller
1991; Pöysä & Pesonen 2007). In one of the
clearest demonstrations, Zanette et al. (2006)
showed that food abundance affected overall
egg production, but variation in nest predation
explained apportionment within and among
nesting attempts in Melospiza melodia; higher
predation was associated with smaller clutches
and more nesting attempts. Tests of causes of
variation in mean number of broods or nesting attempts across species are rare, but in one
such test, nest predation explained a significant amount of variation in mean expression
of numbers of broods across diverse species
(Martin 1995). The investment in current versus future attempts within and between seasons
relative to nest predation risk remains understudied, but differential strategies may play a
particularly strong role in influencing fitness
and other life history traits (Slagsvold 1984;
Major 1991; Martin 1995; Zanette et al. 2006).
Timing of the Onset of Incubation
If incubation is initiated prior to laying
the last egg, asynchronous development and
hatching may result (Clark & Wilson 1981;
Hussell 1985). Increased nest predation, particularly during the laying period, has been
proposed to favor early onset of incubation to
reduce development time and risk of predation
(Clark & Wilson 1981; Hussell 1985; Briskie
& Sealy 1989) and allow increased crypsis and
parental defense responses (Tewksbury et al.
2002; Fontaine & Martin 2006a). Variation in
nest predation has been argued to explain plasticity within species (Hussell 1985) and mean
expression across species (Clark & Wilson 1981)
in the timing of the onset of incubation. However, tests remain rare. More detailed studies of
predation rates during laying and variation in
onset of incubation among diverse species are
needed, as well as experimental tests of whether
phenotypic plasticity in this trait covaries with
predation risk.
Incubation Activity
Increased nest predation risk can favor reduced parental activity, when predators are
visually oriented, because the activity can increase the risk of attracting predators (Skutch
1949; Martin et al. 2000a; Rastogi et al. 2006;
see earlier). This possibility can be manifested
during the incubation stage in two ways. First,
males can reduce the rate that they visit the
nest to feed their mates (Martin & Ghalambor
1999). Males might feed females away from
the nest or guard them to increase their foraging efficiency during off-bouts (Barber et al.
1998). Moreover, males reduce singing activity
when nest predation risk is greater (Fontaine
& Martin 2006b), which also may reduce the
risk of attracting predators when visiting nests.
Second, incubating females can increase the
length of on- and off-bout duration to reduce
the number of times she gets on and off the nest
(Weathers & Sullivan 1989; Conway & Martin
2000).
Experimental tests show that males exhibit
plasticity and reduce the rate they visit the nest
to feed mates with increased predation risk
(Ghalambor & Martin 2000, 2002; Fontaine
& Martin 2006a). Moreover, the steepness of
the reaction norm increases in species with
greater predation risk (Ghalambor & Martin
2002). Mean expression of male mate-feeding
rate also is negatively correlated with nest predation risk across species (Martin & Ghalambor
1999), supporting both proximate and ultimate
predictions.
More attention has been paid to female than
male behavioral responses to nest predation
risk in species in which only the female incubates (see review in Conway & Martin 2000).
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Martin & Briskie: Nest Predation and Life History Strategies
Females increase on- and/or off-bout durations
to reduce incubation activity in response to increased nest predation risk both within (e.g.,
Ferretti et al. 2005; Kleindorfer 2007; Massaro
et al. 2008; also see Weathers & Sullivan 1989)
and across (Conway & Martin 2000) species
among very different geographic locations and
systems. In the end, both male and female incubation activity seem to be quite sensitive to predation risk, although numbers of species tested
remain limited, and male behavior in particular
remains poorly studied.
Nest Attentiveness
Nest attentiveness, the percentage of time
spent on the nest incubating, can respond to selection from nest predation in two ways. First,
nest attentiveness is generally associated with
increased egg temperature that reduces length
of the incubation period and thereby reduces
length of time exposed to predators (Martin
2002; Martin et al. 2007). Second, nest attentiveness can potentially increase crypsis of the
nest and allow females to respond to potential predators with distraction displays (Montgomerie & Weatherhead 1988; Martin 1992b;
Kleindorfer & Hoi 1997). Such benefits could
favor the evolution of shared incubation, where
males and females share incubation, to increase
nest attentiveness in species with greater predation risk (Kleindorfer & Hoi 1997).
Nest attentiveness showed plastic responses
to variation in current risk; nest attentiveness
decreased with decreased risk of predation in
predator removal experiments among 12 bird
species, and this response occurred despite increased mate feeding by the males (Fontaine
& Martin 2006a). This latter result is particularly interesting, because females accepted increased food resources from males and still
spent more time off the nest obtaining food
resources for themselves when risk of nest predation was reduced. This result indicates that
females will compromise their own condition
for offspring in the face of increased predation
risk (see Fontaine & Martin 2006a).
Despite the plastic responses in nest attentiveness in the preceding predator removal experiment, nest attentiveness was not related to
nest predation rates across species in several different studies and systems, whereas incubation
activity was related to predation risk (Conway &
Martin 2000; Martin 2002; Martin et al. 2007).
Similarly, experimental removal of predators
yielded changes in incubation activity through
changes in length of on- and off-bouts but did
not affect nest attentiveness in a New Zealand
bird (Massaro et al. 2008). Incubation activity
through on- and off-bout durations is responsive to predation risk both within and across
species (see earlier), but changes in activity do
not necessarily affect attentiveness; birds with
20-min on-bouts and 20-min off-bouts have
the same attentiveness as a bird with 40-min
on- and 40-min off-bouts (50% attentiveness
in both cases), whereas activity is much lower
in the latter case. Activity through bout durations seems to be more responsive to selection from nest predation than nest attentiveness
both within and among species, but this conclusion is based on only a few studies to date.
Parental Feeding Behavior
As with selection on parental activity during incubation (see earlier), nest predation
may favor reduced parental activity during the
nestling period through reduced trips to the
nest to feed young and/or simultaneous arrival of both parents (Skutch 1949; Sargent
1993; Martin et al. 2000a, 2000b; Ghalambor
& Martin 2001; Ferretti et al. 2005; Muchai
& duPlessis 2005; Eggers et al. 2005, 2008;
Fontaine & Martin 2006a; Massaro et al. 2008;
Peluc et al. 2008). Sensitivity of parental activity to selection by nest predation should vary
with predator type and their reliance on visual
cues for locating prey. Moreover, perception of
risk may be affected by structural complexity
and cover beyond predator type alone (Eggers
et al. 2008). For predators that are less visually
oriented (such as many snakes), selection on
parental feeding rates may be relaxed, although
210
comparisons of responses to different predator types are lacking. Nonetheless, many studies have found parents exhibiting plasticity and
reducing parental feeding rates in the face of
greater predation risk within species (e.g., Ghalambor & Martin 2001; Eggers et al. 2005,
2008; Fontaine & Martin 2006a; Massaro et al.
2008; Peluc et al. 2008). Moreover, rates at
which parents visit the nest to feed offspring
are correlated with nest predation risk across
species (Martin et al. 2000a, 2000b). Thus,
both within and among species, incubation
activity and parental feeding activity can be
quite sensitive to variation in nest predation
risk.
Reduced rates of visiting the nest to feed offspring might constrain energy for growth (see
discussion following), and one way that parents might offset this cost is by increasing the
size of food loads brought to the nest on each
visit (Martin 1996; Martin et al. 2000a). In one
of the only studies to examine such compensatory tradeoffs, Martin et al. (2000a) found evidence of compensatory changes in food load
with feeding rates across species. This potential tradeoff in parental care strategies deserves
more attention relative to predation risk, both
within and among species.
Finally, some species exhibit female-only
care of eggs, nestlings, and fledglings. Such behavior may evolve in species where nest predation risk is particularly high, as a means of reducing activity and conspicuousness of the nest
(Willis et al. 1978; Frith et al. 1997; Willis &
Oniki 1998). For example, manakins (e.g., Pipra
spp., Lepidothrix spp., Manacus spp.) have femaleonly care and commonly have high nest predation rates (see Skutch 1985; Ryder et al. 2008).
On the other hand, many other species with
female-only care do not show particularly high
nest predation. For example, in a Venezuela
study site, among 33 passerine species intensively studied, Mionectes olivaceus has female-only
care but had nest predation rates that were significantly lower than the average across species
(Martin, unpublished data). Thus the ability of
nest predation to explain female-only care in
Annals of the New York Academy of Sciences
general remains unclear, but broad comparative tests are lacking.
Development Rates and Periods
Increased risk of predation on offspring in
the nest can favor reduced exposure to risk
through evolution of shorter length of development periods (i.e., incubation and nestling periods) by faster development (Case 1978; Bosque
& Bosque 1995; Remeš & Martin 2002; Martin
2002; Ferretti et al. 2005; Roff et al. 2005; Martin et al. 2007). Shorter periods of exposure in
the nest are especially favored if predation risk
is lower after leaving the nest (Roff et al. 2005).
Shorter development periods, especially during
the embryo stage, may be achieved through selection on maternal effects (see Mousseau & Fox
1998), whereby mothers increase embryo exposure to androgens in species with greater risk
of nest predation (Schwabl et al. 2007; Martin
& Schwabl 2008). Such endocrine mechanisms
may provide an alternative to nest attentiveness
for shortening the incubation period while incurring lower energy costs to the parent (Martin & Schwabl 2008). However, selection on
endocrine mechanisms may interact with selection on nest attentiveness and its effects on
egg temperature to further affect incubation period length, although such possibilities have not
been explored. Experimental reductions in predation risk have not yielded increases in length
of incubation periods in experimental tests (i.e.,
Fontaine & Martin 2006a; Massaro et al. 2008;
also see Ferretti et al. 2005 for a nonexperimental example in a Neotropical thrush). On
the other hand, a nonsignificant trend in the
correct direction was found in a study of a
New Zealand passerine and may indicate that
more power is needed (Massaro et al. 2008).
Tests across species have found clear patterns
of shorter incubation periods associated with
increased predation risk (e.g., Bosque & Bosque
1995; Martin 2002; Martin et al. 2007). Thus,
plasticity in incubation period in response to
nest predation appears weak based on existing
Martin & Briskie: Nest Predation and Life History Strategies
studies, whereas evolutionary responses across
species appear strong.
The nestling period represents a particularly interesting stage of development relative
to nest predation risk. Greater nest predation
risk should favor faster growth and a shorter
nestling period (Bosque & Bosque 1995; Martin 1995; Remeš & Martin 2002), but nestling
growth is affected by parental feeding, which
can be constrained by nest predation risk (see
earlier). This potentially antagonistic interaction has not been examined across species.
Studies within species show that reduced
parental feeding in response to increased nest
predation risk can yield slower-growing young
that fledge at smaller sizes (Scheuerlein &
Gwinner 2006; Thomson et al. 2006). No studies that we know of show faster nestling growth
in response to increased predation risk, and
such responses may be limited by constraints
on parental feeding. At the same time, nest
predation may favor an alternative solution
whereby the development period is reduced
(i.e., the young leave the nest at an earlier
stage) under greater predation risk (Remeš &
Martin 2002; also see Bosque & Bosque 1995;
Martin 1995; Roff et al. 2005). Evidence indicates that growth rate is faster and nestling
period is shorter among populations or species
with greater risk of predation (Remeš & Martin 2002; Ferretti et al. 2005). Earlier fledging may require faster development of locomotor modules (e.g., Dial 2003a, 2003b) and/or
endothermy ability that may trade off with
other physiological or morphological components, although such tradeoffs are unexplored.
Thus, nest predation appears to favor evolution of faster growth and earlier departure, but
plastic responses may be opposite because of
opposing selection on feeding rates; resolution
of this interaction across species awaits tests.
Nestling Begging
High rates of predation are expected to favor
less conspicuous begging by nestling birds (Redondo & Castro 1992; Haskell 1994; Leech &
211
Leonard 1997; Briskie et al. 1999). Conspicuous begging can cause increased predation rates
(e.g., Redondo & Castro 1992; Haskell 1994;
Leech & Leonard 1997), which demonstrates
the potential for nest predation to exert selection on evolution of the trait. A strong correlation between begging intensity/loudness and
nest predation risk across species, controlled for
offspring age and size, provides correlative support for action of that selection (Briskie et al.
1999). However, studies of other species and of
plasticity of begging in young relative to variation in predation risk are needed. The common
occurrence of nestlings begging in response to
inappropriate stimuli, such as the approach of
a potential nest predator, also suggests the presence of tradeoffs between signal design and predation risk that warrant further study (Leonard
et al. 2005).
Nest Size and Conspicuousness
Nest predation has been proposed to favor smaller or inconspicuous nests that may
constrain clutch size (Lill 1974; Snow 1978;
Slagsvold 1982a). Nest predation rates are often, although not always, greater in the tropics (e.g., see Oniki 1979; Martin 1996; Martin
et al. 2006, 2007), and this was argued to favor smaller nests that explained small clutch
sizes in the tropics (Lill 1974; Snow 1978). Experimental studies have demonstrated an increase in nest predation with experimentally
increased nest size in a few species (Slagsvold
1982b, 1989a, 1989b; Møller 1990), providing
a basis for selection on nest size if the result is
general. To date, no study has examined variation in nest size among species relative to nest
predation rates or whether nests are relatively
smaller in the tropics than temperate zones.
Similarly, no study has examined whether nest
size changes with variation in nest predation
risk within species. Finally, no study has examined whether nest size, corrected for body size,
explains any variation in clutch size within or
among species.
212
Nest predation may influence nest structure
and conspicuousness of eggs or nests (Oniki
1985; Götmark 1993; Westmoreland & Kiltie
2007; Westmoreland 2008; Galligan & Kleindorfer 2008; Kreisinger and Albrecht 2008),
although arguments over the importance of
nest predation versus sexual selection on egg
color exist and may change with nest conspicuousness (e.g., Götmark 1992, 1993; Moreno
& Osorno 2003; Kilner 2006). Nest type and
structure appear to strongly influence predation risk. Galligan and Kleindorfer (2008) experimentally demonstrated that presence or absence of a false cup nest on top of an enclosed
nest, as typical of Acanthiza chrysorrhoa in Australia, influenced nest predation risk; predation
was reduced when a false cup was present. Auer
et al. (2007) showed that species with enclosed
(i.e., ball) nests had lower predation rates than
species with open nests in an Argentina community, leading to the question of why more
species do not show such adaptations to reduce nest predation risk. Nest size, shape, and
conspicuousness have been considered relative
to habitat selection (see Oniki 1985; Martin
1992a, 1993b, 1998), but studies relative to
nest predation risk remain rare. More focused
study on nest type evolution relative to nest
predation is needed. Nest type (cavity, niche,
enclosed, covered, open) clearly may affect nest
predation risk (Martin & Li 1992; Martin 1995;
Sieving 1992; Auer et al. 2007; Fontaine et al.
2007; Kreisinger & Albrecht 2008), and many
of the traits discussed here are likely to coevolve with evolution of nest design. Moreover,
the interaction between nest type and nest predation could even influence sexual dichromatism, where greater risk of nest predation may
favor more cryptic color in both males and females to reduce attracting nest predators (Martin & Badyaev 1996). The interaction and coevolution of traits in the face of the influence of
nest type and conspicuousness on nest predation variation remains an understudied aspect
deserving of much greater attention.
Current evidence suggests that nest predation can play an important role in a wide di-
Annals of the New York Academy of Sciences
versity of life history traits from parental care
behavior to reproductive effort to developmental strategies to nest size. Often this evidence
is based on a limited number of studies and
species, and the generality of responses remains
open. Plasticity and variation in the slopes of
reaction norms among species remains poorly
studied but can provide an important avenue
for future understanding of the role of nest
predation in shaping the ecological and evolutionary responses of both mean expression
and plasticity in species. Finally, the coevolution of traits and their interacting influence on
nest predation has been little considered both
theoretically and empirically and could provide
a rich avenue of future work.
Acknowledgments
We thank Dan Barton, Yi-ru Cheng, T.
Mousseau, and C. Schlichting for helpful comments on an early draft of the manuscript. Work
by TEM has been supported by National Science Foundation grants (DEB-9981527, DEB0543178), the United States Geological Survey
Climate Change Research Program, and the
National Research Initiative of the U.S. Department of Agriculture Cooperative State Research, Education and Extension Service, grant
number 2005-02817. Work by JVB was supported by the University of Canterbury and
Brian Mason Trust.
Conflicts of Interest
The authors declare no conflicts of interest.
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