Behavioral Ecology Vol. 12 No. 5: 619-625
© 2001 International Society for Behavioral Ecology
Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake
a Department of Zoology, 24 Kincaid Hall, Box 351800, University of Washington, Seattle, WA 98195, USA b Alaska Biological Services Center, U.S. Geological Survey, 1011 E. Tudor Road, Anchorage, AK 99503, USA
Address correspondence to A. Kitaysky. E-mail: kitaysky{at}u.washington.edu .
Received 1 May 1999; revised 10 November 2000; accepted 9 December 2000.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Parent black-legged kittiwakes (Rissa tridactyla) and their dependent chicks respond to food shortages by increasing circulating levels of corticosterone. To examine the behavioral significance of corticosterone release, we experimentally increased levels of circulating corticosterone in parents and chicks up to the levels observed during food shortages. We found that corticosterone-implanted chicks begged more frequently than sham-implanted controls. Corticosterone-implanted chicks in broods of two begged more frequently than singletons. Parent kittiwakes then responded to the increase in corticosterone levels in their chicks by increasing chick-feeding rates. However, feeding rates were not different among corticosterone-implanted chicks in broods of two and singletons. We also found that corticosterone-implanted parents spent more time away from the nest—perhaps foraging—and less time brooding/guarding chicks than sham-implanted controls. Untreated mates of the corticosterone-implanted bird did not compensate for the change in their partner's behavior; consequently, chicks were left unattended about 20% of the time compared to 1% at the control nests. However, corticosterone-implanted parents did not decrease their chick-feeding rates. Our findings suggest two functional implications of the increased corticosterone secretion during food shortages in the black-legged kittiwake: it facilitates begging in chicks, and it affects time allocated by parents to guarding young at the nest. Thus, release of corticosterone might provide a mechanistic link between physiological condition and behavioral interactions among adults and their young.
Key words: begging, corticosterone, food stress, kittiwakes, parent-offspring conflict, Rissa tridactyla, seabirds.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Nest-dependent chicks communicate their needs by begging, and parents use this information to adjust their investment in food provisioning. Parent-offspring conflict theory predicts that chicks should be selected to solicit a greater investment from their parents than the parents have been selected to provide (Trivers, 1974
). Alternatively, signal selection theories suggest that
begging reliably conveys chick nutritional needs and that parents respond
accordingly (Godfray, 1991,
1995a,b;
Zahavi, 1987). The intensity
of chick begging increases with food deprivation (e.g.,
Cotton et al., 1996;
Iacovides and Evans, 1998;
Kilner, 1995;
Stamps, 1993), and, at least
in some species, parents provision more in response to elevated begging
(Henderson, 1975;
Leonard and Horn, 1996;
Price and Ydenberg, 1995).
Although the relationship between hunger levels and chick begging seems well
established, the causal mechanism(s) regulating parent-offspring feeding
interactions during food shortages is not established. Finding a mechanistic
link between hunger and changes in behavior is essential to assessing
theoretical models and, eventually, to better understanding the evolution of
chick-begging behavior and parental provisioning strategies.
When food resources are limiting, long-lived parent birds are expected to
allocate available resources to body maintenance rather than to reproduction
(Cody, 1966). Evidence is
accumulating that a decision of parents about the allocation of available
resources might be based on their physiological condition
(Chaurand and Weimerskirch,
1994; Ricklefs and Schew,
1994; Weimerskirch et al.,
1994). Long-lived birds can accumulate fat as energy reserves for
self-maintenance during reproduction
(Drent and Daan, 1980). As fat
reserves are depleted, parents should rely more on amino acid metabolism
(mostly from muscle protein; Cherel et al.,
1988), which is stimulated by secretion of corticosterone, a
steroid hormone released by the adrenal glands in response to stress
(Veiga et al., 1978).
In adults, increased plasma levels of corticosterone facilitate foraging
behavior, trigger irruptive migration, and mobilize stored energy resources to
fuel increased locomotory activities
(Astheimer et al., 1992;
Bray, 1993;
Wingfield et al., 1997). These
behavioral responses can improve adult survival during food shortages
(Astheimer et al., 1992).
Increased secretion of corticosterone might also change the allocation of
available resources between body maintenance and reproductive processes to
facilitate the survival of affected individuals
(Silverin, 1986;
Wingfield and Silverin, 1986;
Wingfield et al., 1997,
1998).
In contrast to adult birds, nest-bound chicks are limited in their
behavioral responses to food-related stress. A hungry chick can compete with
nest mates and increase its share of parental resources at the expense of
siblings. A hungry chick can also intensify its begging for food from a
parent, which would respond by feeding a chick more frequently. Therefore,
chick behavioral strategies during food shortages may reflect both the
selective pressure of competition between siblings and chick nutritional
requirements (but see Cotton et al.,
1996). Experimental studies have shown that in nest-bound chicks,
food shortages are associated with depleted fat reserves and an increase in
circulating levels of corticosterone
(Kitaysky et al., 1999a;
Nunez-de la Mora et al.,
1996), though little is known about behavioral responses of chicks
to increased corticosterone.
In this study we examined the behavioral responses of black-legged
kittiwakes (Rissa tridactyla) to increased corticosterone.
Black-legged kittiwakes are colonial, cliff-nesting gulls with a maximal brood
size of three, and their chicks are nearly constantly brooded or guarded at
the nest by one of the parents (Braun and
Hunt, 1983; Roberts and Hatch,
1993). Both sexes provision young with food throughout chick
rearing; usually 5-6 weeks. Parent kittiwakes alternate their duties: while
one parent is brooding chicks, another is at sea foraging for itself and
collecting food for the young (Braun and
Hunt, 1983). Males and females do not show differences in nest
attendance or reproductive effort (Coulson
and Wooller, 1984). When a foraging parent returns to the nest, a
brooding parent leaves for the ocean. During good foraging conditions, this
synchronized behavior results in the constant presence of one of the adults at
the nest until chicks are about 34 days old
(Braun and Hunt, 1983). If food
supply is poor, however, parents start to leave their chicks unattended at an
earlier age (Roberts and Hatch,
1993). Thus, experimentally increased levels of corticosterone
might cause a kittiwake raising young chicks to increase time spent foraging
at the expense of leaving chicks unattended.
In black-legged kittiwakes, a hungry chick appears to have only two
behavioral options to improve its chances of survival
(Braun and Hunt, 1983): either
eliminate nest mates (siblicide) or intensify its begging for food. Begging
behavior is probably the only form of foraging behavior available to nestbound
chicks. Because increased levels of corticosterone facilitate foraging
behavior in adult birds, it is reasonable to hypothesize that experimentally
increased levels of corticosterone might affect begging in nest-bound
chicks.
Elsewhere we have shown that a seasonal decrease in parent kittiwake body
condition is associated with a seasonal increase in their circulating levels
of corticosterone (Kitaysky et al.,
1999b). Furthermore, the seasonal increase in baseline levels of
corticosterone is stronger among birds rearing young under poor foraging
conditions compared to those breeding under favorable foraging conditions
(Kitaysky et al., 1999b). We
also have shown that black-legged kittiwake chicks increase circulating levels
of corticosterone in response to food-related stress
(Kitaysky et al., 1999a).
However, the functional role of corticosterone release in regulating feeding
interactions of parents and their chicks has not yet been investigated.
In the present study, we experimentally increased levels of circulating corticosterone in kittiwake parents and chicks at a food-rich colony. Our objectives were to test (1) the behavioral responses of parents and chicks to the experimentally increased circulating levels of corticosterone, (2) the behavioral responses of parents to the corticosterone-induced changes in behavior of their offspring and vice versa, and (3) the behavioral responses of intact parents to the corticosterone-induced changes in behavior of their mates.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Study area
We carried out the experimental manipulations and behavioral observations from 24-27 July 1997 at a colony of seabirds on Gull Island in the lower Cook Inlet, Alaska, USA (59°35' N, 151°19' W). Foraging conditions were favorable for black-legged kittiwakes nesting at the colony in 1997 (Kitaysky et al., 1999b
;
Piatt JF et al., unpublished). The study plot consisted of a 30 x 25 m
vertical wall that contained 40 active nests of black-legged kittiwakes. We
monitored all nests at the study plot at 3-day intervals from the egg-laying
stage to fledging of chicks. We observed birds from a blind that had been
placed at the colony before kittiwakes started egg laying; at the time of the
experiment (mid-chick-rearing), birds were habituated to the presence of
observers in the blind. The blind faced the study plot at a distance of about
15 m.
Experimental design
We randomly selected a total of 24 nests for 4 experimental treatments (in
2 treatments we manipulated chicks and in 2 treatments we manipulated
parents). Each treatment had equal numbers of nests with one and two
chicks.
Experimental manipulations with chicks
At experimental nests we implanted chicks subcutaneously with a single
25-mm silastic tube (Dow Corning) filled with crystallized corticosterone. At
control nests we implanted chicks with a single 25-mm empty silastic tube.
Both chicks from broods of two were treated similarly. We individually marked
chicks using spots of colored dyes on the forehead and breast. This method has
been used in previous experimental studies of birds and does not observably
affect behavior of chicks or parents (e.g.,
Cotton et al., 1999). Estimated
mean distances between nests within a treatment were 1.1 ± 0.52 (SD)
and 1.0 ± 0.54 m for nests with corticosterone-implanted and
sham-implanted chicks, respectively. The average age of
corticosterone-implanted chicks (14.8 ± 3.71 [SD] days after hatching)
was similar to sham-implanted chicks (15 ± 3.35 days). In this study we
were not always able to distinguish between 
and ß chicks within a
brood; therefore, we could not examine behavioral differences between siblings
according to their hierarchical status.
Experimental manipulations with parents
At experimental nests we implanted one of the parents subcutaneously with
two 25-mm silastic tubes filled with crystallized corticosterone. At control
nests we implanted one of the parents with two 25-mm empty silastic tubes.
Estimated mean distances between nests within a treatment were 1.7 ±
1.38 (SD) and 2.1 ± 0.96 m for nests with corticosterone-implanted and
sham-implanted parents, respectively. Age of chicks was similar between the
experimental treatments, averaging 16.3 ± 4.08 (SD) and 16.5 ±
4.37 days old for nests with corticosterone-implanted and sham-implanted
parents, respectively. We individually marked each manipulated bird with a
unique combination of color leg bands and spots of colored dyes on the
forehead and breast.
Nest observations
We conducted observations of all nests from the blind with 8 x 40
binoculars over a 2-day period beginning 24 h after implant placement. We
watched nests continuously from 0700 to 1800 h (by two observers recording
simultaneously during 2-h shifts). We recorded begging rates of chicks, food
provisioning rates, and nest attendance of parents. We also recorded
aggression between siblings. Color markings allowed us to follow the behavior
of individual birds. We defined begging rates as the number of begs per chick
per hour at each nest. We defined begging as a chick solicitation (frequent
vertical movements of the head accompanied by a high-pitch vocalization) for
food from a parent. We considered begging series with pauses of more than 1
min as separate begging signals. We defined feeding rates as the number of
feeds per chick per hour at each nest. We considered consecutive feedings that
occurred more than 5 min apart as separate meals. We calculated the number of
trips away from the nest performed by parents as the mean number of trips per
parent per nest per 2-day study period.
After the experiment, we monitored the experimental birds until chicks fledged. In 1998 and 1999, to resight the experimental adult kittiwakes, we conducted regular surveys from 1 June to 1 July at the colony.
Effect of implantation and corticosterone analyses
In parallel to the experiment, we tested the effects of subcutaneous
corticosterone implantation on birds captured elsewhere at the colony. We
captured undisturbed birds and collected the initial baseline blood samples by
puncturing the alar vein and collecting blood in heparinized microhematocrit
100-µl tubes. After collecting the blood sample, blood flow was stopped by
application of cotton. We banded captured birds with a unique combination of
color bands, implanted them (as described above), and released adults at the
colony and placed chicks back in their nests. Three days later, birds were
recaptured and blood samples were collected (as described above). All blood
samples were collected within 0-3 min after capture and were considered to
reflect baseline levels of corticosterone
(Kitaysky et al., 1999b).
After collecting blood, we emptied hematocrit tubes into 0.5-ml vials,
which were stored on ice. Within 12 h, blood samples were centrifuged and
plasma was collected. Plasma samples were frozen at -20°C and transported
to the University of Washington for radioimmunoassay analyses. We measured
corticosterone concentrations in duplicate for each plasma sample in one assay
after extraction in dichloromethane. Before extraction, we added tritiated
corticosterone (2000 cpm) to each plasma sample to control for a loss of
corticosterone during extraction. Recovery values of the labeled steroid
following extraction ranged from 80-90% and were used to adjust assayed
concentrations of corticosterone. For a detailed description of the
radioimmunoassay analysis, see Wingfield and Farner
(1975) and Wingfield et al.
(1992).
Radioimmunoassay analysis revealed that in 15-day-old black-legged
kittiwakes, a single 25-mm silastic tube filled with crystallized
corticosterone approximately tripled the initial baseline levels of
corticosterone (Figure 1). The
heightened corticosterone levels were similar to the increase of baseline
levels of corticosterone (assayed as described above) observed in kittiwake
chicks that were reared in captivity under conditions of moderate food
deprivation (Figure 1;
Kitaysky et al., 1999a). In
parent kittiwakes, the administered amount of crystallized corticosterone (two
25-mm implants) increased baseline concentrations by about 10 ng/ml
(Figure 1) and was expected to
be metabolized within a 2- to 3-week period after implantation (Wingfield JC,
personal observations). Thus, in this study the implantation elevated levels
of corticosterone to a concentration and for a period similar to those
observed in parent kittiwakes rearing their young during food shortages
(Figure 1;
Kitaysky et al., 1999b).
|
Statistical analyses
We considered each individual nest as an independent sample unit.
Therefore, we calculated chick begging rates and food provisioning rates as
mean values per each nest. Likewise, we calculated parameters of nest
attendance by parents as mean values per each nest. Age of chick was not
significantly different among the treatments and did not significantly affect
any of the measured parameters of chick and parent behaviors, and therefore we
excluded age from further statistical analyses. We compared begging rates
among all four treatments using a two-way ANOVA (blocked by nest) with
experimental treatment and brood size as factors (followed by LSD
planned-comparison post-hoc test, which includes adjustments for multiple
tests). We compared food provisioning rates among all four treatments using
two-way ANOVA (blocked by nest) with experimental treatment and brood size as
factors (followed by LSD planned-comparison post-hoc test). We compared
proportions of time chicks were unattended by parents among all four
treatments using median tests (blocked by nest) with experimental treatments
as factor. We compared the behavioral characteristics of parents between nests
with corticosterone-implanted and sham-implanted chicks using statistical
tests for independent samples, where the experimental treatment (blocked by
nest) was used as a grouping variable. We compared the behavioral
characteristics of corticosterone-implanted and sham-implanted parents using
statistical tests for independent samples. We examined the effects of the
experimental treatments on the behavior of mates within a pair using
paired-sample comparisons (paired by nest).
If data violated the assumptions for parametric tests
(Sokal and Rohlf, 1981), we
used nonparametric equivalents. We completed computation of statistical tests
using STATISTICA.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Chick's responses to experimental treatments
Begging rates
Experimental treatments had a significant effect on chick begging rates (two-way ANOVA, F3,16 = 21.76, p <.001; Figure 2). Corticosterone-implanted chicks begged more frequently than sham-implanted controls and more than chicks in the other two treatments (post-hoc test, p <.001 for all cases between the nests with corticosterone-implanted chicks and the nests either with sham-implanted chicks, corticosterone-implanted parents, or sham-implanted parents; Figure 2). Furthermore, there was a significant interaction between treatment and brood size (F3,16 = 4.095, p =.025); corticosterone-implanted chicks begged almost twice as much in broods of two than in broods of one (post-hoc test, p <.001; Figure 2). Brood size did not affect begging in the nests with sham-implanted chicks, corticosterone-implanted parents, or sham-implanted parents (post-hoc test, p
.273 for all cases; Figure
2).
|
Aggression
We did not observe a significant amount of aggression in the nest with two
siblings. The only attacks of a smaller chick by its bigger sibling were
observed in one of the nests with sham-implanted chicks.
Parent's responses to experimental treatments
Feeding rate
Experimental treatments had a significant effect on the feeding of chicks
by the parents (two-way ANOVA, F3,16 = 6.22, p
=.005; Figure 3).
Corticosterone-implanted chicks were fed more frequently than sham-implanted
chicks (post-hoc test, p <.001), than chicks at the nests with
corticosterone-implanted parents (post-hoc test, p = 0.28), and than
chicks at the nests with sham-implanted parents (post-hoc test, p
=.016). Feeding rates were not significantly different between the nests with
corticosterone-implanted and sham-implanted parents (post-hoc test, p
=.787). Brood size did not affect feeding rate (F1,16 =
0.74, p =.402; Figure
3).
|
Nest attendance
Parents of corticosterone-implanted chicks made more trips (5.3 ±
0.95 [SE] trips per parent during a 2-day period, n = 6) away from
the nest than did parents of sham-implanted chicks (3.5 ± 0.26,
n = 6; Kruskal-Wallis test, H1 = 6.23, n
= 12, p =.013). Corticosterone-implanted parents made more trips (4.5
± 0.34 [SE] trips per 2-day period, n = 6) away from the nest
than did sham-implanted parents (3.2 ± 0.41, n = 6; ANOVA,
F1,10 = 12.31, p =.006) and their untreated mates
(3.0 ± 0.26, n = 6; paired t test, t = 6.71,
df = 5, p =.001).
Corticosterone-implanted parents spent less time (298.2 ± 27.24 [SE] min per 2-day period, n = 6) brooding/guarding chicks compared to sham-implanted parents (668.5 ± 76.85, n = 6; Kruskal-Wallis test, H1 = 8.31, n = 12, p =.004). Corticosterone-implanted parents also spent significantly less time brooding/guarding chicks compared to their untreated mates (760.0 ± 106.55, n = 6; Wilcoxon matched pairs test, Z = 1.199, n = 6, p <.05). Sham-implanted parents spent a similar amount of time brooding/guarding chicks as their untreated mates (617.33 ± 78.95, n = 6; paired t test, t =.329, df = 5, p =.756).
Chicks of corticosterone-implanted parents spent more time unattended by
either of the parents compared to chicks in all other treatments
(Figure 4; median test:
2 = 9.33, df = 3, p =.025).
|
Chick provisioning rates by corticosterone-implanted parents
The experimental increase in corticosterone levels did not alter chick
provisioning rates of cort-implanted parents, which fed their chicks at rates
(0.174 ± 0.012 [SE] feeds/h, n = 6) similar to those of
sham-implanted parents (0.167 ± 0.015, n = 6; ANOVA,
F1,10 = 0.122, p =.734). Feeding rates were also
similar between implanted and untreated mates within a pair (paired t
test, t = 0.349, df = 5, p =.741, and t = 0.466, df
= 5, p =.661, for nests with sham-implanted and
corticosterone-implanted parents, respectively).
Survival and resighting of experimental birds
All experimental and control chicks survived until fledging. All
experimental and control parents survived during a 3-week period after the
implantation and reared their chicks successfully until fledging. During the
reproductive season of 1998, five out of six corticosterone-implanted parents
failed to return to the nesting colony, whereas all other parents (except one
of the sham-implanted birds) returned to the colony. During the reproductive
season of 1999, the individuals that were missing in 1998 were also not
resighted at the colony, whereas all other birds returned to the colony. The
proportion of corticosterone-implanted parents that failed to return to the
breeding colony was significantly larger than in sham-implanted parents
(Fisher's Exact test, p =.04).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Behavioral responses to the experimental increased levels of corticosterone in chicks
Experimental studies have shown that hunger in the nest-bound chick results in increased begging (e.g., Bengtsson and Ryden, 1983
; Cotton et al.,
1996; Henderson,
1975). Furthermore, recent empirical studies showed that
blue-footed booby (Sula nebouxii) chicks release corticosterone in
response to short-term food deprivation
(Nunez-de la Mora et al.,
1996), as do food-restricted black-legged kittiwake chicks
(Kitaysky et al., 1999a). In
the present study, we have taken these observations a step further to show
that high corticosterone levels increase chick begging rates and increase
rates of food provisioning by parents.
Our study suggests that begging behavior is regulated through secretion of
corticosterone. Corticosterone secretion likely maintains and restores animal
homeostasis in response to environmental changes (e.g.,
Silverin, 1998). Our study
shows clearly that the release of corticosterone in hungry kittiwake chicks
allows them to restore depleted energy reserves by modifying the behavior of
their parents. However, such regulation is not without costs. Chronic
elevation of corticosterone is known to suppress memory and immune systems,
promote wasting of muscle tissue, and cause neuronal cell death
(Sapolsky, 1992;
Sapolsky et al., 1986). Thus,
the regulation of begging through secretion of corticosterone is likely to be
associated with benefits and costs, which must be balanced by a begging
chick.
The regulation of begging through secretion of corticosterone might
represent an evolutionarily stable signaling system as a resolution of
parent-offspring conflict in birds. Our study suggests that parent kittiwakes
probably assess the physiological condition of their chicks by monitoring
begging. In such a system, a chick can misrepresent its requirements to
acquire more food than it needs (Godfray,
1995b). Cheating may be prevented if there is a cost associated
with begging that is larger than the benefits of the extra food obtained by a
cheating chick (Godfray,
1995b). If continuous begging is associated with a prolonged
secretion of corticosterone, then a cheating chick would suffer detrimental
effects of chronically elevated levels of corticosterone. Thus, if cheating is
associated with high levels of corticosterone, exaggerated begging might be
costly, and a cheating chick may endanger its future survival. Our conclusion
hinges on the assumption that continuous begging requires continuous secretion
of corticosterone, which remains to be shown. Clearly, future studies
addressing hormonal regulation of begging and potential longterm effects of
chronic elevation of corticosterone levels in nest-dependent chicks are
needed.
In addition to effects of corticosterone, interactions between chicks
within a brood probably increase chick begging rates. In particular, we found
that corticosterone-implanted chicks in broods of two begged more frequently
than single-tons. In contrast, we did not record any aggression between
siblings in the nests with corticosterone-implanted chicks. This supports
earlier observations that competition for food between food-stressed siblings
is initially expressed by increased begging
(Muller and Smith, 1978;
Smith and Montgomerie, 1991).
In the black-legged kittiwake, Braun and Hunt
(1983) observed higher begging
rates of hungry chicks when they occurred in broods of two compared to
singletons. Similar observations were reported for some species of birds
(e.g., Harper, 1986; for
cotingas, Cotingidae), but in other species
(Cotton et al., 1996;
Kacelnik et al., 1995; for
European starling, Sturnis vulgaris) a chick tends to beg in relation
to its own condition regardless of the behavior of its nest mates. It is not
known yet how important phylogenetic constraints are in determining chick
begging strategies, and differences among different studies might reflect that
phenomenon. Nevertheless, our observations are consistent with the theoretical
prediction that the begging rate of a chick depends on its own condition and
on conditions of its nest mates (Godfray,
1995a). Thus, although high levels of corticosterone increase
begging in black-legged kittiwake chicks, further escalation of a chick's
begging probably depends on the begging levels of its sibling.
Although corticosterone-implanted chicks in broods of two begged at almost
twice the rate of singletons, parents did not feed them at twice the rate of
corticosterone-implanted singletons (mean feeding rates differed by 13%
between chicks in broods of two and singletons). In contrast to these results,
other experimental studies have shown that parental provisioning is
proportional to chick begging (e.g.,
Kacelnik et al., 1995).
However, parental ability to increase feeding rates is likely to be limited,
and it is possible that parents of all corticosterone-implanted chicks were
probably provisioning food at or near maximal rates. On the other hand, we
cannot exclude the possibility that somehow parent kittiwakes are able to
discriminate between changes in a chick's begging behavior due to the change
in its physiological condition from changes reflecting social interactions
between siblings within a brood.
Foraging conditions were favorable for kittiwakes breeding in the study
area in 1997 (Kitaysky et al.,
1999b; Piatt JF, unpublished data). Thus, we observed parental
responses to the corticosterone-induced begging of chicks in a situation when
parents could provide more food. Responses of parent kittiwakes to chick
demands might differ under less favorable foraging conditions, thereby
changing provisioning rates. If parents cannot provide food in response to
chick demands, then aggression leading to siblicide would probably occur
(Braun and Hunt, 1983). Before
reaching this point, however, begging behavior would offer some evolutionary
advantages over aggressive behavior. Begging behavior probably requires less
energy (McCarty, 1996;
Soler et al., 1999) and
entails less risk of injury than aggressive behavior.
Behavioral responses to the experimental increased levels of
corticosterone in parents
This study also suggests a physiological mechanism for the regulation of
resource allocation by adult black-legged kittiwakes during chick rearing. We
found that corticosterone-implanted parent kittiwakes performed more trips
away from the nests than did sham-implanted parents. We assumed when birds
were away from the nests, they were foraging. This assumption seems to be
reasonable (e.g., Monaghan et al.,
1996) and was justified by direct observations of chick-rearing
black-legged kittiwakes (Irons,
1998). Kitaysky et al.
(1999b) have shown that parent
kittiwakes respond to food shortages by increased secretion of corticosterone.
Moderate increases in corticosterone secretion are known to increase foraging
activities (Astheimer et al.,
1992; Wingfield et al.,
1998) and food intake
(Wingfield and Ramenofsky,
1999). Thus, we suggest that frequent trips of the
corticosterone-implanted parent kittiwakes away from the nests were probably
due to an increase in their food demands.
Our results show that in response to the experimental increase in
circulating levels of corticosterone, adult kittiwakes increased foraging at
the expense of guarding their chicks. This resulted in a considerable increase
in the amount of time that chicks were unattended and potentially vulnerable
to predation. A similar increase in the time that young kittiwake chicks spent
unattended during poor foraging conditions was observed by Roberts and Hatch
(1993). High corticosterone
levels also affect parental behavior in other species
(Silverin, 1986; Wingfield et
al., 1997,
1998). In contrast to other
studies of the experimentally increased corticosterone levels in chick-rearing
birds (e.g., Silverin, 1986),
our results do not demonstrate an effect of high corticosterone on the
breeding success of black-legged kittiwakes. Yet we examined the relationship
between high corticosterone and parental behavior in the context of a
food-rich colony where nonexperimental parents were not off foraging as much,
thereby protecting both their own chicks and the implanted birds' chicks from
predators. However, food shortages are likely to affect the behavior of all
birds breeding at a particular colony in a similar manner, and all affected
birds would be leaving their chicks unattended. In this manner, increased
corticosterone secretion can be an important factor determining breeding
success of black-legged kittiwakes during food shortages.
The major prediction of life-history theory is that long-lived birds should
balance survival of their current offspring with their own survival
(Linden and Møller,
1989). Current reproductive effort affects residual reproductive
value in the black-legged kittiwake (Golet
et al., 1998; Hatch et al.,
1993,
1994). Kitaysky et al.
(2000) have shown that a
decrease in food abundance causes an increase in energy expenditures of parent
kittiwakes, whereas growth rates of their chicks are not affected. An increase
in parental effort of black-legged kittiwakes results in a decrease of their
body condition (through a depletion of fat reserves), which may affect their
postreproductive survival (Golet and
Irons, 1999). A depletion of fat reserves in parent kittiwakes
results in elevation of circulating levels of corticosterone
(Kitaysky et al., 1999b),
which might affect their return rate to the breeding colony (this study). In
this study we established that the individuals with experimentally elevated
levels of corticosterone increased foraging at the expense of
brooding/guarding their chicks, but did not alter their chick provisioning
rates and could suffer a long-term effect of chronically elevated levels of
corticosterone.
|
ACKNOWLEDGEMENTS |
|---|
We thank Roman Kitaysky, Stephani Zador, Mike Shultz, and April Nielsen for their help during the experiment. We thank David West-neat, Marc Mangel, Morgan Benowitz-Frederiks, Samrrah Raouf, Ignacio Moore, and anonymous reviewers for reading the manuscript and for providing numerous useful comments. Financial support for this study was provided through EVOS Trustee Council (Restoration Projects 98163M and 99479) to J.F.P. and A.S.K., and National Science Foundation grant OPP9530826 to J.C.W. The Soldovia Native Corporation granted permissions to work on Gull Island. The experimental manipulations with birds conformed to the rules of Laboratory Animal Care and Use Protocol, University of Washington.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Astheimer, LB, Buttemer WA, Wingfield JC, 1992. Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scand 23: 355-365.
Bengtsson H, Ryden O, 1983. Parental feeding rate in relation to begging behavior in asynchronously hatched broods of the great tit Parus major. Behav Ecol Sociobiol 12: 243-251.
Braun BM, Hunt GL, 1983. Brood reduction in black-legged kittiwakes. Auk 100: 469-476.
Bray MM, 1993. Effect of ACTH and glucocorticoids on lipid metabolism in the Japanese quail, Coturnix coturnix japonica. Comp Physiol Biochem A 105: 689-696.
Chaurand T, Weimerskirch H, 1994. The regular alternation of short and long trips in the blue petrel Halobaena caerulea: a previously undescribed strategy of food provisioning in a pelagic seabird. J Anim Ecol 63: 275-282.
Cherel Y, Robin J-P, Le Maho Y, 1988. Physiology and biochemistry of long-term fasting in birds. Can J Zool 66: 159-166.
Cody ML, 1966. A general theory of clutch size. Evolution 20: 174-184.
Cotton PA, Kacelnik A, Wright J, 1996. Chick begging
as a signal: are nestlings honest? Behav Ecol
7: 178-182.
Cotton PA, Wright J, Kacelnik A, 1999. Chick begging strategies in relation to brood hierarchies and hatching asynchrony. Am Nat 153: 412-420.
Coulson JC, Wooler RD, 1984. Incubation under natural conditions in the kittiwake gull, Rissa tridactyla. Anim Behav 32: 1204-1215.
Drent RH, Daan S, 1980. The prudent parent: energetic adjustments in avian breeding. Ardea 68: 225-252.
Godfray HCJ, 1991. Signaling of need by offspring to their parents. Nature 352: 328-330.
Godfray HCJ, 1995a. Evolutionary theory of parent-offspring conflict. Nature 376: 133-138.[Medline]
Godfray HCJ, 1995b. Signaling of need between parents and young: parent-offspring conflict and sibling rivalry. Am Nat 146: 1-24.[ISI]
Golet GH, Irons DB, 1999. Raising young reduces body condition and fat stores in black-legged kittiwakes. Oecologia 120: 530-538.
Golet GH, Irons DB, Estes JA, 1998. Survival costs of chick rearing in black-legged kittiwakes. J Anim Ecol 67: 827-841.
Harper AB, 1986. The evolution of begging: sibling competition and parent-offspring conflict. Am Nat 128: 99-114.
Hatch SA, Kondratyev AY, Kondratyeva LF, 1994. Comparative demography of black-legged kittiwakes (Rissa tridactyla) in the Gulf of Alaska and Sea of Okhotsk. Bridges of the Sciences between North America and the Russian Far East. 45th Arctic Science Conference. Abstracts, book 1. Russian Academy of Sciences and American Association for the Advancement of Science. Vladivostok: Dalnauka.
Hatch SA, Roberts BD, Fadley BS, 1993. Adult survival of black-legged kittiwakes Rissa tridactyla in a Pacific colony. Ibis 135: 247-254.
Henderson BA, 1975. Role of the chick's begging behavior in the regulation of parental feeding behavior of Larus glaucescens. Condor 77: 488-492.
Iacovides S, Evans RM, 1998. Begging as graded signals of need for young in young ring-billed gulls. Anim Behav 56: 79-85.[ISI][Medline]
Irons DB, 1998. Foraging area fidelity of individual seabirds in relation to tidal cycles and flock feeding. Ecology 79: 647-655.
Kacelnik A, Cotton PA, Stirling L, Wright J, 1995. Food allocation among nestling starlings: sibling competition and the scope of parental choice. Proc R Soc Lond B 259: 259-263.
Kilner R, 1995. When do canary parents respond to nestling signals of need? Proc R Soc Lond 269: 343-348.
Kitaysky AS, Hunt GL, Flint EN, Rubega MA, Decker MB, 2000. Resource allocation in breeding seabirds: responses to fluctuations in their food supply. Mar Ecol Prog Ser 206: 283-296.
Kitaysky AS, Piatt JF, Wingfield JC, Romano M, 1999a. Stress response of black-legged kittiwake chicks in relation to dietary restrictions. J Comp Physiol B 169: 303-310.
Kitaysky AS, Wingfield JC, Piatt JF, 1999b. Dynamics of food availability, body condition and physiological stress response in breeding black-legged kittiwakes. Funct Ecol 13: 577-584.
Leonard ML, Horn AG, 1996. Provisioning rules in tree swallows. Behav Ecol Sociobiol 42: 431-436.
Linden M, Møller AP, 1989. Cost of reproduction and covariation of life history traits in birds. Trends Ecol Evol 4: 367-371.
McCarty JP, 1996. The energetic cost of begging in nestling passerines. Auk 113: 178-188.
Monaghan P, Wright PJ, Bailey MC, Uttley JD, Walton P, Burns MD, 1996. The influence of changes in food abundance on diving and surface-feeding seabirds. In: Studies of high-latitude seabirds. 4. Trophic relationships and energetics of endotherms in cold ocean systems. Occas Papers Can Wildl Serv 91: 10-19.
Muller RE, Smith DG, 1978. Parent-offspring interactions in zebra finches. Auk 95: 485-495.
Nunez-de la Mora A, Drummond H, Wingfield JC, 1996. Hormonal correlates of dominance and starvation-induced aggression in chicks of the blue-footed booby. Ethology 102: 748-761.
Price K, Ydenberg R, 1995. Begging and provisioning in broods of asynchronously-hatched yellow-headed blackbird nestlings. Behav Ecol Sociobiol 37: 201-208.
Ricklefs RE, Schew WA, 1994. Foraging stochasticity and lipid accumulation by nestling petrels. Funct Ecol 8: 159-170.
Roberts BD, Hatch SA, 1993. Behavioral ecology of black-legged kittiwakes during chick rearing in a falling colony. Condor 95: 330-342.
Sapolsky RM, 1992. Neuroendocrinology of the stress-response. In: Behavioral endocrinology (Becker JB, Breedlove SM, Crews D, eds). Boston, Massachusetts: MIT Press; 287-324.
Sapolsky RM, Krey LC, McEwen BS, 1986. The neuroendocrinology of stress and aging: the glucocorticosteroid cascade hypothesis. Endocr Rev 7: 284-301.[ISI][Medline]
Silverin B, 1986. Corticosterone binding proteins and behavioral effects of high plasma levels of corticosterone during the breeding period in the pied flycatcher. Gen Comp Endocrinol 64: 67-74.[ISI][Medline]
Silverin B, 1998. Behavioural and hormonal responses of the pied flycatcher to environmental stresses. Anim Behav 55: 1411-1420.[ISI][Medline]
Smith HG, Montgomerie R, 1991. Nestling American robins compete with siblings by begging. Behav Ecol Sociobiol 29: 397-312.
Sokal RR, Rohlf FJ, 1981. Biometry, 2nd ed. San Francisco: W.H. Freeman.
Soler M, Soler JJ, Martinez JG, Moreno J, 1999. Begging behaviour and its energetic cost in great spotted cuckoo and magpie host chicks. Can J Zool 77: 1794-1800.
Stamps J, 1993. Begging in birds. Ethology 3: 69-77.
Trivers RL, 1974. Parent-offspring conflict. Am Zool 14: 249-264.
Veiga JAS, Roselino ES, Migliorini RH, 1978. Fasting, adrenalectomy, and gluconeogenesis in the chicken and a carnivorous bird. Am J Physiol 234: R115-R121.
Weimerskirch H, Chastel O, Chaurand T, Ackerman L, Hindermeyer X, Judas J, 1994. Alternate long and short foraging trips in pelagic seabird parent. Anim Behav 47: 472-476.
Wingfield JC, Bruener C, Jacobs J, 1997. Corticosterone and behavioral responses to unpredictable events. In: Perspectives in avian endocrinology (Harvey S, Etches RJ, eds). Bristol, UK: Journal of Endocrinology Ltd; 267-278.
Wingfield JC, Farner DS, 1975. The determination of five steroids in avian plasma by radioimmunoassay and competitive protein binding. Steroids 26: 311-327.[ISI][Medline]
Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD, 1998. Ecological bases of hormone-behavior interactions: the "emergency life history stage." Am Zool 38: 191-206.
Wingfield JC, Ramenofsky M, 1999. Hormones and behavioral ecology of stress. In: Stress physiology in animals (Balm PHM, ed). Sheffield, UK: Sheffield Academic Press; 1-51.
Wingfield JC, Silverin B, 1986. Effects of corticosterone on territorial behavior of free-living male song sparrows, Melospiza melodia. Horm Behav 20: 405-417.[Medline]
Wingfield JC, Vleck CM, Moore MC, 1992. Seasonal changes of the adrenocortical response to stress in birds of Sonoran Desert. J Exp Zool 264: 419-428.[ISI][Medline]
Zahavi A, 1987. The theory of signal selection and some of its implications. In: Proceedings of the International Symposium on Biological Evolution. Bari, Italy: Adriatica Edetricia; 305-325.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  H. Wada and C. W. Breuner Transient elevation of corticosterone alters begging behavior and growth of white-crowned sparrow nestlings J. Exp. Biol., May 15, 2008; 211(10): 1696 - 1703. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Saino, C. Suffritti, R. Martinelli, D. Rubolini, and A. P. Moller Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica) Behav. Ecol., May 1, 2003; 14(3): 318 - 325. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||