Differential physiological responses to prey availability by the great egret and white ibis
The Journal of Wildlife Management; DOI: 10.1002/jwmg.445
Differential Physiological Responses to PreyAvailability by the Great Egret and White Ibis
GARTH HERRING,1,2 Department of Biological Sciences, Florida Atlantic University, 777 Glades Road, Boca Raton, FL 33431, USA
DALE E. GAWLIK, Department of Biological Sciences, Florida Atlantic University, 777 Glades Road, Boca Raton, FL 33431, USA
ABSTRACT In long-lived species, the balance between the beneﬁts of reproduction and the costs fromreduced survival or productivity is particularly challenging in dynamic environments like wetlands, wherefood levels vary greatly year to year. Some wetland species exhibit changes in reproductive strategies inresponse to food availability but whether physiological responses function in a similar manner is unclear. Wecompared the pre-breeding physiological responses (fecal corticosterone [FCORT], heat shock protein 60[HSP60], and mass) of 2 species of wading birds with contrasting foraging strategies (great egret [Ardea alba],an exploiter, and white ibis [Eudocimus albus], a searcher) during years with contrasting levels of preyavailability. Both species were in good physiological condition, with low levels of HSP60 and FCORT,during a year with high prey availability (2006). In a contrasting year with lesser prey availability (2007),HSP60 and FCORT concentrations indicated that ibis physiological condition was reduced, whereas egretsshowed little change. Egrets and male ibis increased body mass, whereas female ibis decreased mass, in theyear with low prey availability. Although poorly understood, we hypothesize that the differential responsebetween female ibis and the others is associated with differential investment strategies based on long-termcosts of reproduction. Model results identiﬁed prey availability and the 2-week water recession rate as theprimary habitat variables that were associated with the physiological condition of white ibises, whereas greategret physiological condition was inﬂuenced mostly by 2-week water recession rate. Our results support thehypothesis that prey availability and hydrological factors play crucial roles in regulating populations of wadingbirds in the Florida Everglades. The results of this study show a more complete pathway by which hydrologicpatterns affect wading birds, and it suggests that ibis are more sensitive to habitat conditions than are egrets.
This information can be used to reﬁne species models designed to evaluate water management scenarios andwill improve our ability to manage and restore wetland ecosystems ß 2012 The Wildlife Society.
KEY WORDS Ardea alba, corticosterone, Eudocimus albus, Florida Everglades, heat shock proteins, nesting ecology,pre-breeding.
Reproduction is a costly undertaking for most species, with
birds to their local environment should reﬂect local condi-
those individuals that reproduce more than once having to
tions and their inherent ability to forage within those
balance the cost of reproduction with surviving to future
reproduction attempts (Ricklefs 1977, Partridge and Harvey
One way birds respond to unpredictable food availability
1988, Roff 1992, Golet and Irons 1999). One mechanism in
during the reproductive period is to use different forag-
birds that increases productivity while minimizing risk of
ing strategies that allow them to maximize food intake
mortality, is improving pre-breeding physiological condition
while potentially minimizing competition. Wading birds
prior to egg laying, thereby increasing the likelihood of
have been categorized relative to a foraging strategy contin-
successful breeding, (i.e., capital breeders; Drent and Daan
uum bounded by searchers and exploiters (Gawlik 2002),
1980). The value of this mechanism depends on the amount
analogous to the cream-skimmer–crumb-picker continuum
of food that is available in the environment, the ability of the
(Brown et al. 1997). Searcher species (e.g., white ibis
bird to access it, and the demands of the pre-breeding period.
[Eudocimus albus], wood stork [Mycteria americana]) select
If birds are able to recognize changes in habitat conditions,
high quality foraging patches and abandon those sites when
then their life-history traits are predicted to track an optimal
patch quality declines (e.g., prey densities reach a critical
reaction norm with regard to the particular environment
giving up density; Gawlik 2002). Exploiter species (e.g.,
encountered (Stearns 1992, Kawecki and Stearns 1993,
great egret [Ardea alba], great blue heron [A. herodias]) follow
Kisdi et al. 1998). Accordingly, the observed responses of
a different rule in regards to when they should leave a patch,leaving when patch quality is lower and after the searchers
Received: 12 December 2011; Accepted: 30 May 2012
have abandoned the patch (Gawlik 2002). These foragingstrategies evolved over long periods of time under natural
wetland conditions; the ability of birds to predict conditions
Present address: U.S. Geological Survey, Forest and Rangeland
may be more difﬁcult when wetlands become highly altered
Ecosystem Science, 25 Center, 3200 SW Jefferson Way, Corvallis,OR 97331, USA.
Herring and Gawlik Ibis and Egret Pre-Breeding Physiology
One method for understanding the role that food avail-
iological condition might play an inﬂuential role in setting up
ability plays in avian ecology is to examine the physiological
these responses observed later in the reproductive cycle.
condition of birds. Physiological biomarkers have the poten-
Our objectives were to compare the physiological responses
tial to respond directly and predictably to ecological con-
of pre-breeding great egrets and white ibises to landscape-
ditions, making them useful for quantifying how wading
level prey availability and the hydrologic variables that
birds respond to ﬂuctuating resource levels, particularly in
inﬂuence foraging conditions in the Florida Everglades.
highly stochastic ecosystems (Herring et al. 2011). Studies
We focused on the great egret and white ibis because they
of physiological responses can identify the mechanisms
have different foraging strategies and have shown different
by which 1 foraging strategy becomes more beneﬁcial
trends in nest numbers; great egret increased steadily during
than another under particular environmental conditions.
the 1990s, whereas the white ibis declined or remained stable
Further, understanding these physiological responses during
(Crozier and Gawlik 2003a). White ibises are more restrict-
the pre-breeding period may provide a basis for understand-
ed in their use of habitats than are great egrets (Gawlik 2002,
ing subsequent species-speciﬁc differences in reproductive
Beerens et al. 2011); therefore we expected that the physio-
logical condition of white ibises would also be more restricted
One physiological biomarker is the hormone corticoste-
by habitat conditions than would that of great egrets. We
rone, which serves as a physiological signal to modify behav-
hypothesized that during good habitat conditions (e.g., hy-
ior and metabolism in response to potentially adverse change.
drologic conditions that produce predictable patches of con-
Corticosterone is released into the blood stream via the
centrated prey), great egrets and white ibises would be in
adrenocortical tissue when birds become stressed (e.g., low
good pre-breeding physiological condition. However, during
food availability) inducing a response, and allowing them to
poor habitat conditions (hydrologic conditions that fail to
overcome the short-term deﬁciency (Astheimer et al. 1992,
produce predictable patches of concentrated prey), we
Wingﬁeld 1994). Increased corticosterone levels in birds
expected white ibises to be in poorer physiological condition
have been correlated with food shortages (Kitaysky et al.
than great egrets. We used measures of physiological condi-
2003, Herring et al. 2011). Corticosterone can be measured
tion that we expected would represent a temporal continuum
either directly from the blood stream or excreta, although
of responses from the short and medium term (FCORT
fecal corticosterone (FCORT) metabolite levels are less than
metabolites; Wasser et al. 2000, Herring et al. 2011) to long
circulating levels (Wasser et al. 2000) because of rapid and
term (heat shock protein 60 [HSP60]; Sørensen et al. 2003,
extensive metabolization before excretion.
Toma´s et al. 2004, Herring et al. 2011). We also examined
An alternative but less utilized group of physiological
changes in body mass (a common measure of body condition;
parameters for measuring nutritional condition are the stress
Ankney and MacInnes 1978, Afton and Ankney 1991) in
proteins, which function as molecular chaperones for pro-
egrets and ibises throughout the pre-breeding stage.
teins within cells (Linquist 1986, Bierkens 2000). Duringperiods of increased stress, the molecular chaperone role isampliﬁed to minimize cell protein damage (Locke and Noble1995, Ra˚berg et al. 1998). Their delayed response relative toplasma corticosterone (Burel et al. 1992) suggests that theybetter indicate chronic long-term stress (Martı´nez-Padilla
et al. 2004, Toma´s et al. 2004) and should be independent ofcapture stress. In many species and taxa, stress proteins are
The Florida Everglades is a large subtropical oligotrophic
induced in response to a variety of stressors including heavy
wetland in southern Florida with pronounced annual wet and
metals (Werner and Nagel 1997, Martı´nez et al. 2001),
dry seasons (Obeysekera et al. 1999). The dry season, when
nutritional stress (Merino et al. 2002), food limitation
most wading birds reproduce, is typically from November
(Herring et al. 2011), and others (see Herring and Gawlik
until May but can vary slightly between years. Over half
of the spatial extent of the Everglades has been lost to
In the Florida Everglades, environmental conditions, such
agriculture and urban development. The hydrologic
as water depth, recession rate, and landscape-level prey
patterns of remnant areas were greatly altered, thus changing
availability are known to inﬂuence breeding success and
the timing, magnitude, and predictability of seasonal
wading bird foraging (Frederick and Collopy 1989,
prey concentration events that are critical to wading bird
Gawlik 2002, Herring et al. 2010). Gawlik (2002) proposed
reproduction (Ogden 1994). We conducted our study in
that species-speciﬁc differences in foraging strategies could
the 3 Water Conservations Areas (WCAs 1–3: 57,951,
account for species-speciﬁc population trends under the same
54,390, and 236,984 ha, respectively) that comprise the
environmental conditions, although he did not identify a
northern Everglades. Because we captured wading birds
mechanistic pathway of the effects. Most recently, Herring
early in the dry season, our capture sites were restricted to
et al. (2010, 2011) found that differences in nesting success
the short hydroperiod portions of the WCAs, where prey
and physiological condition observed during the breeding
ﬁrst become concentrated and available to wading birds.
season were linked in part to species-speciﬁc foraging strate-
The study area was bounded to the north by 26.68408,
gies (searchers vs. exploiters) and prey availability across the
the east by À80.22178, the west by À80.85608, and the
landscape. As a result, we expected adult pre-breeding phys-
We recorded tarsus length (middle of midtarsal joint to
the end of tarso-metatarsus), wing chord, wing ﬂattened,
exposed culmen length, bill depth, and mass for both
Hydrologic conditions in the Florida Everglades during the
species, and curved bill length for white ibis only. We
2006 dry season were near optimal for wading bird nesting as
recorded all measurements to the nearest 1 mm using
suggested by Gawlik (2002). Water depths were above aver-
calipers or a wing ruler, except mass, which we measured
age at the start of the dry season and then receded unhin-
to the nearest 5 g using a spring scale. We captured all
dered by signiﬁcant water level reversals, which result in the
birds during the morning (0600 hours to 1000 hours). We
redistribution of concentrated prey and diminish accessible
banded all birds with uniquely numbered United States
foraging patches because of increased water depths (Herring
Geological Survey bands and attached radio transmitters
et al. 2011). This stable, protracted recession in 2006 fostered
to all birds for a related study examining habitat selection
comparatively elevated prey densities (Herring et al. 2010,
and nest survival of egrets and ibises (Herring et al. 2010,
2011) and a large number of nesting wading birds (Cook and
Beerens et al. 2011). We sexed all birds later using
Call 2006). The widespread recession and succeeding abnor-
DNA analysis (Zoogen Services Inc., Davis, CA; Herring
mally delayed wet season of 2006 produced unusually low
water levels during the 2006 wet season, and culminated inan ofﬁcial drought during the 2007 dry season (Herring et al.
2010). The 2007 dry season was parallel to that of 2006, with
We homogenized thawed fecal samples and divided them
few hydrological reversals and a moderately continuous re-
into 2 equal 1-ml wet portions, which we dried using a
cession; however, water depths were lower, hydroperiods
Labconco CentriVap Concentro (Labconco, Kansas City,
were shorter, and mean prey density and biomass were
MO). We mixed dried samples (approx. 0.25 g) with 5 ml of
relatively low (Herring et al. 2010, 2011). Concurrent studies
95% ethanol and vortexed for 30 minutes. After centrifuga-
on the physiological conditions of egret and ibis nestlings
tion (15 min, 2,500g) we transferred the supernatant to a
during these same 2 years found that both species responded
new vial, and then evaporated it under a stream of nitrogen
negatively to the decreased habitat conditions in 2007, but
gas. We resuspended CORT metabolites in diluted extrac-
the effect was greater for ibis (Herring 2008, Herring et al.
tion buffer and measured them using the Correlate-EIATM
2010). Based on the fact that ibis were found to be food
Corticosterone Enzyme Immunoassay Kit (EIA; Rothschild
limited during 2007 (Herring et al. 2011), we classiﬁed 2006
et al. 2008, Herring and Gawlik 2009) following the
as a year with good habitat conditions and 2007 as a year with
manufacturer’s instructions (Assay Designs, Inc., Ann
Arbor, MI). We determined inter- and intra-assay coefﬁ-
cients of variation for FCORT internal standards to be 7%
We captured great egrets and white ibises during the pre-
and 11%, respectively, for egrets, and 8% and 9%, respec-
breeding season using either a net-gun or modiﬁed ﬂip trap
tively, for ibises. We validated EIAs for FCORT metabolites
(Herring et al. 2008a) and decoys (Crozier and Gawlik
(Herring et al. 2011). We also validated the assumption that
2003b, Heath and Frederick 2003) between 10 January
FCORT levels did not change after freezing (Herring and
and 23 March. Capture dates corresponded with the seasonal
pattern of the 2 species arriving in the Everglades in great
We washed red blood cells 3 times using phosphate-
numbers prior to the upcoming breeding season, which
buffered saline, centrifuged the red blood cells, and removed
began in late March to early April. Both species generally
the pellet after the ﬁnal wash. We mixed the red blood cell
spend the non-breeding season throughout the southeastern
pellet with 1Â extraction reagent and a protease inhibitor
United States and move slowly back to the Everglades as the
cocktail (Sigma, St. Louis, MO), placed it in a vortexer for
breeding season approaches (Heath et al. 2009, McCrimmon
5 minutes, and then sonicated it for 1 minute. We centri-
et al. 2011). During 2006 and 2007, we captured and sam-
fuged samples again (15 min, 2,500g) and removed the
pled 209 adult birds (79 great egrets [49 F, 30 M] and 130
supernatant. We measured HSP60 (HSPD1) in the super-
white ibises [67 F, 63 M]) across the entire pre-breeding
natant using EIA kits speciﬁc to just those stress proteins and
not all other HSP60 family members. We determined inter-
Upon capture of a bird, we immediately placed a hood on its
and intra-assay coefﬁcients of variation for HSP60 internal
head to minimize movement during subsequent sampling
standards to be 5% and 7%, respectively. We ran all samples
and measurements. We collected up to 1 ml of blood from
in duplicate, and used the means of duplicates in subsequent
the brachial vein using a 27.5-gauge needle and stored
analyses. We validated all EIA kits using serial dilutions and
samples in heparinized vacuutainers, placed on ice until
spike tests to determine percent recovery (Herring et al.
transport to the lab. We then extracted up to 2 ml of fecal
material directly from the cloaca of the adult using a micro-pipette. We stored fecal samples in micro centrifuge tubes
and placed them on ice. In the lab, we centrifuged (15 min,
We used the Everglades Depth Estimation Network
10,000g) blood samples, to separate plasma and red blood
(EDEN; USGS 2006) to estimate water depth and water
cells. We subsequently froze blood and fecal samples at
level recession rate at foraging sites where adults were
captured. The EDEN used a network of water level gauges
Herring and Gawlik Ibis and Egret Pre-Breeding Physiology
to produce a water surface model that, when combined
inﬂuenced the response of each physiological parameter for
with a ground elevation model, provided an estimate of
each species. We used an information-theoretic approach
water depth for the entire freshwater portion of the
(Akaike 1974, Burnham and Anderson 2002) that ranked
Greater Everglades. The EDEN calculated water level stage
competing models developed from a biological understand-
in 400-m by 400-m grid cells at daily time steps accounting
ing of wading foraging ecology and evidence from previous
for evapotranspiration, rainfall, and sheet ﬂow. The estimat-
ed water depths were accurate to within 5 cm (Liu et al.
We ran separate models for each species to understand
2009). A depth of 0 cm indicated that the water surface was
their individual physiological responses (FCORT, HSP60,
at the average ground elevation. In such cases, standing
mass) to differing habitat conditions (i.e., hydrology and
water was present in small areas within a cell.
prey availability and date within years) with sex as a covari-
To estimate recession rate and water depth at foraging
ate. We included a variable for mean prey availability for
sites, we ﬁrst used ArcGIS 9.1 (Environmental Systems
each year because food abundance is considered one of the
Research Institute, Inc., Redlands, CA) to delineate the
most inﬂuential determinants of nesting effort (Lack 1954,
EDEN grid cells within 3 km of each capture site. We
Ricklefs 1968) and it may be linked to the size of wading
assumed this area contained the habitat that birds used
bird populations in the Everglades (Kahl 1964, Kushlan
within 2 weeks prior to their capture because radio-tagged
1977, Gawlik 2002, Herring et al. 2010). We included
birds regularly returned to within about 3 km of the
standardized date to better understand the physiological
capture site for the subsequent several days. We extracted
condition changes over the weeks leading up to reproduc-
daily water depth values for the 7 and 14 days preceding
tion. We included measurements of the 1-week and 2-week
a bird’s capture for all cells within the foraging area, and
mean water depth (depth) and the quadratic forms of water
used the mean depth and change in depth over each period
depth (depth þ depth2) 1 week and 2 weeks before we made
as the measures of water depth and recession rate, respec-
an estimate of physiological condition because water depth
tively. Positive recession rates indicate decreasing water
can limit foraging (Kushlan 1976, Gawlik 2002). We also
included models with the 1-week and 2-week mean reces-sion rate (recession) and the quadratic form of recession rate
(recession þ recession2) 1 week and 2 weeks before we made
We measured the biomass of wading bird prey that was
an estimate of physiological condition because recession rate
available to wading birds across the ecosystem in 2006
is a determinant of wading bird nesting success (Frederick
and 2007 in a concurrent study (see Pierce and Gawlik
and Collopy 1989, Herring et al. 2010) and distributions in
 for details on sampling design). We estimated prey
the Everglades (Bancroft et al. 2002, Russell et al. 2002,
availability as the mean biomass of all prey (ﬁshes and macro-
Beerens et al. 2011). We included the sex of a bird in the
invertebrates) captured during the period of our adult trap-
models as a covariate to account for potential differences in
ping and sampling. Our measure of prey biomass was an
acceptable surrogate for prey availability because we obtained
In the models of mass, we also included an index of
our samples from shallow water with an open habitat struc-
body size as a covariate to account for some of the variance
ture, 2 factors that make prey highly vulnerable to capture by
in the analysis associated with structural size differences.
birds (Gawlik 2002). Thus, density was the primary deter-
The body-size index consisted of the standardized scores
minant of availability in our case. We determined mean prey
of the ﬁrst principal component PC1 obtained from a
biomass during 2006 and 2007 to be 41.82 g/m2 (Æ18.78
principal component analysis on 5 morphometric measure-
SE, n ¼ 91) and 6.55 g/m2 (Æ0.72 SE, n ¼ 168), respec-
ments taken from each bird (Afton and Ankney 1991,
tively. Although we averaged these estimates across the
Esler et al. 2001). The ﬁrst principal component explained
landscape, they did demonstrate large differences between
59%, 53%, 50%, and 78% of the overall variation among
years, as indicated by non-overlapping 95% conﬁdence inter-
morphometric measurements for female and male egrets
vals (Gawlik et al. 2008), and we found them to be similar to
and ibises, respectively. Global models included all main
differences from an independent measure of prey density at
effects, excluding the body size covariate, and their
more localized sites during the same years (Herring et al.
2010, Beerens et al. 2011). Florida Atlantic University
We used Akaike’s Information Criterion values adjusted
Institutional Animal Care and Use Committee (Protocol
for small samples sizes (AICc) in all models (Burnham and
A0534) approved the research techniques, and we conducted
Anderson 2002). We calculated differences in AICc (Di) and
the research under United States Fish and Wildlife Service
Akaike weights (wi). We considered competing models with
Research Permit 23354 and Florida Fish and Wildlife
2 to be equally plausible and models with
Conservation Commission Scientiﬁc Research Permit
4 to have less support (Burnham and Anderson
2002). To assess the relative inﬂuence of each parameter, wealso calculated their parameter weights by summing Akaike
weights across all models that included each variable. We
We used Proc Mixed in SAS (SAS Institute, Inc., Cary,
calculated the model-averaged parameter estimates and their
NC), specifying the maximum likelihood variance estimator
standard errors using the full set of models (Burnham and
(Littell et al. 1996) to determine which habitat variables most
contained the variables for the 2-week recession rate and2-week depth (w ¼
only the 2-week recession rate was 1.6 and 1.8 times more
Three plausible models explained FCORT metabolite levels
likely than the next 2 models (Table 1). Models containing
in pre-breeding great egrets. The ﬁrst model contained only
the 2-week recession rate had a combined AICc weight of
0.67, with little evidence for effects of 2-week depth (0.26),
second model contained the variables for 2-week recession
sex (0.22), prey availability (0.15), date (0.06), 1-week reces-
sion rate (0.03), or 1-week water depth (0.03). All of the
Table 1. Akaike’s Information Criterion (adjusted for small sample sizes; AICc) model selection for adult great egret and white ibis fecal corticosterone(FCORT), heat shock protein 60 (HSP60), and mass. Samples were collected in Water Conservation Areas 2A, 3A, and the Arthur R. Marshall LoxahatcheeNational Wildlife Refuge between 10 January and 23 March in both 2006 and 2007. Models presented only include those that were within 3 AICc units of the topmodels (DAIC ¼
Sex, date, 2-week recession, prey availability
Sex, date, 2-week depth, prey availability, PC1e
Sex, date, 2-week depth, prey availability, sex Â prey availability, PC1
Sex, 2-week recession, prey availability, PC1
Sex, date, 2-week depth, 2-week recession, prey availability, PC1
Sex, date, 2-week recession, prey availability, PC1
Sex, date, 1-week depth, prey availability, PC1
2-Week depth, 2-week recession, prey availability
Date, 2-week recession, prey availability
Sex, 2-week depth, 2-week recession, prey availability
Sex, date, 2-week recession, prey availability
Sex, date, 2-week depth, prey availability
Sex, 2-week depth, 2-week recession, prey availability
Sex, date, 2-week recession, prey availability, sex Â prey availability, PC1
Sex, date, 2-week depth, prey availability, sex Â prey availability, PC1
Sex, date, 1-week recession, prey availability, sex Â prey availability, PC1
Sex, date, 1-week depth, prey availability, sex Â prey availability, PC1
Sex, 1-week depth, prey availability, sex Â prey availability, PC1
Sex, 2-week recession, prey availability, sex Â prey availability, PC1
Sex, 2-week depth, prey availability, sex Â prey availability, PC1
Sex, 1-week recession, prey availability, sex Â prey availability, PC1
Sex, date, 2-week depth, 2-week recession, prey availability, sex Â prey availability, PC1
a Number of estimated parameters in the model including the variance plus the intercept.
b Second-order Akaike’s Information Criterion (AICc).
c The difference in the value between AICc of the current model and the value of the most parsimonious model.
d Likelihood of the model given the data, relative to models in the candidate set.
e First principal component for body measurements.
Herring and Gawlik Ibis and Egret Pre-Breeding Physiology
variables of inﬂuence for great egret FCORT metabolitelevels had beta coefﬁcient estimates with 95% conﬁdenceintervals that overlapped zero, suggesting none of them had alarge effect (Table 2). Great egrets had similar FCORTconcentrations between the year with high prey availabilityand the year with low prey availability (Fig. 1).
The most parsimonious model explaining differences in
HSP60 concentrations in pre-breeding great egrets includedsex, date, and the 2-week recession rate (w ¼
No other models of great egret HSP60 concentrations werecompetitive (Table 1). The weight of the evidence suggestedthat the top model was 3.4 and 7.7 times more likely toexplain HSP60 levels than the next 2 models (Table 1).
Parameter likelihoods showed that the most inﬂuential var-iables were 2-week recession (0.88), sex (0.77), and date
Table 2. Variable weights and weighted parameter estimates Æ standarderror (SE) from general linear mixed models evaluating the response of greategret and white ibis fecal corticosterone metabolites (FCORT), heat shockprotein 60 (HSP60), and mass in the Everglades, 2006–2007. Explanatoryvariables were included if variable weight exceeded 0.10; variables with thegreatest relative support have variable weights close to 1.0.
Figure 1. Model-averaged least-square mean estimates of great egret and
white ibis corticosterone metabolites (FCORT), heat shock protein 60
(HSP60), and mass controlling for structural size during a year with elevated
(2006; light bar) and low (2007; dark bar) prey availability in the Everglades.
(0.70), with less inﬂuence from prey availability (0.31) and
2-week water depth (0.24), and little effect from 1-week
recession rate (0.02) or 1-week water depth (0.00). Great
egret HSP60 concentrations decreased by 4.6 ng/ml with
each 1-cm increase in recession rate, were on average 1.3 ng/
ml greater in females, and decreased by 0.11 ng/ml with each
advancing day of the pre-breeding season (Table 2). Great
egrets had similar HSP60 concentrations between the year
with high prey availability and the year with low prey avail-
The most parsimonious of 5 competitive models predicting
mass contained the variables sex, date, 2-week depth, and
receiving support (<2.0 DAICc; Table 1). Of those compet-
sex, date, 2-week depth, and prey availability was 2.3 times
itive models, the best model (1.7 and 1.8 times more likely
more likely than the next competitive model (Table 1). The
than the next 2 models) contained the variables for sex, date,
other plausible models also included a term for 2-week
prey availability, 2-week recession rate, and the interaction of
recession rate. Parameter likelihood values suggested great
sex Â prey availability (Table 1). Parameter likelihood
egret mass was most inﬂuenced by sex (0.97), prey availability
values suggested white ibis mass was most inﬂuenced
(0.84), date (0.63), 2-week water depth (0.57), and 2-week
by sex (0.98), prey availability (0.98), the interaction of
recession rate (0.34). However, the beta coefﬁcient 95%
sex Â prey availability (0.98), and date (0.60), and to a lesser
conﬁdence intervals for the 2-week water depth and 2-
extent by the 2-week recession rate (0.43). We found even
week recession rate overlapped zero indicating a weak effect
less support for 2-week water depth (0.28), 1-week water
from these variables, and suggesting that mass was mostly
depth (0.26), and 1-week recession rate (0.17; Table 2). The
inﬂuenced by sex and prey availability. We found little
beta coefﬁcient 95% conﬁdence intervals for date overlapped
support for the 1-week recession rate (0.11), and 1-week
zero indicating a weak effect and suggesting that mass was
water depth (0.06; Table 2). Great egret mass was greater in
most inﬂuenced by sex and prey availability. The supported
males than females on average by 48 g, increased by 1.4 g/
interaction of sex Â prey availability showed that in response
day during the pre-breeding stage, and was greater during
to decreasing prey availability, females decreased their mass
the year with low prey availability on average by 69 g
by 51 g, whereas males increased their mass by 72 g (Table 2,
Fig. 1). On average males were 63 g heavier than females(Table 2, Fig. 1).
White IbisThe model selection process identiﬁed 3 competitive models
to explain FCORT metabolites levels in pre-breeding white
The physiological condition of great egrets was inﬂuenced
ibises; the best model included the 2-week recession rate and
less consistently by low prey availability than was the physi-
ological condition of white ibises. We found strong support
and 2.5 times more likely than the next 2 competitive models
for the effects of sex on differences in mass and HSP60 in
(Table 1). The other 2 competitive models contained vari-
ibises. Of the landscape variables, we also found strong
ables similar to those in the top model with the addition of
support for the inﬂuence of prey availability on white ibis
sex and 1-week recession rate (Table 1). Parameter likeli-
FCORT and HSP60 concentrations (low prey availability
hood values suggested that white ibis FCORT metabolite
increased concentrations), and mass. We also found moder-
levels were most inﬂuenced by prey availability (0.77) and
ate support for the inﬂuence of the 2-week recession rate on
2-week recession rate (0.49), with moderate support for sex
ibis FCORT and SP60 concentrations, and mass.
(0.39), and little support for the 2-week depth (0.21), date
In the case of great egrets, sex and date inﬂuenced both
(0.19), 1-week recession rate (0.18), and the 1-week depth
mass and HSP60, whereas prey availability inﬂuenced egret
(0.09; Table 2). However, the beta coefﬁcient 95% conﬁ-
mass. The 2-week recession rate inﬂuenced HSP60 concen-
dence intervals for the 2-week recession rate and sex both
trations (high recession rates decreased HSP60 concentra-
overlapped zero indicating a weak effect from these variables
tions) and FCORT concentrations (although the beta
and suggesting that FCORT levels were mostly inﬂuenced
coefﬁcient suggested this effect was small). Positive recession
by prey availability. White ibis FCORT levels increased
rates produce a high density of prey within local patches and
during the year with decreasing prey availability on average
move the location of available patches across the landscape
because the ecosystem has a gradual slope southward.
The model selection process identiﬁed 4 competitive mod-
Although we saw no evidence of negative effects of high
els to explain HSP60 levels in pre-breeding white ibises
recession rate over the range we observed, we would expect
(Table 1). The best model contained the variables sex, the
negative effects at a greater recession rate because the loca-
2-week recession rate, and prey availability (w ¼
tion of available patches can move too quickly and be beyond
1.5 and 1.8 times the support of the 2 next best models
an effective foraging distance from a colony, thus causing
(Table 1). Parameter likelihood values suggested white ibis
nest abandonment (Bancroft et al. 1994). Also, a rapid
adult HSP60 levels were most inﬂuenced by prey availability
recession rate may reduce prey availability by drying patches
(0.95), sex (0.68), and 2-week recession rate (0.56), with less
before birds have a chance to access their prey, thereby
support for date (0.34), 2-week water depth (0.27), and 1-
reducing prey availability at a landscape level rather than
week recession rate (0.23), and no support for 1-week mean
water depth (0.08; Table 2). Also, the beta coefﬁcient 95%
Prey availability inﬂuenced the physiological condition of
conﬁdence intervals for date overlapped zero indicating a
pre-breeding great egrets less than did recession rate based
weak effect. White ibis HSP60 level increased during the
on the model selection results. The response of adult egrets
year with low prey availability on average 6.7 ng/ml and was
to greater levels of prey availability was unexpected in the
on average 1.4 ng/ml greater in females than males (Table 2,
case of mass; lesser prey availability resulted in an increase in
mass. The greater inﬂuence of recession rate than actual prey
As with great egrets, we found considerable uncertainty in
availability suggests that recession may affect foraging
the models of white ibis mass, with 7 competitive models
patches in more ways than simply concentrating prey. We
Herring and Gawlik Ibis and Egret Pre-Breeding Physiology
speculate that an additional way in which positive recession
prey availability, so this strategy might have some long-term
rates may affect foraging birds is by improving their ability to
ﬁnd predictable feeding patches because new patches are
Great egrets have several characteristics that may allow
always formed just down the elevation gradient from existing
them to increase their body masses during years when prey
availability is low. Their long legs, broad diet, and exploiter
Great egret FCORT metabolite concentrations in both
foraging strategy allow great egrets to exploit a wide variety
sexes were similar between years, as were HSP60 levels.
of habitat conditions (e.g., water depths; Gawlik 2002,
These results suggested that egrets may not respond as
Beerens et al. 2011), thus reducing the frequency at which
acutely as do ibises to variability in prey availability.
they need to search for new foraging patches as water levels
Indeed, the physiological condition of great egrets was
change. Indeed, both species ﬂew shorter distances to forag-
most inﬂuenced by the 2-week recession rate, whereas
ing patches in the year with low prey availability (Beerens
prey availability and the 2-week recession rate were more
2008) and in doing so may have reduced the costs of foraging.
inﬂuential for white ibis physiological condition. We also
Further, although not widely reported in the literature
found differential responses between species to changes in
(McCrimmon et al. 2011), great egrets foraged nocturnally
landscape prey availability throughout the remainder of the
on numerous occasions (Herring 2008) and this foraging
breeding season for other parameters. During the low prey
strategy could improve their overall daily intake of prey
availability year, white ibises laid smaller clutches and ﬂedged
fewer chicks (Herring et al. 2010), and the physiological
This study demonstrated consistently different physiologi-
condition of those chicks was poorer (Herring 2008). Great
cal results between great egrets and white ibises to reduced
egrets maintained their clutch size, but ﬂedged fewer chicks
prey availability; ibises had greater short-term and long-term
than in a good year (Herring et al. 2010), although the
stress levels whereas egret stress levels remained similar
physiological condition of those chicks was similar to that
relative to the year with high prey availability. The extent
of chicks hatched into the good year (Herring 2008).
to which our results can be extrapolated to other species
Our data do not explain why the pattern of body mass in
along the searcher and exploiter continuum will not be clear
female ibis differed from that of male ibis and egrets, nor are
until the responses of other species to variability in land-
comparable ﬁndings available in the literature to clearly
scape-level prey availability have been examined. Comparing
understand these results. However, we believe that the
species along the searcher and exploiter continuum will
most plausible hypothesis is that the costs and beneﬁts of
improve our understanding of the generalized patterns
different reproductive approaches differ for female ibis.
within these 2 groups and potentially yield new insights
During good years, both egrets and ibises may not beneﬁt
into how sympatric species can respond differently to the
from an increase in body mass leading up to breeding,
same environmental conditions, with implications for sub-
because prey availability is high and predictable, and mini-
mizing mass reduces energetic costs. Models of foragingstrategies (McNamara and Houston 1987, Anholt and
Werner 1998) predict that animals in rich environments
The rate that water rises or falls is a parameter of high
will spend less time feeding than those in poor environments.
management importance because it can often be manipulated
Most research in this ﬁeld has focused on the response of
by managers and it has broad ecologically signiﬁcance. Water
birds to condition of low food availability (see Gosler et al.
recession rate and other variables that determine prey avail-
1995, Rogers and Reed 2003) or unpredictable food (see
ability were inﬂuential in almost every egret and ibis physio-
Pravosudov and Grubb 1997, Cuthill et al. 2000), demon-
logical model, demonstrating the fundamental importance of
strating an increase in mass or lipid reserves storage. A key
maintaining good foraging habitat throughout the period of
point that all of these studies demonstrated inadvertently
time leading up to, and through, the breeding season.
is that during good years, birds do not need to have high
Although shallow water conditions are needed to attract
mass levels. Abreu and Kacelnik (1999) experimentally dem-
wading birds to the Everglades during the early dry season,
onstrated this response in European starlings (Sturnus vul-
steady recession rates, and suitable foraging depths may act
garis), when starlings had predictable food sources they
together as a switch to initiate the physiological changes that
lost mass. However, this strategy of preparing for unpredict-
precede nesting. Recent research, consistent with our ﬁnd-
able food availability would not explain the response of
ings, demonstrated that a recession rate of 0.5 cm/day was
female ibis during the year with low prey availability nor
optimal for maximizing nest success in great egrets (Herring
why male ibis would have a different strategy under the
et al. 2010), but that lesser recession rates were acceptable
same conditions. Perhaps female ibises are minimizing
management targets for foraging wading birds (Beerens
long-term costs of reproduction to increase their likelihood
et al. 2011) if the landscape had a high biomass of prey.
of potential future reproductive success as suggested by
If prey biomass is unknown, then maintaining recession rates
theoretical models (Drent and Daan 1980). This ﬁnding
around 0.5 cm/day throughout the pre-breeding and breed-
is supported by the fact that female ibises lay fewer eggs
ing seasons is a reasonable management target in our study
during years with lesser prey availability (Herring et al.
site. Nevertheless, the greater sensitivity of white ibis than
2010). However, female ibises were more stressed as evi-
great egrets to habitat conditions may lead to different
denced by greater levels of HSP60 during the year with low
population responses, as we believe has occurred in the
Everglades. Incorporating these species-speciﬁc responses
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The Festival of Sukkot begins on Tishri 15, the fifth day after YomKippur. It is quite a drastic transition, from one of the most solemnholidays in our year to one of the most joyous. This festival is sometimes referred to as Zeman Simkhateinu , the Seasonof our Rejoicing. Sukkot lasts for seven days. The two days following thefestival are separate holidays, Shemini Atzeret and Simkhat Torah, bu
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