Division of Comparative Physiology and Biochemistry, Society for Integrative and
Comparative Biology
Phenotypic Flexibility of Body Composition in Relation to Migratory State, Age, and Sex in
the Western Sandpiper ( Calidris mauri )
Author(s): Christopher G. Guglielmo and Tony D. Williams
Source: Physiological and Biochemical Zoology, Vol. 76, No. 1 (January/February 2003), pp. 8498
Published by: The University of Chicago Press. Sponsored by the Division of Comparative
Physiology and Biochemistry, Society for Integrative and Comparative Biology
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84
Phenotypic Flexibility of Body Composition in Relation to Migratory
State, Age, and Sex in the Western Sandpiper (Calidris mauri)
Christopher G. Guglielmo*
Tony D. Williams
Centre for Wildlife Ecology, Department of Biological
Sciences, Simon Fraser University, Burnaby, British Columbia
V5A 1S6, Canada
Accepted 10/3/02
ABSTRACT
We investigated the flexibility of body composition in relation
to seasonally variable demands for endurance flight capacity
and hyperphagia in a migratory shorebird. Migrating western
sandpipers were sampled in spring and fall while refueling at
a north temperate stopover and were compared with nonmigrating birds captured at a tropical wintering area in Panama.
Sandpipers weighed 25% more at stopover, and nearly 40% of
migratory mass increase consisted of lean body components.
Most organs and flight muscles were 10%–100% larger during
migration, and the greatest relative size increases occurred in
the digestive system (including liver). Birds preparing to initiate
spring migration from Panama deposited only fat, suggesting
that changes in lean body components take place after migration has begun, possibly through training effects. Sex did not
influence body composition. Juveniles making their first southward migration were similar to adults in structural size and
body mass but had substantially enlarged alimentary tracts.
Sandpipers appeared to deposit lean mass during stopover in
fall but not in spring. The dramatic enlargement of the digestive
system in this small species that makes short flights and fuels
frequently contrasts with the reduction of digestive components
in larger species that fuel only once or twice by making one
or two very long flights to their destination.
Introduction
Physiological systems must have the capacity to meet energetic
or material demands placed on them, but natural selection
* Corresponding author. Present address: Division of Biological Sciences, University of Montana, Missoula, Montana 59812; e-mail: cgugliel@mso.umt.edu.
Physiological and Biochemical Zoology 76(1):84–98. 2003. 䉷 2003 by The
University of Chicago. All rights reserved. 1522-2152/2003/7601-2013$15.00
should act to eliminate wasteful excess (Diamond and Hammond 1992). Phenotypic plasticity refers to variation in the
phenotype generated by an environmental factor and defined
by a reaction norm, but the resultant phenotype is usually
considered static. Phenotypic flexibility has been used to refer
to plasticity that is temporary, reversible, and repeatable
(Piersma and Lindström 1997). Flexibility of physiological phenotypes within individuals can be expected when demand functions vary through time as a result of ontogeny, shifting environmental regimes (e.g., winter cold), or behavioral decisions
(e.g., to reproduce or migrate).
Organs act as the metabolic machinery that supports maintenance metabolism, production, reproduction, and activity, so
it has been proposed that organ functional capacities may limit
sustained metabolic rate (Hammond et al. 1994; Hammond
and Diamond 1997). Variation in basal metabolic rate (BMR)
may be linked to organ size because organs have high metabolic
activities relative to other body structures (Hammond and Diamond 1997). During periods of high energetic or biosynthetic demand (e.g., lactation, cold exposure, migration, or
chick provisioning), the mass of the metabolic machinery may
increase (Hammond and Diamond 1992; Hammond et al.
1994; Koteja 1996; Piersma et al. 1996; Speakman and McQueenie 1996). Conversely, when demands decrease, such as
when migratory birds become resident at a tropical wintering
area, metabolic machinery and BMR may be reduced (Castro
et al. 1992; Piersma et al. 1996; Kersten et al. 1998).
Migratory birds are interesting models of phenotypic flexibility because they can have dramatic cyclical changes in body
composition (Jehl 1997; Piersma and Lindström 1997). Longdistance migration is a period of high sustained metabolic demand for two reasons. First, endurance flight requires a very
high rate of energy consumption that is maintained for up to
100 h (Butler and Woakes 1990; Jenni and Jenni-Eiermann
1998). Second, between bouts of flight, birds are hyperphagic
and deposit mass rapidly (Lindström 1991). The feeding rate
in refueling migrants can approach the theoretical maximum
rate of metabolizable energy intake (Lindström 1991; Klaassen
and Biebach 1994; Karasov 1996; Lindström et al. 1999).
Migrants store large amounts of fat, sometimes to a point
where lipid comprises greater than 50% of body mass (Piersma
and Gill 1998). Early studies suggested that lean body mass was
relatively stable through migration (Connell et al. 1960). However, there is now good evidence that lean body components
are not static and that variation can occur at several levels. First,
there can be an overall hypertrophy of lean body components
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Body Composition Flexibility in Sandpipers
during the migration season to provide added nonfat fuel or
muscle power (Marsh 1984; Evans et al. 1992; Lindström and
Piersma 1993). Second, catabolism of lean body components
(particularly the gut) can occur in flight as a result of fasting
and a metabolic requirement for amino acids for gluconeogenesis and anaplerotic flux, or it can occur to meet the demand
for water that is stored more abundantly in lean tissue (Klaassen
and Biebach 1994; Hume and Biebach 1996; Klaassen et al.
1997; Jenni-Eiermann and Jenni 1998; Karasov and Pinshow
1998, 2000; Battley et al. 2000). Third, body composition can
fluctuate even within a stopover event as the digestive system
is first rebuilt to allow for rapid deposition of lean and fat mass
and then, in some cases, reduced just before departure (Piersma
et al. 1993, 1999b; Battley and Piersma 1997; Jehl 1997; Piersma
1998; Piersma and Gill 1998). It is unlikely that body composition can be optimized for both high intensity endurance
exercise and hyperphagia simultaneously. A large gut may be
advantageous for maximizing fueling rate but may be unnecessary ballast during flight, and its volume could be better used
for additional fat storage (Piersma and Lindström 1997;
Piersma 1998). In fact, species that fuel only once or twice by
making one or two very long flights appear to significantly
reduce the mass of nutritional organs before flights (Piersma
1998). Whether birds that migrate in short bouts and feed
continuously along their journey have small digestive systems
is unknown.
We investigated body composition flexibility in the western
sandpiper (Calidris mauri), a long-distance migrant shorebird.
In contrast to other shorebirds that have been studied, such as
the bar-tailed godwit (Limosa lapponica; Piersma and Gill 1998),
red knot (Calidris canutus; Battley and Piersma 1997; Piersma
et al. 1999b), and great knot (Calidris tenuirostris; Battley et al.
2000), western sandpipers generally follow a short-hop migration strategy, feeding frequently as they travel between mainly
tropical wintering sites and Arctic breeding areas (Butler et al.
1996; Iverson et al. 1996). Female sandpipers are 10% larger
than males and tend to winter farther south (Wilson 1994).
Juveniles undertake their first southward migration within 8–12
wk of hatching (Wilson 1994). We tested two major hypotheses.
First, given that migrants face elevated demands for exercise
and hyperphagia, lean body components should hypertrophy
during migration. Second, as suggested by other studies
(McLandress and Raveling 1981; Carpenter et al. 1993; Klaassen
et al. 1997; Karasov and Pinshow 1998), sandpipers preparing
to initiate migration from a wintering area should grow lean
body components before or simultaneous with fat deposition.
We also investigated the effects of sex and age on body composition, looked for evidence of lean mass deposition during
stopover refueling, and used scaling and multivariate statistical
approaches to explore relationships among body components.
85
Material and Methods
Migrating western sandpipers were sampled during stopover
refueling for 2 yr (1995, 1996) at the Fraser estuary, British
Columbia, Canada (49⬚10⬘N, 123⬚05⬘W). Each spring (April
25–May 10), 15 adults of each sex were collected, and each fall
15 of each sex were taken in July (adults) and August (juveniles). Wintering (nonmigratory) and premigratory birds were
sampled at Playa el Agallito, Chitre, Panama (8⬚N, 79⬚W). We
studied only females in Panama because of permit limitations
on the total number of collections. In Panama, only second
year and older birds (adults) molt into breeding plumage, gain
mass, and prepare to migrate north by late March (O’Hara
2002). We collected 15 adult and 15 juvenile females in winter
(December 15, 1995, to January 8, 1996) and 15 females of
each age class during premigration (March 4–18, 1996). Our
intent was to study premigratory changes in adults, using the
juveniles as a within-site control group of birds experiencing
identical environmental conditions but not preparing to
migrate.
We captured sandpipers in mist nets (Avinet, Dryden, N.Y.)
under permits from the Canadian Wildlife Service and the National Institute for Renewable Resources (Panama). Protocols
conformed to the Canadian Committee for Animal Care guidelines. Birds were anaesthetized (Guglielmo et al. 1998), weighed,
and bled from a jugular incision. Culmen, tarsus, and sternum
lengths were measured with digital calipers (Ⳳ0.01 mm).
In British Columbia, birds were double wrapped in plastic
bags, packed on ice, and dissected within hours. In some cases,
the alimentary tract was measured fresh, and the remaining
organs were measured after overnight freezing. In Panama,
birds were double wrapped in plastic, frozen at ⫺20⬚C, and
transferred within 2 wk to ⫺80⬚C. Carcasses from Panama were
kept deep frozen during transport to Canada and were in excellent condition during dissection. The small intestine was
straightened to a relaxed length and measured (Ⳳ0.5 mm) on
a moistened (0.9% NaCl) plastic ruler. Large intestine and ceca
lengths were measured with digital calipers. Mesenteric fat from
the gizzard, intestines, and ceca was returned to the carcass.
The gizzard was cut open and emptied, and the intestines and
ceca were emptied by gentle squeezing, blotted, and weighed.
Heart, lung, liver, pancreas, kidney, and the pectoralis and supracoracoideus muscles were dried by lyophilization to constant
mass. Heart, liver, right pectoralis, and right supracoracoideus
were packed in preweighed filter paper envelopes (Whatman
1) and Soxhlet extracted with petroleum ether for 8 h. The
culmen, lower legs, and wings distal to carpal joint were dried
at 60⬚C. The remaining carcass was plucked, frozen, cut into
pieces, and placed in a preweighed filter paper envelope for
lyophilization and fat extraction. Where necessary, liver, heart,
and adipose tissue masses were corrected for subsamples taken
for other studies (Egeler and Williams 2000; Egeler et al. 2000;
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86 C. G. Guglielmo and T. D. Williams
Guglielmo et al. 2002a), and total pectoralis mass was estimated
as twice right pectoralis.
We analyzed lean dry masses of heart, liver, pectoralis, and
supracoracoideus and dry masses of all other body components. Intestinal and cecal wet masses were used in analyses
that included spring and fall 1995 samples because they had
been squeezed empty a second time before drying. None of the
sample distributions deviated systematically from normality
(Shapiro-Wilk test). The first principal component (PC1) from
a principal components analysis (PCA) of sternum, tarsus, and
culmen lengths was used as a measure of body structural size
(Rising and Somers 1989). In both sexes, PC1 explained 52%
of the variation, and the eigenvectors for the three variables on
PC1 were the same in the two sexes (sternum p 0.41,
tarsus p 0.67, culmen p 0.62), indicating that females are essentially enlarged versions of males. Thus, to control for the
effect of body size when comparing between sexes, we used
PC1 scores from a single PCA of all birds. For analyses within
a sex, we used PC1 scores generated for that sex.
Within each sex, we tested for season and age-related differences using ANCOVA with body size (PC1) as the covariate.
When controlling for body mass in ANCOVA, variables were
log transformed to account for allometric scaling, and partwhole correlation was eliminated by using log(body mass ⫺
component mass) as the covariate (Christians 1999). Comparisons among experimental classes were made only if class by
covariate interactions were nonsignificant at a p 0.05. Within
each sex, experimental classes to be tested in multiple comparison tests were coded by season and age (e.g., winter adult,
fall 1996 juvenile; females: n p 10 classes; males: n p 6 classes)
and were analyzed together. Comparisons were made on least
squares means generated by ANCOVA. In this univariate approach, each body component was considered separately, and
for each component, experiment-wise error rate was controlled
at a p 0.05 by Bonferroni correction, accounting for the number of preplanned comparisons (females: n p 16, adjusted
a p 0.003; males: n p 8, adjusted a p 0.006). We argue that
this achieved a balance between the probabilities of committing
both Type I and Type II errors.
For each age class, we tested for sex differences in body
component masses during spring and fall migration using both
body size (PC1) and log(body mass ⫺ component mass) as
covariates. Comparisons were only made if sex by size or sex
by mass interactions were nonsignificant. Data from 1995 and
1996 were pooled if prior within-sex analysis indicated no year
differences. Fall-migrating females from 1995 were omitted because they had extremely untypical body masses for migrants
(see “Results”). For each migration season, we also tested to
see whether sexes differed in overall body condition using
ANCOVA of body mass with body size (PC1) as the covariate.
Time series data collected from a single population are recommended for estimation of relative deposition of lean versus
fat mass (Lindström and Piersma 1993). On the time scale of
months, our study meets this requirement because (1) sandpiper body size (PC1) did not vary among seasons and sites
(see “Results”) and (2) marked birds are known to use both
the Panama and the Fraser estuary (R. W. Butler, unpublished
data). Unfortunately, western sandpipers do not arrive at and
depart from the Fraser estuary synchronously, so as an alternative we used regression of lean body mass on total fat mass
controlling for body structural size (PC1) to look for evidence
of lean mass deposition during stopover (model 2b in van der
Meer and Piersma 1994; Battley and Piersma 1997). Each group
of refueling migrants (divided by year, age, sex, and season)
was tested separately, and relative lean mass deposition was
estimated from the regression coefficient for total fat mass.
Scaling of log10 body component wet masses and lengths to
log10 fresh body mass was examined with ordinary least squares
(OLS) regression and reduced major axis (RMA) regression
(RMA software, A. J. Bohonak shareware, San Diego State University). Principal component analysis was used to investigate
relationships among body components. Using all birds (males
and females), we entered most body components into the analysis as log10 dry or log10 lean dry mass, and part-whole correlations were eliminated. Small and large intestine and ceca
were entered as log10 wet mass.
Results
The term “stage” refers to a combination of year and season
(e.g., fall 1996), and “group” refers to stage plus age and sex
(e.g., fall 1996 adult male). Unless noted, results are only described if they were statistically significant using the Bonferroni
corrections outlined in “Material and Methods.” Structural
body size (PC1) did not vary by age or stage within sexes
(female: F9, 136 p 1.1, P p 0.36; male: F9, 97 p 1.1, P p 0.34). As
expected, the culmen, tarsus, and sternum were larger in females but did not vary by stage or age within sexes (Table 1;
culmen: female, F9, 136 p 1.8, P p 0.07; male, F9, 97 p 1.4, P p
0.20; tarsus: female, F9, 136 p 1.0, P p 0.46; male, F9, 97 p 1.0,
P p 0.48; sternum: female, F9, 136 p 0.8, P p 0.58; male,
F9, 97 p 1.4, P p 0.19). Thus, within each sex, our sample populations were equivalent in physical dimensions, and fall juveniles were already fully grown by the time they reached the
Fraser estuary.
Female body mass, lean mass, and fat mass varied among
Table 1: Morphometric measurements (mm Ⳳ
SE) of male and female western sandpipers
collected for body composition analysis
Culmen
Tarsus
Sternum
Male (n p 98)
Female (n p 148)
22.66 Ⳳ .10
24.81 Ⳳ .07
23.66 Ⳳ .07
26.75 Ⳳ .08
26.69 Ⳳ .05
24.56 Ⳳ .06
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Figure 1. Female and male body mass (circles), wet lean mass (squares), and fat mass (triangles) of adult (filled symbols) and juvenile (open
symbols) western sandpipers. Values are least squares means (ⳲSE) controlling for body size (PC1) during spring (Spr), fall (Fall), winter
(Win), and premigration (Prem). Asterisks indicate Bonferroni-corrected significance between adjacent stages. Letters along the top margin
indicate significant age differences at that stage for body mass (A), wet lean mass (B), and fat mass (C). Numerals along the right margin
indicate the following significant differences for mass (M), lean mass (LM), and fat (F): 1995 spring adult versus 1996 spring adult (1); 1995
fall adult versus 1996 fall adult (2); 1996 fall adult versus winter adult (3); 1995 fall juvenile versus 1996 fall juvenile (4); 1996 fall juvenile
versus winter juvenile (5).
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88 C. G. Guglielmo and T. D. Williams
ages and stages (Fig. 1; mass: F9, 134 p 19.7, P p 0.0001; lean
dry mass: F9, 119 p 15.4, P p 0.0001; fat: F9, 120 p 7.4, P p
0.0001). Body mass, lean mass, and fat mass were lowest during
winter and increased during migration. The small sample of
adult females (n p 8 ) from fall 1995 were most similar to wintering birds. During premigration, adults increased body mass
by the deposition of fat only. This was followed by an increase
in lean mass between premigration and spring stopover. Total
body mass tended to increase during this transition as well
(P p 0.01). Hence, 40% of the mass gain from winter to spring
stopover consisted of lean body components. In Panama, adults
maintained greater lean mass than juveniles during premigration and tended to do so in winter (P p 0.006). Female juveniles had greater fresh and lean mass in fall 1996 than in fall
1995.
Body mass did not vary significantly among samples of male
migrant sandpipers (F5, 91 p 1.5 , P p 0.19), but lean and fat
mass differed in some cases (dry lean mass: F5, 88 p 4.5, P p
0.001; fat: F5, 90 p 2.9, P p 0.018; Fig. 1). In fall 1996, juveniles
were fatter than adults and, like juvenile females, had greater
lean mass than juvenile males in fall 1995.
Female Body Composition
Controlling for body structural size (PC1), we found that female body composition changed dramatically through the year
in relation to migration, and there were several age differences
(Fig. 2). In light of the unusual body composition of the adult
females collected in fall 1995, we confirmed seasonal differences
by comparing winter adults to fall 1996 migrants. There was
significant age- and stage-dependent variation in the lengths of
the small intestine (F9, 129 p 2.5, P p 0.01), large intestine
(F9, 130 p 4.4, P p 0.0001), and ceca (F9, 126 p 2.4, P p 0.02), but
the only consistent pattern was for wintering juveniles to have
shorter large intestines and ceca than juvenile migrants in fall
1995. Juveniles also had shorter small intestines than adults
during premigration, and winter juveniles tended to have
shorter small intestines than fall 1995 migrants (P p 0.005).
Much greater variability was apparent in the masses of the
alimentary tract components (wet small intestine: F9, 131 p
47.4, P p 0.0001; wet large intestine: F9, 131 p 7.7, P p 0.0001;
wet ceca: F9, 131 p 6.23, P p 0.0001; dry gizzard: F9, 131 p 12.4,
P p 0.0001). In both age classes, small intestine, large intestine,
and gizzard mass decreased during winter and increased again
by 23%–60% during migration. Pancreas and liver mass increased 70%–100% during migration (dry pancreas: F9, 131 p
42.9, P p 0.0001; lean dry liver: F9, 129 p 23.2, P p 0.0001). No
digestive organs changed in length or mass during the premigratory period in adults or juveniles.
The remaining major body components of females also varied by age and stage (dry kidney: F9, 131 p 17.2, P p 0.0001; dry
lung: F9, 131 p 4.9, P p 0.0001; lean dry heart: F9, 129 p 12.8,
P p 0.0001; lean dry pectoralis: F9, 125 p 9.9, P p 0.0001; lean
dry supracoracoideus: F9, 127 p 4.4 , P p 0.0001). Kidney, heart,
and pectoralis masses were lowest during winter and premigration and increased by 10%–30% during migration. Lung
mass showed no consistent migration-related variation. Low
supracoracoideus masses in spring and fall 1995 samples are
due to different dissection techniques of technicians. As with
digestive organs, there were no significant increases in the
masses of the kidneys or the “exercise” components in adults
during premigratory mass gain.
In both years, fall juvenile females making their first southward migration had small intestines that were much heavier
than at any other stage (33% heavier than adult migrants; Fig.
2). In fall 1996, juveniles also had heavier large intestines and
ceca than adults. Adults maintained heavier gizzards and hearts
than juveniles during the winter.
In most cases, controlling for log(body mass ⫺ component
mass) rather than PC1 did not qualitatively change our interpretation of seasonal and age-dependent variation. However,
when log(body mass ⫺ component mass) was used as a covariate, lean dry pectoralis mass no longer varied significantly
by season or age, and lean dry heart mass only differed between
adults and juveniles in winter, between premigratory and spring
1996 adults, and between 1996 fall juveniles and winter juveniles. These results indicate that flight muscle and heart mass
are more closely adjusted to body mass at all times than are
other body components.
Male Body Composition
Male body composition data were limited to spring and fall
migrants (Fig. 3). Controlling for body size (PC1), several body
components varied significantly among stages and ages (wet
small intestine: F5, 91 p 9.0, P p 0.0001; ceca: F5, 89 p 3.8, P p
0.004; lean dry liver: F5, 90 p 2.9, P p 0.017; dry lung: F5, 90 p
6.7, P p 0.0001; lean dry heart: F5, 90 p 6.1, P p 0.0001; lean
dry supracoracoideus: F5, 91 p 4.6 , P p 0.0009). Adult male
body composition was relatively constant, but small intestine
and ceca mass were lower in fall than in spring of 1996. Most
notably, in both years, small intestine mass was much greater
in fall-migrating juveniles than in adults, as was the case in
females. In fall 1996, ceca mass was greater in juveniles, and
there was a similar trend for the large intestine (P p 0.01).
Conversely, juveniles in fall 1995 tended to have smaller gizzards (P p 0.012), livers (P p 0.017), hearts (P p 0.05), and
pectoralis muscles (P p 0.032) than adults, which likely contributed to their significantly lower total lean body mass. Controlling for log(body mass ⫺ component mass) only affected
the relationships shown in Figure 3 in the following ways: (1)
small intestine mass was lower in adult fall migrants in 1996
compared with 1995; (2) in fall 1995, juveniles had smaller
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Figure 2. Organ and muscle sizes in adult (filled circles) and juvenile (open squares) female western sandpipers during spring (S), fall (F), winter
(W ), and premigration (P). Values are least squares means (ⳲSE) controlling for body size (PC1). Asterisks indicate Bonferroni-corrected
significance between adjacent stages. The letter A at the top margin indicates a significant age difference at that stage. Numerals along the right
margin indicate significant differences: 1995 spring adult versus 1996 spring adult (1); 1995 fall adult versus 1996 fall adult (2); 1996 fall adult
versus winter adult (3); 1995 fall juvenile versus 1996 fall juvenile (4); 1996 fall juvenile versus winter juvenile (5).
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90 C. G. Guglielmo and T. D. Williams
Figure 3. Organ and muscle sizes in adult (filled circles) and juvenile (open squares) male western sandpipers during spring (S) and fall (F ).
Values are least squares means (ⳲSE) controlling for body size (PC1). Asterisks indicate Bonferroni-corrected significance between adjacent
stages. The letter A at the top margin indicates a significant age difference at that stage. Numerals along the right margin indicate significant
differences: 1995 fall adult versus 1996 fall adult (2); 1995 fall juvenile versus 1996 fall juvenile (4).
gizzards than adults; (3) adult lung mass was greater in spring
1996 than spring 1995; and (4) pectoralis was smaller in fallmigrating juveniles than in fall-migrating adults in both years
of study.
Sex Differences
Controlling for body size (PC1) and log(body mass ⫺
component mass), there were no sex differences in the masses
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Body Composition Flexibility in Sandpipers
91
Table 2: Allometric (log10⫺log10) ordinary least squares (OLS) and reduced major axis (RMA)
regressions of body component lengths and wet masses versus body mass (g) for male and female
western sandpipers (n p 240)
OLS
(bI)
Length (mm):
Small intestine
Large intestine
Combined ceca
Mass (g):
Whole gut
Gizzard
Small intestine
Large intestine
Combined ceca
Pancreas
Liver
Kidney
Heart
Lung
Pectoralis
Supracoracoideus
r
2
.34a
.34a
.34a
.14
.04
.04
1.00b
1.00b
1.00b
1.00b
1.00b
NAc
.88b
.91b
.91d
.95b
1.00d
1.00d
.30
.30
.23
.05
.09
.24
.37
.32
.39
.11
.59
.21
RMA
Slope (b)
.30 Ⳳ .05
.20 Ⳳ .07*
.20 Ⳳ .07*
1.02
.91
1.20
.49
.71
1.38
1.37
.76
.67
.38
.58
.47
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
.10
.09
.14
.14**
.15*
.16*
.12**
.07*
.05**
.07**
.03**
.06**
Intercept (a)
1.89 Ⳳ .07
.95 Ⳳ .10
1.38 Ⳳ .09
⫺1.27
⫺1.46
⫺1.84
⫺2.05
⫺2.40
⫺2.63
⫺1.81
⫺1.49
⫺1.40
⫺1.02
⫺.18
⫺.87
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
.14
.13
.20
.19
.21
.23
.16
.10
.08
.10
.04
.08
r2
Slope (bR)
.14
.04
.04
.80 (.71–.89)
1.06 (.93–1.20)
1.01 (.88–1.13)
.30
.30
.23
.05
.09
.24
.41
.45
.49
.22
.62
.25
1.86
1.65
2.52
2.15
2.36
2.84
2.33
1.41
1.18
1.50
.82
1.07
(1.68–2.09)
(1.49–1.83)
(2.24–2.81)
(1.90–2.41)
(2.04–2.81)
(2.47–3.22)
(2.12–2.59)
(1.26–1.57)
(1.06–1.33)
(1.31–1.71)
(.76–.88)
(.94–1.21)
Intercept (a)
1.18 Ⳳ .06
⫺.26 Ⳳ .10
.24 Ⳳ .10
⫺2.45
⫺2.50
⫺3.71
⫺4.39
⫺4.73
⫺4.69
⫺3.67
⫺2.99
⫺2.74
⫺3.28
⫺1.05
⫺2.29
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
Ⳳ
.15
.13
.21
.19
.27
.26
.17
.11
.09
.15
.05
.10
Note. Within-species OLS regression slopes (b) are tested against literature values for interspecific slopes (bI). Values are ⳲSE,
and 95% confidence intervals are given in parentheses for RMA slope (bR). All OLS regressions were significant (P ! 0.01).
Whole gut p gizzard ⫹ small intestine ⫹ large intestine ⫹ ceca.
a
Interspecific slopes were taken from Ricklefs (1996).
b
Interspecific slopes were taken from Calder (1984).
c
Slope unavailable; tested against b p 1.00.
d
Interspecific slopes were taken from Schmidt-Nielsen (1984).
* P ! 0.05.
** P ! 0.001.
of any body components at any stage of migration in either
age class (0.13 ! P ! 0.94). Significant sex by mass interactions
precluded analysis of liver, kidney, lung, and heart mass in fallmigrating adults, but none of these organs differed between
sexes during spring migration. Juvenile gizzard mass could not
be analyzed because of a sex by body size interaction. There
was no difference in overall body condition (assessed by
ANCOVA of body mass controlling for PC1) between sexes of
either age class in spring 1995, fall 1995, or fall 1996 (0.18 !
P ! 0.95). In spring 1996, adult female sandpipers were significantly heavier for their body size than adult males (P p
0.008).
Lean Mass Deposition during Stopover
Controlling for body size (PC1), we found that there was no
relationship between residual lean mass and residual total body
fat during spring migrations (1995, 1996) in either sex
(0.08 ! P ! 0.92) or in adult females in fall 1995 (P p 0.53).
In fall 1995, lean mass was significantly related to fat mass in
adult males (F1, 12 p 10.1, P p 0.008), juvenile males (F1, 12 p
13.8, P p 0.003), and juvenile females (F1, 11 p 17.8, P p
0.001), indicating lean mass deposition rates of 42%, 41%, and
22% of total mass for the three groups, respectively. In fall
1996, lean mass deposition was indicated for adult females
(29%; F1, 11 p 7.7, P p 0.018) and adult males (46%; F1, 17 p
11.9, P p 0.003) but not for juveniles of either sex (P 1 0.35).
Within each sex, we pooled groups for which lean mass deposition was indicated and used the same method to determine
which major body components were involved. In females, there
were significant positive relationships between residual fat mass
and residual pancreas (F1, 26 p 7.6 , P p 0.01), liver (F1, 26 p 7.8,
P p 0.01), kidney (F1, 26 p 9.4, P p 0.005), and pectoralis
(F1, 26 p 23.2, P p 0.0001). In males, there were significant positive relationships between residual fat mass and residual small
intestine (F1, 46 p 28.2, P p 0.0001), gizzard (F1, 46 p 11.0, P p
0.002), pancreas (F1, 46 p 8.4, P p 0.006), liver (F1, 46 p 9.4,
P p 0.004), kidney (F1, 46 p 9.1, P p 0.004), and pectoralis
(F1, 46 p 8.5, P p 0.006). As a negative control, we tested for
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92 C. G. Guglielmo and T. D. Williams
lean mass change in premigratory adult females and found none
(F1, 11 p 1.7, P p 0.22).
Table 3: Eigenvectors of the first three principal
components of log-transformed masses of body
components of male and female western
sandpipers (n p 226)
Intraspecific Scaling and Multivariate Analysis
Body Component
PC1
PC2
PC3
All body components scaled significantly with fresh body mass
(Table 2). Except for the whole gut and its major components
(gizzard and small intestine), OLS regression slopes (b; or scaling exponents) generally differed from those found in interspecific studies that have also used OLS regression. As would
be expected, RMA regression slopes were much higher than
OLS regression slopes. In particular, RMA regression indicated
that, except for pectoralis and supracoracoideus muscles, body
components became disproportionately large with increasing
mass, and this was especially true for digestive organs. Across
the entire sample of males and females, only the wet masses
of pectoralis, supracoracoideus, and lung were strongly positively related to body size as measured by PC1 (pectoralis:
r 2 p 0.27, P p 0.001; supracoracoideus: r 2 p 0.28, P p 0.001;
lung: r 2 p 0.13, P p 0.001).
The first three principal component axes explained 62% of
the variation in body component masses (PC1: 35%; PC2: 16%;
PC3: 11%; Table 3). All variables loaded positively on the first
principal component axis, which reflected absolute component
mass. The second principal component axis mainly reflected
differences in residual variation related to the digestive system,
including liver (loading negatively) and components related to
exercise performance (loading positively). The kidneys were not
clearly segregated into either the digestive or exercise category,
possibly reflecting their important role in both aspects of metabolism. The third principal component axis was difficult to
interpret, but residual variation in lipid masses all loaded
strongly negatively, indicating that low PC3 scores may be associated with being fat.
We used a modification of the biplot technique (Gabriel
1971; Piersma et al. 1996, 1999b) to visualize relationships
among body components. Gabriel (1971) developed the
method with a two-dimensional plane but encouraged the extension to three-dimensional representations, provided they
could be accurately produced. For this analysis, the eigenvectors
for the first three principal components of variable were plotted,
and vectors from the origin (0, 0, 0) were drawn to each point.
The length and proximity of these vectors in space is an indication of the strength of the relationships among variables
and were examined by graphical rotation of the plots (Fig. 4a,
4b). Along the PC2 axis, segregation between “exercise” and
“digestive” components (positive and negative PC2 values, respectively) is readily apparent (Fig. 4a). Adding PC3 indicated
that large intestine and ceca were most closely related to each
other, as were (1) liver and pancreas, (2) heart and lung, (3)
gizzard and small intestine, and (4) pectoralis, supracoracoideus, and the remaining carcass.
Gizzard
Small intestine
Large intestine
Combined ceca
Pancreas
Liver
Kidney
Heart
Lung
Pectoralis muscle
Supracoracoideus muscle
Remaining carcass
Total lipid
.319
.285
.195
.226
.325
.353
.367
.268
.227
.290
.182
.207
.283
⫺.088
⫺.389
⫺.296
⫺.188
⫺.286
⫺.205
⫺.004
.219
.288
.393
.386
.396
.056
⫺.014
.046
.520
.551
⫺.252
⫺.232
⫺.110
⫺.082
⫺.115
.099
.157
.319
⫺.372
Note. Small intestine, large intestine, and ceca were entered as
wet mass. Liver, heart, pectoralis, supracoracoideus, and carcass
were entered as lean dry mass. Other components were entered
as dry mass.
Discussion
Body composition of female western sandpipers changed markedly in response to migration. As expected, migrants were much
fatter than wintering birds, yet 40% of the total mass increase
of migrants was lean tissue. Lean mass deposition rates of
20%–40% of total mass have been reported previously in premigratory birds as well as during real and simulated stopover
(Lindström and Piersma 1993; Klaassen and Biebach 1994;
Klaassen et al. 1997; Karasov and Pinshow 1998). We could
have overestimated seasonal lean mass deposition if the typical
bird captured at the Fraser estuary was relatively fat depleted
from flight or if refueling sandpipers tend to deposit lean mass
before fat (McLandress and Raveling 1981; Carpenter et al.
1993; Klaassen et al. 1997). Some migrant birds, such as the
blackcap (Sylvia atricapilla), appear to catabolize and deposit
fat and lean mass simultaneously (Karasov and Pinshow 1998).
All organs and muscles were enlarged during migration, but
the relative increases were greater for digestive organs than for
exercise components. Within the digestive organs, the liver and
pancreas showed the greatest relative increase from winter to
migration, and the large intestine and ceca the smallest. The
ingestion of hard-shelled prey can alter shorebird stomach mass
(Piersma et al. 1999a), but it is unlikely that this can explain
the seasonal changes in digestive organs we measured. Western
sandpipers eat mostly soft-bodied worms and small crustaceans,
and mollusks and other hard-shelled animals were rarely noted
in gizzard contents of our sample at any time of the year (C.
G. Guglielmo, personal observation). Moreover, the two organs
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Body Composition Flexibility in Sandpipers
93
Figure 4. Three-dimensional projections of eigenvectors for body components on the first three principal component axes. Vectors are drawn
from the origin (0, 0, 0) to points defined by the three eigenvectors and are viewed coming toward the viewer (a) and after 90⬚ rotation (b).
The length and proximity in space of these vectors to each other indicate the strength of the relationships among them. Abbreviations are liver
(LV ), pancreas (P), ceca (CE), large intestine (LI ), small intestine (SI ), gizzard (G), kidney (K ), heart (H ), lung (LU ), pectoralis (PE),
supracoracoideus (SU ), lean carcass (CR), and total body fat (F).
that changed most dramatically are associated with digestive
enzyme secretion (pancreas), bile production, and postabsorptive nutrient processing (liver) rather than bulk processing of
ingesta. This suggests that variation in nutrient load, not prey
type, was the primary factor driving digestive system change.
Hypertrophy of most body components remained significant
when body mass rather than body size was used as a covariate,
indicating that these changes were out of proportion to normal
scaling to body mass. Thus, changes in most organ masses
appeared to be driven by external demands, such as hyperphagia and endurance exercise, supporting our first hypothesis.
A notable exception was the pectoralis muscle, which did not
vary significantly while controlling for body mass. Flight muscle
size in migrants but evidently not in premigrant sandpipers
may be adjusted to meet the power requirements of flight at
any given body mass (Marsh 1984; Lindström et al. 2000).
The overall seasonal patterns of body composition can be
visualized easily by plotting individual scores along the first and
second principal component axes (Fig. 5). Wintering and premigrant birds scored low on PC1 and high on PC2, indicating
that they had small organs that were biased toward exercise
components. The transition to migration was characterized by
an increase in organ masses and a shift in body composition
toward a relatively large digestive system. The dominance of
the digestive system was most pronounced in fall-migrating
juveniles. Facultative reduction of the digestive organs just before departure to decrease ballast has been demonstrated in
several long-jump migrant species (Piersma et al. 1993, 1999b;
Battley and Piersma 1997; Jehl 1997; Piersma 1998; Piersma
and Gill 1998). Although our data are not suitable for detecting
reductions of gut size just before departure, they clearly show
that western sandpipers have enlarged digestive systems during
the migration season. If gut reductions do occur before departures or by in-flight catabolism, the major digestive system
components (small intestine, liver, pancreas) of western sandpipers essentially never reach the small sizes found in nonmigratory individuals in Panama. As short-hop migrants with
stopover times of 1–3 d (Butler et al. 1987; Iverson et al. 1996),
it may be beneficial for western sandpipers to maintain a large
gut that allows immediate hyperphagia and rapid fueling at the
next stopover. Western sandpipers are also much smaller than
species examined in previous studies that have demonstrated
programmed gut reduction in migrants. Maintenance of a large
gut during migration could be necessary for small birds with
high mass-specific metabolism to offset rapid gut reduction
during in-flight fasting, but this requires further study.
With a larger sample of western sandpipers, Butler et al.
(1987) found that both sexes were significantly heavier in the
spring than in the fall. In our study, body composition did not
differ systematically between spring and fall migration in either
sex, indicating that spring migrants do not carry extra reserves
when heading north into potentially uncertain weather conditions. Fall migration in 1995 may have been stressful because
the adult females we captured had low body mass and small
organs and juveniles had lower lean masses than in 1996.
Modulation of Metabolic Machinery During, Not Before,
Migration
We expected that adult sandpipers would alter lean body composition during premigration so that critical metabolic ma-
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94 C. G. Guglielmo and T. D. Williams
Figure 5. Principal component scores for female western sandpipers on the first two axes from a principal components analysis of body
composition. Open and filled symbols represent birds collected in Panama and birds collected during migratory stopover at the Fraser estuary,
respectively. PC1 reflected overall component masses, and PC2 reflected exercise (positive loadings) versus digestive components (negative
loadings). Migrants had higher PC1 scores than birds in Panama (F1, 129 p 121.5 , P p 0.0001). Regression lines used in ANCOVA are shown
for (1) premigrant adults, (2) winter adults, (3) 1996 spring and fall adult migrants, (4) 1995 spring adult migrants, and (5) 1995 and 1996
fall juvenile migrants. Slopes did not differ (P p 0.79). Differences (P ! 0.05) in elevation are indicated by different line patterns.
chinery would be in place before endurance flights and before
high feeding rates had to be supported. Premigratory adults in
Panama appeared externally (on the basis of mass and plumage)
to be very similar to spring migrants caught 6 wk later at the
Fraser estuary. However, contrary to our second hypothesis,
premigrants only had the large fat stores and not the enlarged
lean body components of true migrants. Another small sandpiper, the little stint (Calidris minuta), appears to have a similar
premigratory fattening strategy (Lindström and Piersma 1993).
The lack of anticipatory increases in flight muscle mass and
fatty acid oxidation capacity (Guglielmo et al. 2002a) during
premigration indicates that flight training may be required to
induce the alteration of muscle mass and biochemical capacity
in this short-hop migrant. Several other studies demonstrate
increases in muscle size without apparent flight training (Evans
et al. 1992; Battley and Piersma 1997; Jehl 1997; Dietz et al.
1999; Piersma et al. 1999b), but these species are all considered
to have long-jump migration strategies.
Western sandpipers were able to deposit a substantial amount
of fat during premigration without hypertrophy of the digestive
system or increased liver lipogenic capacity (Egeler et al. 2000).
The daily rate of mass gain in premigratory western sandpipers
(0.09 g/d; O’Hara 2002) is lower than at migratory stopover
(0.4–1.0 g/d; Butler et al. 1997). A moderate rate of fattening
without gut hypertrophy could be achieved in premigrants by
several mechanisms. First, sandpipers may have enough spare
digestive capacity to increase food intake slightly without inducing morphological change (McWilliams and Karasov 2001).
Second, the birds could make behavioral adjustments, such as
reducing activity or extending daily feeding time without increasing the instantaneous rate of food intake. Third, premigrants could increase food retention time (Hume and Biebach 1996) or enhance enzymatic hydrolysis and nutrient uptake mechanisms (Karasov 1996) to increase nutrient (particularly lipid) assimilation efficiency (Bairlein 1985). Such enhanced food assimilation, combined with a shift in oxidative
fuel selection away from dietary fatty acids (Jenni-Eiermann
and Jenni 1996; Guglielmo et al. 2002b), could result in fat
deposition in premigrants. Some studies have suggested that
migrants can make anticipatory changes in the gut through
hormonal or neuronal mechanisms (Jehl 1997; Piersma and
Lindström 1997). However, gut hypertrophy in western sandpipers occurred after migration was initiated. In general, empirical evidence indicates that changes in gut morphology are
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Body Composition Flexibility in Sandpipers
not proactive but are reactions to changes in feeding rate (fasting, hyperphagia) that are determined by exogenous (thermoregulatory cost, food shortage, food quality) or endogenous
(hormonal cycles) factors (Karasov 1996; Karasov and Hume
1997). Elevated intraluminal nutrient concentrations are
thought to be a proximate cause of gut hypertrophy when
digestive load exceeds capacity (Karasov and Hume 1997).
Age and Sex Variation
Juveniles making their first southward migration were similar
to adults in structural size, body mass, and fat stores. Migrant
juveniles (especially males) tended to have smaller exercise
components than adults, but the major age difference was a
dramatically heavier alimentary tract in juveniles. We propose
five hypotheses to explain why juvenile sandpipers might have
large guts. First, as suggested by Hume and Biebach (1996) for
juvenile garden warblers (Sylvia borin), large guts in young birds
may reflect continued growth during migration. Growing
chicks generally have enlarged digestive systems (Karasov 1996),
but the adult size and body mass of migrant juvenile sandpipers
does not support this explanation. Second, juveniles may capture less digestible prey than adults, requiring higher food intake. Third, shorebirds ingest sediment as they feed on buried
invertebrates (Tsipoura and Burger 1999), and juveniles may
consume more indigestible bulk by being less proficient than
adults at separating food from sediment. Perhaps our observation of increased mass, not length, of the gut is related to
the mechanics of processing sediment. Fourth, if juveniles are
less successful than adults at finding and capturing prey, their
digestive strategy may be to maximize efficiency by having slow
food passage rates and larger guts (Jackson 1992; Barton and
Houston 1993). Adults may maximize net rate of energy gain
by having a smaller gut and more rapid passage rate (see Castro
et al. 1989). Finally, enlarged small intestines in juveniles could
be a response to higher intestinal parasite loads. However, small
intestine size was unrelated to intestinal helminth abundance
in snow geese (Shutler et al. 1999). Further investigation is
required to test these hypotheses.
By the time juvenile sandpipers settled on the wintering area,
the alimentary tract was much reduced in mass and was not
different from that of adults. Throughout winter and premigration, juveniles tended to have smaller organ masses and
lower overall lean mass than adults. If lean mass and organ
sizes are an indication of energetic state and condition, this
may indicate that juveniles were under greater stress than adults
at the wintering site (Katti and Price 1999).
Seasonal changes in body composition in males are probably
similar to those we have described in females because the annual
patterns of body mass variation in the two sexes are similar
(O’Hara 2002). Organ and muscle masses did not differ between males and females once we controlled for body size and
mass. In spring 1996, females carried relatively more total body
95
mass than males; however, this was not the case in spring 1995.
Moreover, female body composition did not differ substantially
between spring and fall migration in 1996, indicating that females do not carry extra reserves to the breeding grounds for
egg production. Income breeding in arctic-breeding shorebirds
is corroborated by stable carbon isotope analysis of adult feathers, eggs, and natal down in 10 additional species (Klaassen et
al. 2001). Butler et al. (1987) used wing chord to control for
body size differences between sexes and found that female western sandpipers carried extra reserves in the spring. Using (wing
chord)3, arguably a better measure of structural size, yields a
size correction factor of 1.12 (compared with 1.04) and indicates that controlling for body size, males and females in their
study had nearly identical body masses.
Deposition of Lean Mass during Stopover
Significant deposition of lean mass appeared to occur during
stopover at the Fraser estuary in some fall migrants but not
during spring. In spring, western sandpipers make numerous
short flights along the coast before arriving at the Fraser estuary,
whereas in the fall, they make a 2,000–3,000-km overwater
flight from western Alaska (Butler et al. 1996; Iverson et al.
1996). The long flight in fall could result in more substantial
catabolism of lean tissue, which may be replaced during stopover. At the organ level, most lean mass was deposited in the
digestive system, which is consistent with the idea that the
digestive system may be catabolized during long-distance flight
(Klaassen and Biebach 1994; Hume and Biebach 1996; Klaassen
et al. 1997; Karasov and Pinshow 1998, 2000; Piersma and Gill
1998; Battley et al. 2000; McWilliams and Karasov 2001).
Scaling and Organ System Design
Study of how the size and physiological properties of organs
and muscles scale with body mass has been crucial to the development of thinking on the evolutionary design of organisms
(Calder 1984; Schmidt-Nielsen 1984). Whether scaling rules
determined from interspecific relationships apply within species
is unclear. For example, interspecifically, metabolic rates are
consistently related to M 0.65 (Reynolds and Lee 1996) or M 0.75
(Schmidt-Nielsen 1984), whereas intraspecific BMR scaling exponents are often much greater than 0.75 (Battley et al. 2001).
We report scaling exponents from OLS regression because most
previous studies have used this method of analysis. However,
model II regression (RMA) is recommended to describe functional (i.e., nonpredictive) relationships where appreciable error
in the x variable (log10 mass) is expected, such as in morphometric studies (McArdle 1988). In general, RMA regression
indicated two things about intraspecific scaling in sandpipers.
First, only the supracoracoideus and pectoralis muscles scaled
with exponents equal to or less than predicted from interspecific
regressions (Schmidt-Nielsen 1984; Daan et al. 1990). Intra-
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96 C. G. Guglielmo and T. D. Williams
specific scaling exponents for pectoralis from OLS regression
have been reported to be 1.25 in tree swallows (Tachycineta
bicolor; Burness et al. 1998) and near 0.65 for pectoralis in two
shorebird species (Davidson and Evans 1988; Battley and
Piersma 1997). Second, scaling exponents were greater for digestive organs than for exercise components (only the 95%
confidence interval of the gizzard overlapped with any exercise
component), a difference that was mirrored in the principal
component analysis. The heaviest birds were fat migrants, and
the large scaling exponents of the digestive system reflect the
more substantial hypertrophy of these organs to maximize refueling capacity during migration.
Piersma et al. (1996, 1999b) used the first two principal
component axes to investigate the structure of body composition variation in shorebirds and defined two broad groups:
“exercise” and “digestive” components. This simple division
implies that, within a group, organ sizes are somehow coregulated by shared mechanisms, but the two groups are relatively
independent of each other. We further resolved relationships
among organs and muscles by considering the third principal
component axis. Some functional interpretations of the groups
are intuitive, such as muscles being related to flight performance
and heart and lung being primarily involved in oxygen supply.
Within the digestive system, small intestine and gizzard size
may respond to overall energy demand and food intake, while
the large intestine and ceca may be important in water balance
(Karasov and Hume 1997). The liver and pancreas (loading
strongly on PC3) may respond particularly to fattening. While
necessarily speculative, our analysis indicates the potential for
future studies of coregulation of multiple body components.
Acknowledgments
Many thanks to all of those (more than 50) who helped in the
field and laboratory, particularly J. Christians, O. Egeler, D.
Lissimore, C. Martyniuk, B. Mezzerosi, J. Moran, P. O’Hara,
G. Reardon, E. Reid, G. Robertson, J. Roy, B. Sandercock, P.
Shepherd, M. Smyth, R. Stein, S. Tapia, S. Ternan, and J. Terris.
We are also grateful to R. Butler, R. Elner, and M. Klaassen for
their insights. Thanks to John Christy and the staff of the
Smithsonian Tropical Research Institute for assistance in Panama. Comments from three excellent reviewers greatly improved the manuscript. Funding was provided by the Canadian
Wildlife Service and the Natural Sciences and Engineering Research Council of Canada.
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