Developmental plasticity of physiology and morphology in diet-restricted European shag nestlings (Phalacrocorax aristotelis)
Department of Biology, Norwegian University of Science and Technology, NO-7491 Trondheim, Norway
* Author for correspondence (e-mail: borge.moe{at}bio.ntnu.no)
Accepted 4 August 2004
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: developmental plasticity, metabolism, growth, development, diet restriction
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Developmental plasticity, caused by poor feeding conditions, can affect
adult morphology (De Kogel,
1997; Birkhead et al.,
1999
) and result in long-term consequences
(Lindström, 1999
;
Metcalfe and Monaghan, 2001
;
Dufty et al., 2002
). However,
developmental plasticity can also show reversible patterns
(Schew and Ricklefs, 1998
).
Energy expenditure and body temperature
(Prinzinger and Siedle, 1988
;
Schew, 1995
), but also
morphology (Emlen et al.,
1991
; B.M., S.B., D.M., T.E.B. and C.B., unpublished data), may
show considerable reversible short-term responses to temporal variation in
environmental conditions during the development. A number of recent studies
have investigated how growing birds can modify the pattern of energy use and
allocation as a response to short-term diet restriction (e.g.
Schew, 1995
;
Kitaysky, 1999
;
Konarzewski and Starck, 2000
;
Brzek and Konarzewski, 2001
;
Moe et al., in press
).
Physiological and morphological responses of nestlings to short-term diet
restriction form a practical experimental system for studying developmental
plasticity, an important aspect of life-history.
Fluctuations in food availability
(Konarzewski and Starck, 2000)
and sibling competition (Brzek and
Konarzewski, 2001
) are among the factors that may have selected
for adaptive developmental responses to temporal food shortage
(Schew and Ricklefs, 1998
).
During periods of food shortage, lasting less than some critical proportion of
the chick's growth period and longer than a short period that can be easily
buffered by stored energy reserves, a reduction in metabolism is expected to
enhance survival (Schew and Ricklefs,
1998
). Sibling competition has also been suggested to select for
reductions in metabolic rate (MR) as a response to temporal food shortage
(Brezek and Konarzewski, 2001), but it has been suggested to select against
slowing of growth and maturation of the parts of the skeleton most important
in competing with nest mates for food
(Schew and Ricklefs, 1998
).
This is apparently conflicting if growth rate and metabolism is positively
related (Drent and Klaassen,
1989
; Klaassen and Drent,
1991
), and it would require a substantial change in the energy
allocation from maintenance to growth.
Modification of the basal level of energy expenditure could occur as an
adaptive response to food shortage. Alternatively, any reduction of the basal
level of energy expenditure could be a direct consequence of the lack of
sufficient nutrients during food shortage. Also, the lack of nutrients could
impose reductions in growth rate and in the size of energy consuming organs,
which consequently could cause reductions in the basal level of energy
expenditure, as a non-adaptive response. However, reductions in the size of
energy-consuming organs (Piersma and
Lindstrøm, 1997) and in growth rate
(Emlen et al., 1991
) could
also be adaptive responses. Visceral organs (especially the heart, liver,
kidneys and intestine) are believed to consume much of the energy used in
basal metabolism (Daan et al.,
1990
), but the specific organs and tissues that predict RMR differ
among studies (e.g. Burness et al.,
1998
; Bech and Østnes,
1999
; Chappell et al.,
1999
; Moe et al., in
press
). Hence, it is not fully understood how body composition
functionally relates to RMR.
Despite the view that the skeleton and the nervous system are regarded as
less flexible compared with visceral organs and physiological processes
(Schew and Ricklefs, 1998;
Pigliucci, 2001
), several
distinct growth patterns in response to food shortages have been reported. At
reduced levels of energy intake, the structural growth rate can be maintained
rigidly within the limits of the food intake (e.g.
Konarzewski et al., 1996
). By
contrast, growth and development can be temporally stalled (e.g.
Emlen et al., 1991
;
Schew, 1995
;
Starck and Chinsamy, 2002
).
Alternatively, energy can be specifically allocated to growth of favoured
structural elements at the expense of others (e.g.
Øyan and Anker-Nilssen,
1996
; Kitaysky,
1999
; Moe et al., in
press
).
Nestling European shags (Phalacrocorax aristotelis L.) are very
well suited for studying physiological and morphological responses to temporal
food shortage. As individual nestlings exhibit high growth rates
(Østnes et al., 2001)
and compete with siblings for food
(Amundsen and Stokland, 1988
;
Velando et al., 1999
,
2000
), they depend on
successful food provisioning rates to follow their normal developmental
trajectory. Owing to a very low deposition of lipids
(Bech and Østnes, 1999
),
the nestlings have a limited capacity for buffering temporal food shortages.
In the study area, the European shag is an inshore and offshore benthic
feeder, and relies on gadoids (Barrett et
al., 1990
). It is reported that nestling European shags are likely
to encounter variable food provisioning during early development due to
adverse weather conditions, which affects the foraging success of the parents
(Velando et al., 1999
).
Adverse weather also increases the need for brooding at the expense of
foraging (Beintema and Visser,
1989
).
The evolution of developmental responses is driven by natural selection and
limited by internal constraints (Starck
and Ricklefs, 1998; Ricklefs
et al., 1998
; Pigliucci,
2001
), of which genetic and developmental constraints are
important (Pigliucci, 2001
).
Hence, developmental mode, in the altricialprecocial spectrum, could
possibly constrain or determine the physiological and morphological responses
to temporal food shortage. However, only a few altricial species, of which all
were passerines, have been investigated in this context. So far, contrasting
patterns of physiological responses have been revealed. Sand martins
(Riparia riparia; Brzek and
Konarzewski, 2001
) and house martins (Delichon urbica;
Prinzinger and Siedle, 1988
)
use hypothermia and lower their basal metabolism, while song thrushes
(Turdus philomelos; Konarzewski
and Starck, 2000
) and starlings
(Schew, 1995
) do not show any
energy-saving responses to temporal food shortage. In addition, contrasting
patterns of structural growth have been revealed (e.g. white-fronted
bee-eaters, Merops bullockoides, versus song thrushes;
Emlen et al., 1991
;
Konarzewski et al., 1996
).
This study is the first study to investigate physiological and morphological
developmental responses to temporal food shortage in an altricial seabird.
In the present study, we experimentally imposed short-term diet restriction
on 1216-day-old nestling European shags, kept under laboratory
conditions. Mass-specific RMR is very high during this age period
(Bech and Østnes, 1999;
Østnes et al., 2001
).
We reveal whether nestling European shags exhibit any energy saving that can
lessen the detrimental effects of reduced food intake during early
development, and reveal how the nestlings allocated the energy between
maintenance and growth. We also assess whether hypothermia or changes in body
composition are components of any energy saving processes. Information about
the effect of diet restriction on thermoregulatory capacity and on subsequent
growth during re-alimentation will be published elsewhere.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Housing conditions, feeding protocols and treatment groups
A sample of 34 nestlings was brought to the laboratory at the age of 12
days for the purpose of subsequent metabolic measurements. The nestlings were
kept, 48 together, in an enclosure (100x50 cm) with a heat lamp
providing a constant range of operative temperatures
(Bakken, 1992) of
2233°C. We randomly assigned 12 nestlings to a diet-restricted
feeding protocol (hereafter `diet-restricted nestlings') and 22 nestlings to a
control group (hereafter `controls'). Within the controls, 12 nestlings were
subject to metabolic measurements at the age of 12 days, whereas 10 nestlings
were subject to a control-feeding protocol. The diet-restricted and the
control-fed nestlings were hand fed with fillets of saithe (Pollachius
virens) and cod (Gadus morhua), because these gadoids constitute
70% of the diet of shags breeding in the study area
(Barrett et al., 1990
). They
were fed for 4 days, until they were 16 days old and metabolic rates were
measured. The diet-restricted nestlings received small portions of food
810 times a day to maintain a relatively stable body mass, while the
controls were fed every second hour, allowing them to follow a normal body
mass growth trajectory. The National Committee for Animal Research in Norway
(`Forsøksdyrutvalget') approved the experimental protocols.
Metabolic measurements
Oxygen consumption rates were measured by open-flow respirometry
(Withers, 1977). Outside air
was dried using silica gel and pumped through a 10-litre temperature
controlled metabolic chamber with a flow rate of 3.3l min-1. The
actual flow rates entering the metabolic chamber were measured with a
calibrated mass flow controller (Bronkhorst Hi-Tec, Rurlo, Holland; type
F-201C-FA-22-V). Excurrent air was dried before a fraction of the air was
directed to the oxygen analyser (Servomex, Crowborough, East Sussex, UK; type
244A). The oxygen (O2) analyser was calibrated with dry atmospheric
air (20.95%) and pure stock nitrogen. Any changes from the preto the
post-experiment readings of the O2 content in dry atmospheric air
were controlled for by assuming a linear drift. Measurements of the
O2 content in excurrent air (accuracy 0.001%) were stored, along
with the measurements of body and ambient temperatures (Tb
and Ta; accuracy 0.1°C) on a data logger (Grant,
Cambridge, UK, type Squirrel) at 30 s intervals.
The metabolic measurements were performed on post-absorptive nestlings. The lengths of fasting before the measurements were 6.4±0.5, 7.3±0.5 and 9.4±0.4 h for 12-day-old controls, 16-day-old diet-restricted and 16-day-old controls, respectively. The longer length of fasting of the latter group was chosen due to higher gut content.
The metabolic measurements were performed at different times of the day, but diet-restricted nestlings and controls were randomly measured with respect to time of the day. More importantly, RMR showed no diurnal cycle.
O2 consumption rates were calculated by using formula 1d in
Withers (1977), assuming a
constant respiratory quotient of 0.72 and corrected for wash-out delays in the
system by using the method given by Niimi
(1978
). In this way, we
obtained the instantaneous O2 consumption rates. Values of MRs were
calculated from the O2 consumption rates using 5.4611 W as the
caloric equivalent for 1 l O2 h-1, using gas exchange
conversion factors from Schmidt-Nielsen
(1990
).
RMR was defined as the lowest MR calculated with a 25 min running average
during exposure to thermoneutral conditions. The use of a running average over
a 25 min interval was justified after plotting the minimum values of the MR,
calculated in five randomly selected experimental runs using intervals that
varied from 560 min. For a running average lower than 15 min, these
curves revealed a very strong positive relationship between the minimum values
of RMR and the length of the running average interval. Short intervals
resulted in very low minimum values of RMR, thereby underestimating the RMR
level. However, at a running average between 15 min and 60 min, the minimum
values of RMR changed relatively little (see
Meerlo et al., 1997, for a
description of this procedure).
The metabolic chamber was a water-jacketed vessel connected to a
temperature controller (Grant Instruments, Royston, UK; type LT D G) that
provided control of the Ta in the inner metabolic chamber.
The Ta was set between 2931°C for thermoneutral
conditions (Østnes et al.,
2001). Ta was measured with a
copperconstantan thermocouple (California Fine Wire Company, Grover
City, CA, USA; type 0.005) mounted inside the metabolic chamber, and
Tb was measured in the cloaca with a CuCo
thermocouple surrounded by a polypropylene tubing (outer diameter 0.96 mm).
Depending on the nestling's size, the thermocouple was inserted 24 cm
into the cloaca and secured with adhesive tape. Thermal conductance
(TC) during thermoneutral conditions was calculated according to the
following formula:
![]() | (1) |
Body masses of the nestlings were weighed, to the nearest 0.1 g, before and immediately after each experiment. A linear decrease in body mass during the experiment was assumed when calculating the body mass at the time when RMR was obtained. To obtain independent measurements, each individual was only used once in the experiments, and all nestlings originated from different nests.
Body composition
A sample of 28 of the 34 nestlings was anaesthetised with ether
(inhalation) and sacrificed by suffocation immediately after the metabolic
measurements and stored at 20°C for later analysis of body
composition. The remaining six nestlings were brought back to the nest of
origin or to a nest with foster parents. Dissection was done on semi-thawed
carcasses to reduce vaporisation and to improve organ separation. We removed
heart, liver, kidney, gizzard and intestine (small and large). The entire
right breast muscle (m. supracoracoideus and m. pectoralis) was separated from
the skeleton. Also, the entire right leg muscle was separated from the
tibiotarsustarsometatarsus joint. The mass of these muscles was
multiplied by two to get the total breast and leg muscle mass. Gizzard,
intestine and heart atrium was emptied of contents, while all organs and
muscles were carefully trimmed of fat and weighed (±1 mg; carcasses to
±0.1 g). They were then dried to a constant mass at 56°C and
reweighed. Fat content was subsequently removed in baths of petroleum ether
for a minimum of 24 h. Baths were changed until the yellow colour (lipid) of
the solution disappeared and became clear, and the samples where again dried
and reweighed. The lean dry fraction (LDF) of organs was calculated as the
ratio of lipid-free dry organ mass to lipid-free fresh organ mass. The LDF of
most organs and tissues increases during the ontogenetic development due to a
build-up of proteins and functional components on the cellular level. Hence,
the LDF is regarded as reflecting the functional maturity of a tissue
(Ricklefs et al., 1994).
Morphology and growth
Biometry [wing length, tarsus length, skull length (head + bill)] and body
mass of the nestlings were measured every day in the laboratory. Growth rates
were calculated as the daily growth (mm day-1 and g
day-1) during the 4 days (from 1216-day old). Hence, growth
rates of structural elements and body mass were obtained for 16-day-old
diet-restricted and 16-day-old control nestlings. We used a principal
component analysis to extract a factor score (PC1) from the growth rate of the
wing, tarsus and skull.
For comparison, we measured the growth of nestlings that were fed by their parents in the colony. Measurements of body mass (N=1645) and biometry (N=1050) were fitted to a logistic equation. Specific growth rates (g day-1 and mm day-1) from the age of 1216 days were obtained from eight nestlings of which we had repeated measures.
Statistics
We used a general linear model (GLM) with the type III sum of squares to
perform analyses of covariance and variance. We manually excluded
insignificant interaction terms, factors or covariates one by one from the
null model (ENTER method). All variables were inspected graphically to ensure
linearity, and log10 transformation was used to linearize the
variables (MR, body mass, organ mass) before examination.
We analysed the relationship between organ mass and MR by including body
mass as a covariate to remove the effect of body mass (i.e. body mass is held
constant; Hayes and Shonkwiler,
1996). To avoid possible effects of part-whole correlation, we
subtracted organ mass from the body mass variable, when organ mass and body
mass were included in the same analysis
(Christians, 1999
).
Co-linearity diagnostics were used to justify that LDF could be included as a
covariate (together with body mass and organ mass) in the analyses of the
relationship between organ mass and MR (tolerance >0.3 for all
variables).
When two regressions with log10-transformed variables (e.g.
metabolic rate on body mass) have the same slope, but have different
intercepts, we have calculated the percentage difference between the
non-transformed regressions according to formula 4 in Moe et al.
(in press). The GLM procedure
was performed unless otherwise specified. The Student's t-test was
used for comparison of means of two groups. The Bonferroni method was used for
post hoc pairwise multiple comparisons (`post hoc' hereafter). This
method reports adjusted P-values that have been multiplied with the
number of pairs tested. Values reported are means ± 1 S.E.M.
All statistical tests were performed with SPSS version 11.5.1 (2002).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
The differences in daily food intake had a huge effect on the body mass (Fig.1B). The body mass of the diet-restricted nestlings was maintained at a relatively stable level, but with a significant gain of 5.7±0.8 g day-1 (P<0.001). By contrast, the control fed nestlings followed a normal body mass growth trajectory, to the age of 15 days, close to that of the nestlings fed by parents in the colony (Fig. 1B). However, at the age of 16 days the body mass growth of the control fed nestlings deviated substantially from that of the nestlings fed by parents, mainly due to the fasting before the metabolic measurements.
Resting metabolic rate and body temperature
RMR scaled to body mass by the power of 0.84±0.12 (mean ±
S.E.M.; F1,31=51.2, P<0.001;
Fig. 2) in both groups (RMR
x body mass interaction, F1,30=0.5,
P>0.1). RMR was substantially affected by the diet restriction.
With respect to body mass, the RMR of the diet-restricted nestlings was 36.5%
lower than the controls (F1,31=90.0, P<0.001;
Fig. 2). With respect to age,
the mass-specific RMR was 11.6±0.36, 11.1±0.34 and
7.4±0.37 W kg-1 for 12-day-old controls, 16-day-old controls
and 16-day-old diet-restricted nestlings, respectively. The mass-specific RMR
of the 16-day-old diet-restricted nestlings was lower compared with the
16-day-old controls (post hoc, P<0.001) and the 12-day-old
controls (post hoc, P<0.001), whereas that of 16-day-old controls
and 12-day-old controls was not significantly different (post hoc,
P>0.1).
|
Diet-restricted nestlings exhibited a lower Tb compared with controls. A post hoc comparison showed that the Tb of 16-day-old diet-restricted nestlings (36.1±0.34°C) was 2.1°C lower compared with 16-day-old controls (38.2±0.15°C; P<0.001; Fig. 3). The diet-restricted nestlings also exhibited a lower Tb than expected from body mass (F1,28=8.58, P<0.007). The Tb of diet-restricted nestlings of 355 g (the mean body mass of the 16-day-old diet-restricted nestlings) was 1.3°C lower than predicted for controls of the same body mass.
|
Structural growth
The growth of the skull, tarsus and wings is given in
Fig. 4AC for the
nestlings of which we had biometric measurements every day. The growth rates
of the skull (t-test, t=2.7, d.f.=10,
P<0.05; Fig. 4D)
and the wings (t-test, t=2.3, d.f.=10,
P<0.05; Fig. 4F)
were slightly lower in the 16-day-old diet-restricted nestlings compared with
the 16-day-old controls. By contrast, the growth rate of the tarsus
(t-test, t=0.1, d.f.=10, P>0.1;
Fig.4E) was not significantly
different between the controls and the diet-restricted nestlings. Thus, the
structural growth of the diet-restricted nestlings was almost in line with the
age-specific growth of the control fed nestlings, and it contrasted to the
vast reductions in body mass growth rate
(Fig. 4DF). With respect
to body mass, the 16-day-old diet-restricted nestlings exhibited 17.8% longer
wings (F1,20=38.5, P<0.001), 13.0% longer
tarsus (F1,20=36.4, P<0.001) and 10.4% longer
skull (F1,20=84.7, P<0.001) compared with the
controls (12 and 16 days old).
|
The growth of the nestlings that were fed by their parents in the colony is also shown in Fig. 4. Comparisons between diet-restricted nestlings and nestlings fed by their parents were consistent with the results above. Diet-restricted nestlings exhibited a lower growth rate of the skull (post hoc, P<0.05; Fig. 4D) and the wings (post hoc, P<0.001; Fig. 4F), while the growth rate of the tarsus was not significantly different (post hoc, P>0.1; Fig. 4E) compared with that of the nestlings fed by their parents. The structural growth trajectory of the control fed nestlings in the laboratory was slightly different to that of the nestlings fed by their parents in the colony (Fig. 4AC). While the growth rate of the skull (post hoc, P>0.1; Fig. 4D) and the tarsus (post hoc, P>0.1; Fig. 4E) did not differ significantly, the growth rate of the wings was significantly lower in the control fed nestlings compared with that of the nestlings fed by their parents (post hoc, P<0.01; Fig. 4F).
Body composition
In contrast to the structural components, organs and muscles were either
reduced or maintained with respect to body mass as a response to the diet
restriction (Fig. 5). With
respect to body mass, the total lipid mass (F1,25=69.6,
P<0.001; Fig. 5A),
the liver mass (F1,25=97.4, P<0.001;
Fig. 5B), the pectoral muscle
mass (F1,25=19.9, P<0.001;
Fig. 5C), the heart mass
(F1,25=18.2, P<0.001;
Fig. 5D), the gizzard mass
(F1,24=25.9, P<0.001) and the kidney mass
(F1,25=4.9, P<0.05) of the diet-restricted
nestlings were 41.4, 29.2, 18.9, 17.4 and 9.8% lower compared with that of the
controls, respectively. In addition, the leg muscle mass tended to be slightly
lower in diet-restricted nestlings compared with controls
(F1,25=3.8, P=0.06;
Fig. 5E). However, one visceral
organ, the intestine, was strictly maintained with respect to body mass as a
response to the diet restriction. Both the mass
(F1,25=0.1, P>0.1;
Fig. 5F) and the length of the
intestine (F1,25=0.4, P>0.1) of the
diet-restricted nestlings was not different to that of the controls. The lean
dry fraction (LDF) was not different between 16-day-old diet-restricted and
16-day-old controls in any organ or muscles, except for the intestine. The LDF
of the intestine was lower in diet-restricted nestlings compared with controls
(post hoc, P<0.05).
|
To control for age-dependent effects on body composition, we also performed separate analyses of body composition (organ mass/body mass) in relation to age and treatment. The results from those analyses were consistent with the analyses that were performed in relation to body mass.
Correlations between organ masses and metabolic rate
To evaluate whether the changes in body composition could explain any of
the differences in RMR between the treatment groups, we tested whether organ
masses correlated to RMR (Table
1). The lean dry mass of the liver (r=0.64,
F1,22=15.2, P<0.001), the pectoral muscles
(r=0.50, F1,23=7.8, P<0.01) and the
lipid mass (r=0.44, F1,24=5.8,
P<0.05) correlated significantly and positively with RMR, while
the lean dry mass of the leg muscles, heart, gizzard, kidney and intestine did
not. We controlled for organ LDF, body mass (minus organ mass) and treatment
in these analyses (Table 1).
Treatment was a strong and significant factor in all the models.
|
Growth rates and RMR
The extracted factor score (PC1) from a principal component analysis
explained 57% of the variance in the log10-transformed growth rates
of the skull (r=0.93), tarsus (r=0.45), and wings
(r=0.80). The PC1 correlated positively with RMR
(F1,8=8.5, P<0.05) and the interaction
(treatmentxPC1) was not significant (F1,7=0.5,
P>0.1), indicating that structural growth and RMR was positively
related within both treatment groups. Body mass and treatment were controlled
for by including them in the analyses as a covariate and a factor,
respectively.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The visceral organs are believed to consume much of the energy used in
basal metabolism (Daan et al.,
1990; Chappell et al.,
1999
). In our study, the mass of the liver, the pectoral muscles
and the lipid mass were positively correlated to RMR. Liver tissue has a high
intrinsic MR (Scott and Evans,
1992
), and Bech and Østnes
(1999
) suggested the liver to
have a great influence on RMR of nestling European shags. In a study on
metabolic responses to food-shortage, the liver size was a significant
predictor of the differences in RMR between diet-restricted and ad
libitum fed ducklings (Moe et al., in
press
). The positive correlation between the liver mass and RMR in
the present study, indicate that the reductions in the liver mass of the
diet-restricted nestlings could be an important predictor of the observed
differences in RMR. However, liver mass and treatment were a strong and
significant covariate and factor, respectively, in the GLM model.
Consequently, variation in liver mass together with other physiological
changes induced by the diet-restriction treatment must have affected RMR. By
using 2.71 ml O2 g-1 h-1 for liver MR
(Scott and Evans, 1992
), liver
mass changes explained only 6% of the difference in the overall RMR between
the controls and the diet-restricted nestlings. Such a quantitative value of
the reduction in RMR should, however, be treated carefully as Scott and Evans
(1992
) measured the MR of
liver samples from adult birds and in different species to ours.
We also revealed a positive correlation between the pectoral muscles and
RMR, which has also been found in juvenile and adult house sparrows
(Passer domesticus; Chappell et
al., 1999) and in migrating knots (Calidris canutus;
Weber and Piersma, 1996
).
However, in contrast to the juvenile and adult birds mentioned above, the
pectoral muscles of the young shag nestlings are very small, constituting only
2% of the total body mass. Hence, the variation in the mass of the pectoral
muscles should have a negligible impact on the variation in total RMR in this
study. The total lipid mass also correlated positively with RMR, but adipose
tissue has a very low intrinsic MR (Scott
and Evans, 1992
) and constitutes <2% of the total body mass of
the shag nestlings. Consequently, the lipid mass should not contribute
significantly to the total RMR in the shag nestlings. If the pectoral muscles
and the lipid mass do not contribute directly to the total RMR, but still
correlate positively to total RMR, they should correlate to other
physiological processes with direct impact on RMR. We suggest that the lipid
mass and the pectoral muscle mass could play a possible role as an internal
signal on nutritional status (i.e. body condition) to which the basal level of
energy expenditure could be regulated.
Energy allocation to growth
The diet-restricted nestlings maintained structural growth very well
despite a food intake of only 46% of that of the control fed nestlings. The
growth rate of the tarsus was not different to that of control fed nestlings,
and the skull and wings showed only a slightly lower growth rate. This rigid
pattern of structural growth was accompanied by a rigid development of
maturity (LDF) of the muscles and the visceral organs (except intestine). The
energy devoted to maintenance and growth constitute substantial parts of the
total energy budget during postnatal development
(Weathers, 1996). Slowing of
structural growth has been regarded as one of the means to lower RMR during
temporal food shortage (Schew and
Ricklefs, 1998
). The high structural growth rate combined with the
low RMR, observed in the diet-restricted nestlings in the present study, could
support the suggested independent
(Ricklefs and White, 1981
) or
negative (Olson, 1992
)
relationship between RMR and growth rate. However, the principal component for
structural growth rate was positively correlated to RMR, indicating an
energetic cost of high structural growth rate within both treatments. The
positive relationship is expected if RMR includes indirect costs of growth, in
terms of costs of maintaining organs that support growth or represent a
potential for growth (Drent and Klaassen,
1989
; Klaassen and Drent,
1991
) or if RMR includes direct cost of growth in terms of cost of
biosynthesis. Although the maintenance of the high structural growth rate may
have been energetically cheap (Ricklefs
and White, 1981
), the observed response must have required a
substantial change in the energy allocation from maintenance to growth.
However, it is difficult to evaluate the relative importance of structural
nutrients and energy nutrients as limiting factors for structural growth.
Calcium and phosphorus are essential inorganic structural nutrients during
growth (Murphy, 1996). If
these nutrients, rather than energy, primarily limit the rate of structural
growth it suggests that the nestlings were provided well in excess during
normal conditions and still in sufficient amount during the food restriction.
Energy nutrients, such as amino acids, may also limit structural growth, but
they appear to be actively scavenged from most visceral organs and the
skeletal muscles during the diet restriction.
Differential developmental plasticity
This study clearly demonstrates differential plasticity in the development
of the physiology and morphology of nestling European shags in response to
food shortage. The substantial energy saving was accompanied by a pattern of
energy allocation reflecting a rigid priority of the structural growth at the
expense of visceral organs, lipid deposits and muscles. Our results contrast
with studies on nestling song thrushes
(Konarzewski et al., 1996;
Konarzewski and Starck, 2000
)
and nestling European starlings (Sturnus vulgaris;
Schew, 1995
) that showed
limited plasticity both in the physiological (metabolism) and in the
morphological (structural growth) responses to temporal food shortages.
Several studies on other species, however, have revealed flexible development
of RMR and body temperature (e.g. Schew,
1995
; Brzek and Konarzewski,
2001
), body composition (e.g.
Moe et al., in press
) and
skeletal growth (e.g. Emlen et al.,
1991
) in response to temporal food shortage.
We did not monitor the changes in RMR and body temperature over the course
of the diet restriction period, which is purported to be necessary to detect
adaptive responses (Schew and Ricklefs,
1998). However, the observed reduction in RMR may have an adaptive
significance in lessening the detrimental effects of food shortage and
increasing survival. Alternatively, the low RMR resulted from pathological
changes or as a passive effect of lack of nutrients (`imposed response';
Schew and Ricklefs, 1998
).
Deleterious pathological changes probably did not occur. Diet-restricted shag
nestlings resumed normal body mass growth immediately at the onset of
re-alimentation (B.M., S.B., D.M., T.E.B. and C.B., unpublished data),
indicating that the cellular structures responsible for growth and metabolism
were intact. Lack of nutrients also seems unlikely because the structural
growth was maintained so well, indicating that nutrients could have been
devoted to basal metabolism at the expense of structural growth. However,
different nutrients may limit basal metabolism compared with structural growth
(energy nutrients versus structural nutrients).
If the observed differential developmental plasticity is adaptive and
results from adaptations, what could be the selective factors for low RMR and
high skeletal growth rates in response to food shortages? Frequent
unpredictable fluctuations in food availability
(Schew and Ricklefs, 1998;
Konarzewski and Starck, 2000
)
are purported to select for low RMR. A recent experiment by Kitaysky
(1999
) showed greater
metabolic responses to food shortage in the piscivorous horned and tufted
puffins (Fratercula corniculata and Lunda cirrhata), which
rely on fluctuating food resources, compared with the planktivorous crested
and parakeet auklets (Aethia cristatella and Cyclorhinchus
psittacula), which rely on continuously available food resources.
However, this could also have a phylogenetic explanation because the puffins
also behaved more similarly to each other than they did to the auklets. Brzek
and Konarzewski (2001
)
demonstrated a reduced RMR in diet-restricted sand martin nestlings, a
response that was amplified by the presence of hungry siblings. Therefore,
they suggested a link between developmental flexibility of RMR and sibling
competition.
Sibling competition has also been suggested to select against slowing of
growth and maturation, especially the parts of the skeleton most important in
competing with nest mates for food, because slowing of growth of such parts
would decrease the competitive abilities of the individual nestling
(Schew and Ricklefs, 1998).
Within broods with established size hierarchies due to hatching asynchrony
(Stokland and Amundsen, 1988
),
structural size may determine the ability to obtain the optimal position in
the nest for begging (Ryden and Bengtsson,
1980
; Bengtsson and Ryden,
1981
; Gottlander,
1987
; McRae et al.,
1993
).
By contrast, it has been argued
(Ricklefs, 1993;
Schew and Ricklefs, 1998
) that
hatching asynchrony could relax the selection to maintain a rigid growth
trajectory in response to temporal food shortage, because hatching order
predetermines the rank in the competitive hierarchy within the brood. However,
an established rank in the hierarchy does not necessarily prevent competition
within asynchronous broods. Amundsen and Stokland
(1988
) manipulated the degree
of asynchrony in nestling European shags and emphasised the importance of the
magnitude of the size disparities within the brood, and not only the rank in
the hierarchy. Therefore, we believe the competitive abilities of European
shag nestlings are sensitive to growth changes as a response to temporal food
shortage.
Sibling competition is not the only possible selective factor for a rigid
skeletal growth trajectory, since it has also been reported in species
producing a single chick. Chicks of the grey-headed albatross (Diomedea
chrysostoma; Reid et al.,
2000) showed a general rigid structural growth, while Atlantic
puffin chicks (Fratercula arctica;
Øyan and Anker-Nilssen,
1996
) showed a high priority to growth of feathers and skull in
response to food shortage. Both studies, however, emphasised the importance of
structures responsible for early fledging and early post-fledging
survival.
Slowing of structural growth as a response to food shortage usually delays
developmental time (e.g. Emlen et al.,
1991; Lepczyk and Karasov,
2000
). Delayed fledging is disadvantageous in species with high
risk of nest predation, and nestling European shags are exposed to predation
(e.g. from the great black-backed gull, Larus marinus). Because
predation rates are regarded as a selective factor for growth rate and
developmental time (Remes and Martin,
2002
), predation may also be a selective factor for reduced
plasticity in structural growth in the European shag.
In conclusion, we have shown that nestling European shags exhibit substantial energy saving as a response to temporal food shortage, and that reductions in Tb and in the size of the liver serve as important physiological processes behind the energy saving. In contrast to reductions in most visceral organs and muscles, the overall structural growth was very well maintained, showing nearly the same age-specific growth rate as the controls. These physiological and morphological responses demonstrate differential developmental plasticity in the European shag nestlings.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Amundsen, T. and Stokland, J. N. (1988). Adaptive significance of asynchronous hatching in the shag a test of the brood reduction hypothesis. J. Anim. Ecol. 57,329 -344.
Bakken, G. S. (1992). Measurement and application of operative and standard operative temperatures in ecology. Am. Zool. 32,194 -216.
Barrett, R. T., Røv, N., Loen, J. and Montevecchi, W. A. (1990). Diet of Shags Phalacrocorax aristotelis and Cormorants P. carbo in Norway and possible implications for gadoid stock recruitment. Mar. Ecol. Prog. Ser. 66,205 -218.
Bech, C. and Østnes, J. E. (1999). Influence of body composition on the metabolic rate of nestling European shags (Phalacrocorax aristotelis). J. Comp. Physiol. B 169,263 -270.
Beintema, A. J. and Visser, G. H. (1989). The effects of weather on time budgets and development of chicks of meadow birds. Ardea 77,181 -192.
Bengtsson, H. and Ryden, O. (1981). Development of parent-young interaction in asynchronously hatched broods of altricial birds. Z. Tierpsychol. 56,255 -272.
Birkhead, T. R., Fletcher, F. and Pellatt, E. J. (1999). Nestling diet, secondary sexual traits and fitness in the zebra finch. Proc. R. Soc. Lond. B. 266,385 -390.[CrossRef]
Boersma, P. D. (1986). Body temperature, torpor, and growth of chicks of fork-tailed storm petrels (Oceanodroma furcata). Physiol. Zool. 59, 10-19.
Bradshaw, A. D. (1965). Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13,115 -155.
Brzek, P. and Konarzewski, M. (2001). Effect of
food shortage on the physiology and competitive abilities of sand martin
(Riparia riparia) nestlings. J. Exp. Biol.
204,3065
-3074.
Burness, G. P., Ydenberget, R. C. and Hochachka, P. W. (1998). Interindividual variability in body composition and resting oxygen consumption rates in breeding tree swallows, Tachycineta bicolor. Physiol. Zool. 71,247 -256.[Medline]
Chappell, M. A., Bech, C. and Buttemer, W. A.
(1999). The relationship of central and peripheral organ masses
to aerobic performance variation in House sparrows. J. Exp.
Biol. 202,2269
-2279.
Christians, J. K. (1999). Controlling for body mass effects: is part-whole correlation important? Physiol. Biochem. Zool. 72,250 -253.[CrossRef][Medline]
Daan, S., Masman, D. and Groenewold, A. (1990). Avian basal metabolic rates: their association with body composition and energy expenditure in nature. Am. J. Physiol. 259,333 -340.
De Kogel, C. H. (1997). Long-term effects of brood size manipulation on the morphological development and sex-specific mortality of offspring. J. Anim. Ecol. 66,167 -178.
Drent, R. H. and Klaassen, M. (1989). Energetics of avian growth: the causal link with BMR and metabolic scope. In Physiology of Cold Adaptation in Birds (ed. C. Bech and R. E. Reinertsen), pp. 349-359. New York: Plenum.
Dufty, A. M., Clobert, J. and Møller, A. P. (2002). Hormones, developmental plasticity and adaptation. Trends Ecol. Evol. 17,190 -196.[CrossRef]
Emlen, S. E., Wrege, P. H., Demong, N. J. and Hegner, R. E. (1991). Flexible growth rates in nestling white-fronted bee-eaters: a possible adaptation to short-term food shortage. Condor 93,591 -597.
Gottlander, K. (1987). Parental feeding behaviour and sibling competition in the pied flycatcher Ficedula hypoleuca. Ornis. Scand. 18,269 -276.
Hayes, J. P. and Shonkwiler, J. S. (1996). Analyzing mass-independent data. Physiol. Zool. 69,974 -980.
Kitaysky, A. S. (1999). Metabolic and developmental responses of alcid chicks to experimental variation in food intake. Physiol. Biochem. Zool. 72,462 -473.[CrossRef][Medline]
Klaassen, M. and Drent, R. H. (1991). An analysis of hatchling basal metabolism: in search of ecological correlates that explain deviations from allometric relations. Condor 93,612 -629.
Konarzewski, M. and Starck, J. M. (2000). Effects of food shortage and oversupply on energy utilization, histology and function of the gut in nestling Song thrushes (Turdus philomelos). Physiol. Biochem. Zool. 73,416 -427.[CrossRef][Medline]
Konarzewski, M., Kowalczyk, J., Swierubska, T. and Lewonczuk, B. (1996). Effect of short-term feed restriction, realimentation and overfeeding on growth of song thrush (Turdus philomelos) nestlings. Funct. Ecol. 10, 97-105.
Lepczyk, C. A. and Karasov, W. H. (2000). Effect of ephemeral food restriction on growth of house sparrows. Auk 117,164 -174.
Lindström, J. (1999). Early development and fitness in birds and mammals. Trends Ecol. Evol. 14,343 -348.[CrossRef][Medline]
Lorentsen, S.-H. (2001). The national monitoring programme for seabirds. Results including the breeding season 2001. Norwegian Institute for Nature Research. NINA Oppdragsmelding 726,1 -36.
Martin, T. E. (1987). Food as a limit on breeding birds: a life-history perspective. Ann. Rev. Ecol. Syst. 18,453 -487.[CrossRef]
McRae, S. B., Weatherhead, P. J. and Montgomerie, R. (1993). American robin nestlings compete by jockeying for position. Behav. Ecol. Sociobiol. 33,101 -106.
Meerlo, P., Bolle, L., Visser, G. H., Masman, D. and Daan, S. (1997). Basal metabolic rate in relation to body composition and daily energy expenditure in the field vole, Microtus agrestis. Physiol. Zool. 70,362 -369.[Medline]
Metcalfe, N. B. and Monaghan, P. (2001). Compensation for a bad start: grow now, pay later? Trends Ecol. Evol. 16,254 -260.[CrossRef][Medline]
Moe, B., Stølevik, E. and Bech, C. (in press). Ducklings exhibit substantial energy saving mechanisms as a response to short-term food shortage. Physiol. Biochem. Zool.
Murphy, M. E. (1996). Nutrition and metabolism. In Avian Energetics and Nutritional Ecology (ed. C. Carey), pp. 31-60. New York: Chapman and Hall.
Niimi, A. J. (1978). Lag adjustments between estimated and actual physiological responses conducted in flow-through systems. J. Fish. Res. Bd Can. 35,1265 -1269.
Olson, J. M. (1992). Growth, the development of endothermy, and the allocation of energy in red-winged blackbirds (Agelaius phoenicus) during the nestling period. Physiol. Zool. 65,124 -152.
Østnes, J. E., Jenssen, B. M. and Bech, C. (2001). Growth and development of homeothermy in nestling European shags (Phalacrocorax aristotelis). Auk 118,983 -995.
Øyan, H. S. and Anker-Nilssen, T. (1996). Allocation of growth in food-stressed Atlantic Puffin chicks. Auk 113,830 -841.
Piersma, T. and Lindstrøm, Å. (1997). Rapid reversible changes in organ size as a component of adaptive behviour. Trends Ecol. Evol. 12,134 -138.[CrossRef]
Pigliucci, M. (2001). Phenotypic plasticity. Beyond Nature and Nurture. Baltimore: The Johns Hopkins University Press.
Prinzinger, R. and Siedle, K. (1988). Ontogeny of metabolism, thermoregulation and torpor in the house martin Delichon u. urbica (L.) and its ecological significance. Oecologia 76,307 -312.
Reid, K., Prince, P. A. and Croxall, J. P. (2000). Fly or die: the role of fat stores in the growth and development of Grey-headed Albatross Diomedea chrysostoma chicks. Ibis 142,188 -198.
Remes, V. and Martin, T. E. (2002). Environmental influences on the evolution of growth and developmental rates in passerines. Evolution 56,2505 -2518.[Medline]
Ricklefs, R. E. (1993). Sibling competition, hatching asynchrony, incubation period, and lifespan in altricial birds. In Current Ornithology, vol. 11 (ed. D. Power), pp. 199-276. New York: Plenum Press.
Ricklefs, R. E. and White, S. C. (1981). Growth and energetics of chicks of the Sooty tern (Sterna fuscata) and Common tern (S. hirundo). Auk 98,361 -378.
Ricklefs, R. E., Shea, R. E. and Choi, I. H. (1994). Inverse relationship between functional maturity and exponential growth rate of avian skeletal muscle: a constraint on evolutionary response. Evolution 48,1080 -1088.
Ricklefs, R. E., Starck, J. M. and Konarzewski, M. (1998). Internal constraints on growth in birds. In Avian Growth and Development (ed. J. M. Starck and R. E. Ricklefs), pp. 266-287. New York: Oxford University Press.
Ryden, O. and Bengtsson, H. (1980). Differential begging and locomotory behaviour by early and late hatched nestlings affecting the distribution of food in asynchronously hatched broods of altricial birds. Z. Tierpsychol. 53,209 -224.
Schew, W. A. (1995). The evolutionary significance of developmental plasticity in growing birds. PhD Thesis. University of Pennsylvania, Philadelphia.
Schew, W. A. and Ricklefs, R. E. (1998). Developmental plasticity. In Avian Growth and Development (ed. J. M. Starck and R. E. Ricklefs), pp.288 -304. New York: Oxford University Press.
Schlichting, C. D. and Pigliucci, M. (1998). Pheotypic Evolution. A Reaction Norm Perspective. Sunderland: Sinauer Associates.
Schmalhausen, I. I. (1949). Factors of Evolution. Philadelphia: Blakiston. Reprinted 1986 in Chicago: Chicago University Press.
Schmidt-Nielsen, K. (1990). Animal Physiology: Adaptation and Environment. Cambridge: Cambridge University Press.
Scott, I. and Evans, P. R. (1992). The metabolic output of avian (Sturnus vulgaris, Calidris alpina) adipose tissue liver and skeletal muscle: implications for BMR/Body mass relationships. Comp. Biochem. Physiol. A 103,329 -332.[CrossRef]
Smith-Gill, S. J. (1983). Developmental plasticity: developmental conversion versus phenotypic modulation. Am. Zool. 23,47 -55.
Starck, J. M. and Ricklefs, R. E. (1998). Variation, constraint, and phylogeny. Comparative analysis of variation in growth. In Avian Growth and Development (ed. J. M. Starck and R. E. Ricklefs), pp. 247-265. New York: Oxford University Press.
Starck, J. M. and Chinsamy, A. (2002). Bone microstructure and developmental plasticity in birds and other dinosaurs. J. Morphol. 254,232 -246.[CrossRef][Medline]
Stokland, J. N. and Amundsen, T. (1988). Initial size hierarchy in broods of the shag: relative significance of egg size and hatching asynchrony. Auk 105,308 -315.
Velando, A., Ortega-Ruano, J. E. and Freire, J. (1999). Chick mortality in European shag Stictocarbo aristotelis related to food limitations during adverse weather events. Ardea 87,51 -59.
Velando, A., Graves, J. and Freire, J. (2000). Sex-specific growth in the European shag Strictocarbo aristotelis, a sexual dimorphic seabird. Ardea 88,127 -136.
Weathers, W. W. (1996). Energetics of postnatal growth. In Avian Energetics and Nutritional Ecology (ed. C. Carey), pp. 461-496. New York: Chapman and Hall.
Weber, T. P. and Piersma, T. (1996). Basal metabolic rate and the mass of tissues differing in metabolic scope: migration-related covariation between individual knots Calidris canatus.J. Avian Biol. 27,215 -224.
Withers, P. C. (1977). Measurement of
VO2, VCO2 and evaporative water loss with flow-through
mask. J. Appl. Physiol.
42,120
-123.