Cost-benefit analysis of mollusc eating in a shorebird I. Foraging and processing costs estimated by the doubly labelled water method
1 Department of Marine Ecology and Evolution, Royal Netherlands Institute
for Sea Research (NIOZ), PO Box 59, 1790 AB Den Burg, Texel, The
Netherlands
2 Animal Ecology Group, Centre for Ecological and Evolutionary Studies,
University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands
3 Centre for Isotope Research, University of Groningen, Nijenborgh 4, 9747
AG Groningen, The Netherlands
* Author for correspondence (e-mail: janvg{at}nioz.nl)
Accepted 8 June 2003
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Summary |
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Key words: aviary experiment, bivalve, Calidris canutus, cost-benefit analysis, digestion, doubly labelled water, energetics, food selection, foraging, prey quality
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Introduction |
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A case in point is the shorebird species studied by our group during the
last decade, the red knot Calidris canutus. This species is a
specialised molluscivore (Zwarts and
Blomert, 1992; Piersma et al.,
1993a
,
1998
,
in press
), often eating rather
poor quality prey types, i.e. low ratios of digestible flesh to shell
(Zwarts and Wanink, 1991
;
Visser et al., 2000
). Red
knots have a large but variable digestive machinery, the gizzard and intestine
especially showing strong variation
(Piersma et al., 1993b
;
Dekinga et al., 2001
;
Piersma, 2002
;
Battley and Piersma, in press
).
Experimental work has indicated that digestive constraints, and possibly the
costs of maintaining a large digestive tract, may be critical in shaping their
foraging decisions (van Gils et al.,
2003a
). Here we present an analysis of energy expenditure of red
knots in different foraging situations, estimated by the turnover of stable
isotopes over experimental periods of 11 h. These energy expenditure levels
are to be interpreted in the context of a cost-benefit analysis of the size
and capacity of the digestive organ system.
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Materials and methods |
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Experimental arena: the NIOZ-indoor tidodrome
The trials were performed in either a large (7.3 mx8.0 mx 3.0
m, lengthxwidthxheight) indoor aviary or a smaller adjacent aviary
(4.7 mx1.1 mx2.5 m, lengthxwidthxheight). The bottom
of the large aviary consisted of a layer (20 cm deep) of wet sand from the
Wadden Sea. The basin could be filled with a layer of seawater, simulating
high tides. The smaller, roost-site aviary, separated from the large tidal
aviary with a sliding door, had a hard floor that was continuously wetted by
seeping of seawater. Together, the two aviaries simulated an intertidal system
with a low-tide foraging area and a high-tide roost, respectively; hence the
name `tidodrome'.
During the experiment the entire tidodrome was maintained at air
temperatures between 16°C and 20°C, at the lower end of the
thermoneutral zone of red knots (Wiersma
and Piersma, 1994), and a relative humidity between 55% and 75%.
Between 20.00 h and 08.00 h the large aviary was flooded with 14 cm seawater
(`high tide'), during which the experimental birds used the small aviary with
only small night-lights on. During the day the sandy bottom in the large
aviary (the intertidal area) was exposed.
Red knots and cockles
This study is based on measurements of five red knots Calidris
canutus L. (three males, two females). A sixth bird (included in the
analyses by Visser et al.,
2000) had a breast wound. Although it participated in some of the
trials, we have not used the data in the present analysis, as a bird with an
incomplete plumage and a damaged skin might bias our estimates of the various
cost factors.
The birds were captured in the Dutch Wadden Sea 9 months before the start
of the experiment and were thus accustomed to captive conditions and frequent
handling. Before the experiment the birds had been fed protein-rich food
pellets ad libitum (Trouvit, Trout Nutrition, The Netherlands;
containing 5.6% water, 48% crude protein and 12% crude fat). 3 weeks before
the first trial, the birds were shifted to a diet of cockles only (ad
libitum), to adjust their digestive tract to a diet of hard-shelled
molluscs. Experiments have shown such adjustments to take less than a week
(Dekinga et al., 2001). During
this training period, the mean mass of the five birds decreased from
128.0±8.3 g (mean ± S.D.) to 113.4±8 g on the
day before the first trial (5 January, 1998).
Prior to each of the separate trials, cockles were freshly collected from
an intertidal flat close to the island of Texel in the western Dutch Wadden
Sea. We determined the following relationship between shell length
(L, mm) and the ash-free dry mass of the soft parts of the cockle
(MAFD, mg):
MAFD=0.006622xL2.840
(N=77, r2=0.89); these values indicate that the
collected cockles were in their normal winter condition (cf.
Zwarts, 1991). The length of
the cockles on offer varied between 6 mm and 15 mm, and they contained 68.6%
water, 29.8% dry shell matter and only 1.6% ash-free dry matter of soft mass
(i.e. digestible `meat').
Experimental protocol and behavioural observations
During trial 1 (IF-C1; Table
1) the birds fed on live cockles buried in the artificial sand
flat. The birds had to walk and to probe to find the cockles. During trial 2
(R-C), trays with live cockles were offered on the roost, enabling the birds
to eat the cockles without the additional effort of walking and probing. Trial
3 (IF-Cd) consisted of feeding on the artificial mudflat on cockles
that were dying because of anoxic conditions in the sediment. As they do in
the field under similar conditions (A. Dekinga and A. Koolhaas, personal
observation), the red knots used their time to remove the flesh from the open
shells. Although they had to do the walking, there was little need for probing
and they were not ingesting shells that needed crushing. Trial 4
(IF-C2) was a repeat of trial 1, except that the quality of the
cockles on offer (meat per unit shell mass; see
van Gils et al., 2003a) was
16% higher (P=0.005). Trial 5 (RF) studied the birds on the roost
while fasting. Trial 6 (R-P) studied birds on the roost feeding on the soft
pellets. Trial 7 (R-Cm) consisted of red knots feeding on the roost
on cockle meat removed from the shell after immersing them for a few seconds
in boiling water. Trial 8 (IF-F) consisted of searching on the artificial
mudflat for prey that were not there.
The eight trials were of equal length (11 h) and similarly structured, as
follows. The evening before an experimental day, the birds were kept in the
small aviary and fed cockles, supplemented with food pellets during the latter
half of the study. In this way we made sure that the birds were able to
balance their energy budget, as confirmed by the constant body masses
maintained throughout this experiment
(Visser et al., 2000). On the
experimental day, birds were captured at 08.00 h and placed individually in
small cardboard boxes, measuring 15 cmx15 cmx15 cm. In an order
that was repeated at the end of the day, one by one the birds were taken out
of the boxes, and when relevant a blood sample was taken to determine
background levels of the isotopes (see below for procedure; 3 birds for each
trial), and weighed to the nearest 0.1 g on a balance (model BD202; Mettler).
In sequence, they were injected ventrally and subcutaneously with a precisely
known amount of doubly labelled water 2H2O18
(range: 0.4-0.9 g) using an insulin syringe weighed to the nearest 0.1 mg on a
Mettler model AE160 balance before and after administration. The DLW-mixture
was obtained by mixing 2H2O (Aldrich, Milwaukee, USA)
with H218O (Rotem, Rehovot, Israel) to yield
2H and 18O concentrations of 30.4% and 62.7%,
respectively, as assessed from isotope dilution measurements
(Visser and Schekkerman,
1999
).
To avoid potential problems of low isotope enrichment relative to background levels at the end of the trials, the highest doses were given in the trials with cockles (IF-C1, R-C, IF-Cd and IF-C2). The dose was chosen such that the 2H and 18O enrichments of the final samples were at least 150 p.p.m. and 200 p.p.m. above the background levels, respectively. After 1 h in the dark cardboard box without food or water (usually at 9.10 h), the birds were reweighed and an (initial) blood sample was taken from the brachial vein after making a little puncture with a sterile needle (at least six 15 µl samples were taken into glass capillaries that were immediately flame-sealed with a propane torch). Thereafter the birds were released in the experimental aviary until about 20.00 h, when they were recaptured by hand, and placed individually in the cardboard boxes. Repeating the morning sequence, the birds were reweighed and a (final) blood sample taken from the brachial vein in the other wing. Flame-sealed capillaries were stored at 4°C until the isotope analysis, which took place within 2 months of the experiment.
During each of the experimental days, behavioural observations were made through one-way screen windows in the experimental aviaries. During the 11 h experimental periods, a scan was recorded every 5 min during which the behaviour of each individual was categorized as either foraging (i.e. walking and active probing or ingesting), resting (subdivided into standing, sleeping and preening) or - rarely - flying. Assuming that scored activities are representative of the previous 5 min interval, time budgets were calculated for each bird (and for each trial). Individual birds were closely observed four times per hour for 1 min to determine the number of prey swallowed, which enabled us to estimate daily intake rate.
DLW analyses and calculations of daily energy expenditure
Samples were analysed in quadruplicate at the Centre for Isotope Research
(CIO) at the University of Groningen, following the procedures described in
detail by Visser and Schekkerman
(1999), Visser et al.
(2000
) and Jenni-Eiermann et
al. (2002
). Briefly, as a first
step, blood samples were cryogenically distilled in a vacuum line. Next, the
18O/16O isotope ratio was determined in CO2
gas (using the CO2 equilibration method) and, after reduction of
the water sample over a hot (800°C) uranium oven, the
2H/1H isotope ratio was determined in H2 gas
using a SIRA 10 Isotope Ratio Mass Spectrometer (Manchester, UK). In each
batch, a diluted sample of the doubly labelled water (DLW) injectate, together
with four internal laboratory standards that covered the observed enrichment
range of the blood samples, were analysed. These standards were calibrated
against IAEA (International Atomic Energy Agency) standards.
The amount of body water in each individual was determined using the
principle of isotope dilution. For a detailed presentation of the calculated
sizes of the birds' body water pools, see Visser et al.
(2000). Fractional isotope
turnover rates for each isotope were calculated based on the isotope
enrichment of the initial and final samples, the population-specific average
enrichment of the background samples, and the time interval elapsed between
the taking of the initial and final blood samples (equation 2,
Visser et al., 2000
). The
coefficients of variation of the final 2H and 18O
measurements above the background values were 0.8% and 1.3%, respectively. The
rates of CO2 production were calculated for each measurement period
using Speakman's equation 7.17 (Speakman,
1997
), which takes into account fractionation effects of the
2H and 18O isotopes, assuming that 25% of the water
efflux was lost through evaporative pathways. In an accompanying study, during
which the DLW method was validated against respiration gas analyses in birds
fed different diets (to induce different rates of water efflux), this equation
has proved to yield the most robust estimates of CO2 production
rates (G. H. Visser, A. Dekinga, J. A. Gessaman, E. R. Th. Kerstel, and T.
Piersma, manuscript in preparation), and measurements were taken over the same
time intervals as applied in the present study.
As a last step, the rates of CO2 production were converted to
energy expenditure values using an energy equivalent of 27.3 kJ l-1
CO2, which is appropriate for diets with very high protein content
(Gessaman and Nagy, 1988).
Statistics
Because of the hierarchically structured design of the experiment
(individual observations nested within trials), we used a hierarchical linear
model (i.e. mixed model or multilevel model) to test for the effects of the
treatments on metabolic rate. These treatments (foraging, crushing and
digestive processing) were entered as categorical variables (either 0 or 1),
and trial, denoting the nesting of the observations, was entered as the
identifier variable. We allowed the intercept to vary across trials, i.e. we
used a random intercept model. The test was performed using the MIX procedure
in SYSTAT 10 (SPSS Inc., Chicago, IL, USA). We used the same type of model to
test for the success of the manipulations. The percentage of time spent
foraging was arcsine-square-root transformed before analysis.
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Results |
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Under this range of experimental conditions the energy expenditures of red knots varied between 1.5 W when not foraging, to over 4 W when working and eating (Fig. 2). The energy expenditures in different foraging contexts (Fig. 2) also indicate (1) that foraging activity (even when not accompanied by actual food intake) is more costly than active rest, (2) that the act of ingesting food items, whether these items are of a soft or a hard-shelled nature, adds importantly to the expenditure level, but (3) that the additional costs of crushing the hard-shelled prey items are small or negligible. A hierarchical analysis of variance (ANOVA; Table 2A) confirms that the additional effect of crushing on energy expenditure is non-significant, which leads to a simplified model that only considers whether food is eaten regardless of prey type (Table 2B).
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To see whether the cost of crushing was nevertheless significant in more controlled pairwise comparisons, we tested for differences in metabolic rates between trials that only differed in whether prey needed to be crushed or not (again using a hierarchical linear model). For both comparisons there again appeared to be no significant metabolic cost of crushing (P=0.887 for the comparison between trials 1 and 4 vs 3; P=0.670 for trial 2 vs 6 and 7).
The cost of maintenance plus limited activity is estimated at 1.665 W (Table 2B). Foraging adds 0.602 W and digestive processing another 1.082 W. Accounting for these three factors, only a small part of the overall variance in energy expenditure remained unexplained. Note that the standard errors were more or less similar for the three components, but were largest relatively for foraging, the smallest component of the energy budget.
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Discussion |
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The digestive processing cost is mainly represented by the energy (heat)
losses due to inefficiencies in intermediary metabolism
(Klasing, 1998). This cost,
often called `Heat Increment' or `Heat Increment of Feeding' (HIF), was
estimated at 17% of the metabolizable energy intake in kestrels Falco
tinnunculus (Masman et al.,
1989
) and at 20% in brent geese Branta bernicla
(Sedinger et al., 1992
). These
values are lower than the contribution of the processing cost to energy
expenditure estimated here (32%). This high value may be due to the highly
proteinaceous diet offered to red knots. In chickens, HIF is considered to be
30% for protein, 15% for starch and 10% for lipids
(Klasing, 1998
).
Alternatively, since the habit of ingesting entire shell fish is accompanied
by the ingestion of huge amounts of water (up to 300 g per trial;
Visser et al., 2000
), heat
loss to the ingested cold water pool (up to 0.58 W) could be part of the
explanation as to why the digestive processing cost is relatively high in red
knots.
Crushing hard-shelled prey did not add significantly to the hierarchical
linear model of cost factors to explain the variance in energy expenditure
levels (Table 2A). Apparently,
the activity of the muscular gizzard is small compared with the other costs of
digestion that relate to processes in the intestinal tract and the liver.
Considering the limited action taking place in the gizzard of red knots (a few
seconds of crushing immediately followed by the evacuation of prey remains
into the intestine, rather than the longer lasting pre-digestion in the
proventriculus and grinding in the gizzard of many other birds;
Klasing, 1998), the small and
immeasurable cost of `crushing' should perhaps not have surprised us. This low
energetic cost of crushing is in sharp contrast to the high overall
time costs involved in the digestive processing of shelled prey items
(van Gils et al., 2003a
).
Finally, we note that the cost of active rest (i.e. 1.665 W, the intercept
of the hierarchical linear model), is much higher than the predicted value for
basal metabolic rate (BMR) of ca. 1 W
(Piersma et al., 1996).
Although the birds were maintained at thermoneutrality, they did not sleep for
most of the time (as they would during the measurement of BMR in darkness),
and although they did not walk much, they went through daily routines such as
bathing and preening. Just being awake and carrying out minimal activities
apparently costs about half as much as being asleep (BMR).
Validation in an outdoor experiment
The present study took place in thermoneutrality, a condition that red
knots only encounter in the tropics
(Wiersma and Piersma, 1994).
In colder environments, knots need to produce heat to stay warm. Whether in
our total budget calculations we can simply add these thermoregulatory costs
to the estimated foraging and processing costs depends on the type of energy
budget model that is used. Additive models assume that this thermoregulatory
heat needs to be generated as an extra by shivering; substitution models
assume that heat generated as a byproduct of metabolic processes can (partly)
substitute for the thermoregulatory heat. A preliminary study under outdoor
conditions using similar experimental techniques and isotope analyses
(Poot and Piersma, 1994
;
Fig. 3) allowed us a
preliminary test among the two models.
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Red knots were allowed to feed on shellfish buried in an intertidal flat
(comparable to our IF-C conditions in Table
1). Over the 24 h period of the DLW measurements, these birds only
had access to the flat for 7.2 h on average, when they were actively feeding
for 71% of their time. Assuming that these birds were maximizing their daily
net energy intake, the remaining 29% of their available foraging time was
probably lost to digestive breaks (cf. van
Gils et al., 2003b). Therefore, foraging costs (0.602 W) were made
for only 71% x 7.2 h per day, HIF costs (1.082 W) for 7.2 h per day, and
resting costs (1.665 W) for 24 h per day. Adding a thermoregulatory cost of
0.88 W that Poot and Piersma
(1994
) estimated from
measurements with heated taxidermic mounts (see
Wiersma and Piersma, 1994
),
the additive energy budget model predicts a daily average metabolic rate
(ADMR) of 3.00 W (Fig. 3). The
substitution model predicts an ADMR of 2.72 W, which is based on the
assumption that a 100% of the heat increment of feeding and 30% of the heat
generated by walking is substitutable (the latter estimate is based on
calculations by Bruinzeel and Piersma,
1998
). The outdoor data averaged 3.17±0.27 W (mean ±
S.E.M., N=12), a value that is not different from the
predictions of either the additive model (P>0.45) or the
substitution model (P>0.10). Although this result does not allow
us to conclusively state whether thermoregulatory heat can be substituted for,
the data indicate that the different cost components estimated indoors may be
robust. This should allow us to use them as predictions for field situations
(van Gils et al., 2003a
).
A cost-benefit analysis
With the estimates for the different cost components at hand
(Table 2B), in combination with
the empirical function relating rate of energy intake to gizzard mass
(van Gils et al., 2003a), we
could calculate an energy-based cost-benefit analysis of the gizzard mass of
red knots (Fig. 4); for the
details of this analysis, see Appendix in the accompanying paper
(van Gils et al., 2003a
). With
an increase in gizzard mass, two processes are implicated. Foremost, intake
rate can be increased (being a quadratic function of gizzard mass;
van Gils et al., 2003a
).
Secondly, a portion of this extra gain disappears due to increases in HIF,
resting and foraging costs. HIF increases simply because food is processed at
a higher rate, resting costs increase (slightly) because larger organs require
larger maintenance costs (BMR), and foraging costs increase (slightly) because
higher locomotory costs are required to carry around the heavier body. These
latter two mass-related costs increase at double speed since a change in
gizzard mass is accompanied by a similar change in intestine mass
(Table 3; Battley and Piersma, in press
).
Under the conditions of the experiment, for gizzard mass higher than 8 g, the
potential intake rate actually exceeds the concomitant cost levels until a
plateau (set by other parts of the digestive system) is reached at gizzard
mass 11-12 g. At this level net intake rate would be maximised
(van Gils et al., 2003a
).
Fig. 4 shows that the
experimental knots kept their energy budget just balanced during the foraging
period. It follows that the birds would have been unable to survive on this
prey type in the field, as the energy budget while foraging should be positive
to compensate for the loss of energy during the high-tide roosting period. We
predict that red knots facing bivalve prey of similar quality in the field as
in the experiment would have larger gizzards. This appears to be the case
(van Gils et al., 2003a
).
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Acknowledgments |
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