Effects of intake rate on energy expenditure, somatic repair and reproduction of zebra finches
Zoological Laboratory, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands
* Author for correspondence at present address: Department Evolution, Ecology and Organismal Biology, Ohio State University, 288 Aronoff Lab, 318 W 12th Avenue, Columbus, OH 43210, USA (e-mail: wiersma.6{at}osu.edu)
Accepted 23 August 2005
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Summary |
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We hypothesize that energy is saved at the expense of `condition', and we tested this hypothesis in two ways. Firstly, we tested the effect of intake rate on the replacement of two plucked tail feathers (a form of somatic repair). Replacement feathers were shorter when intake rate was low, indicating an effect of intake rate on somatic repair ability. Secondly, we tested for carry-over effects of intake rate on reproduction, by giving pairs the opportunity to reproduce with access ad libitum to food after feeding on one of the three chaff/seed ratios for 6 weeks. The interval until laying the first egg increased with decreasing intake rate in the preceding 6 weeks. The effects of intake rate on somatic maintenance and reproduction may explain why birds sustained higher metabolic rates than apparently necessary, but the physiological mechanisms determining the optimal metabolic rate remain to be discovered.
Key words: food availability, basal metabolic rate, ptilochronology, Taeniopygia guttata
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Introduction |
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An explanation for this counterintuitive result may lie in the structure of
the reward schedule, because in starlings the foraging motivation depends on
the variation in reward rate: when food was earned by performing a fixed
number of flights, daily food intake and body mass decreased when the number
of flights required per reward was increased, while within a trial both
remained constant when the number of flights needed to obtain a reward was
variable (Fotheringham, 1998).
Hence, identical mean foraging intake rates that differ only in short-term
variation around the mean may result in very different energy budgets (see
discussion in Kacelnik and Bateson,
1996
). Thus the findings of Deerenberg et al.
(1998
) and Bautista et al.
(1998
) that DEE decreased with
decreasing intake rates may be explained by the use of fixed reward rates in
these studies. Indeed, Wiersma et al.
(2005
) offered starlings
variable reward rates and showed an increase in DEE when foraging costs were
increased beyond those used by Fotheringham
(1998
). In this paper we test
whether zebra finches (like the starlings) increase DEE with decreasing intake
rate when foraging reward rate is variable. We further explore the
consequences of intake rate for reproduction and an aspect of somatic
repair.
Following Lemon (1991), we
created lower intake rates by mixing seeds with increasing amounts of chaff.
In this foraging environment the reward rate is variable, and we therefore
predicted that DEE would increase with increasing chaff/seed ratio. Lemon
(1991
) previously showed that
fitness was lower when more chaff was mixed through the seeds (see also
Spencer et al., 2003
), and he
constructed an energy budget to explain this result. Although intake rate was
strongly affected by the treatment, Lemon
(1993
) did not find
differences in DEE between the experimental groups. However, he constructed
energy budgets indirectly, using a summation of separately measured existence
metabolism values of fasting birds and foraging costs, and if nocturnal
savings occurred (as in Deerenberg et al.,
1998
) these may have concealed differences in diurnal energy
expenditure. Therefore, we used respirometry to measure effects of food intake
rates on energy expenditure separately for the diurnal and nocturnal
phase.
The conditional occurrence of energetic compensation begs the question what
the costs are to a reduction in metabolic rate below levels found under benign
conditions. Possibly, energy is saved by reallocation to foraging from
maintenance and repair processes (e.g. oxidative protection,
Wiersma et al., 2004; or
immune function, Verhulst et al.,
2005
). As an indicator of resource allocation to somatic repair,
we tested whether induced feather growth was affected by foraging costs. This
method has previously been shown to reveal nutritional stress and effects of
parental effort (e.g. Grubb, Jr et al.,
1991
; White et al.,
1991
; Nilsson et al.,
1993
; Jenkins et al.,
2001
). Additionally, we tested for carry-over effects of
manipulated foraging costs on reproductive output by giving birds the
opportunity to breed after being exposed for 6 weeks to different levels of
intake rate. Lemon (1991
)
previously showed that reproductive success, in particular the laying interval
between successive clutches, depends on intake rate, but his birds were
permanently exposed to the different treatments. His finding may therefore be
the combined result of instantaneous effects of the daily energy surplus and
longer term effects on parental condition that affect reproduction, and we
tested the latter hypothesis. Lastly, to evaluate the generality of our
findings regarding effects of intake rate on DEE, we provide an overview of
studies that manipulated intake rate and measured the consequences for
foraging effort, daily energy expenditure and basal metabolic rate.
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Materials and methods |
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Experiment 1: Feeding time and energetics
Twelve single-sex pairs of wild-type zebra finches (6 pairs of each sex)
were all subjected to the three different chaff/seed ratios. After 1 week of
acclimatization on a particular chaff/seed ratio we measured energy
expenditure for 22-23 h in an open-flow respirometer, and this was repeated at
three different temperatures (12, 22 and 32°C) at 3-day intervals. During
these measurements the pair had access to food in the same chaff/seed ratio as
in the preceding week. According to Calder
(1964), 32°C is within the
thermoneutral zone; 22°C resembles the temperature in the holding room;
measurements at 12°C served to test whether nocturnal saving depended on
overall energetic demands. After measuring metabolic rate at the three ambient
temperatures the chaff/seed ratio for that pair was changed, and the procedure
was repeated. We arranged the order of chaff/seed ratios and measurement
temperatures in such a way that treatments and measurement order were not
correlated.
The metabolic measurements were done on the two birds of a pair
simultaneously, for several reasons: (i) to increase oxygen consumption rates,
and hence measurement precision, (ii) to reduce the variance between
measurements, because some averaging is taking place, which increases the
statistical power, and (iii) because the zebra finch is a gregarious species,
it may be more at ease when housed with a conspecific. Although individual
variation becomes less clear with this approach, we considered it preferable
because of the advantages mentioned. Significant repeatability of resting
metabolic rate (RMR) has previously been demonstrated for the zebra finch
(Vézina and Williams,
2005). In the metabolic chamber the two birds were separated by a
transparent partition, so they could see and hear each other but not interact
physically. Measurements of oxygen consumption (using a paramagnetic Servomex
Xentra 4100 analyzer, Crowborough, UK), carbon dioxide production (Servomex
1440) and air flow rate (Brooks 5850S mass-flow controllers, Rijswijk, The
Netherlands) were stored every sixth minute. Mass-flow controllers had been
calibrated using a bubble flow meter
(Levy, 1964
). The respirometer
system was calibrated before each measurement using two 3-digit precision gas
mixtures (N2 with 20.0% O2/0.0% CO2 or 21.0%
O2/1.0% CO2). Dry air was pumped through the 24 l,
Plexiglas respirometer boxes at a rate of 36 l h-1. The air was
dried over a molecular sieve (3Å, Merck, Darmstadt, Germany). The
metabolic rate (MR) was calculated from the oxygen consumption rate using the
RQ-dependent conversion factor as given by Brody
(1945
). All MR measurements
were divided by 2 to obtain values per bird. Before and after the measurement
we measured body mass to the nearest 0.1 g. BMR was defined as the minimum
metabolic rate at thermoneutral temperatures measured during the resting phase
of post-absorptive birds. Since measurements did not cover the whole daylight
period (2-3 h were missing in the middle of the day due to time needed to
exchange birds and for the respirometer system to stabilise), we used the
average of the end and start of the measurement as an estimate for the missing
period to estimate energy expenditure over the whole daylight period.
From a subset of respirometry sessions (N=45) we made 1.5 h video recordings of the feeding behaviour of single birds, starting at the onset of the light period (9:00 h). Due to the position of the camera we could not observe the whole metabolic chamber, and when analyzing the video recordings we only scored the time spent foraging. Activity (presence/absence of movement) was recorded continuously with passive infrared sensors (PIRs) in the metabolic chambers. The PIRs did not distinguish between the two individuals. PIRs sampled movement approximately every second, and `activity' was defined as the proportion of samples with movement. Individual sensors differed in sampling rate, and therefore we corrected for the maximum output of all measurements made by individual PIRs. Pairs were always measured in the same chamber.
Experiment 2: Feather growth and reproduction
Following the metabolic measurements we formed 24 female-male pairs, which
were each maintained on one of the three chaff/seed ratios for 6 weeks (8
pairs for each seed/chaff ratio). We measured the amount of food consumed by
weighing the seeds remaining in the food tray 48 h afterpresenting the food.
This was repeated twice more at weekly intervals. We removed the left and
right outer tail feathers of 12 pairs at the start of the 6 weeks. Length of
the new feathers was measured using a ruler 12 days after feather removal by
an observer who was `blind' with respect to the treatment, and subsequently at
4-8 day intervals. We took the maximum recorded new feather length as an
estimate of the length of the newly formed feather. 6 weeks after feather
removal the new feathers had ceased to grow and the newly formed feathers were
removed and measured.
After 6 weeks all 24 pairs were given a diet with seeds only (i.e. no chaff) and a nest box and nesting material to measure carry-over effects of the chaff/seed ratio on subsequent reproductive output. We recorded day of laying the first egg, clutch size, egg mass, brood size and fledgling number. The first 3 days after the diet switch we measured seed consumption by reweighing the offered seeds at 24 h intervals.
Statistical analyses
We used Generalized Linear Models (GLM), or, when repeated measurements
were collected on the pairs, Generalized Linear Mixed Models (GLMM) with a
pair identifier (i.e. cage number) on the first level. Because video
observations were done on the individual birds of the pairs inside the
respirometer box, models including observational data used average individual
MRs (i.e. two birds of a pair obtained same MR value). On the subset of
respirometer measurements we collected 74 observational data points for 24
individuals. Models excluding observational data used one MR and body mass
data point per pair (i.e. 106 cases; 12 pairs x 3 treatments x 3
temperatures, minus 2 data points due to technical failure respirometer).
Statistically significant variables (including two-way interactions) were
selected using stepwise backward deletion of non-significant variables.
Chaff/seed ratio was entered as a covariate, with values 0, 1 or 3. To test
for nonlinearity we entered chaff/seed-squared and temperature-squared in the
models, but these never yielded significant results. All tests were
two-tailed, except for the tests of treatment effect in experiment 2 on
feather growth and laying interval (P-values denoted by
P1), because previous food manipulations had all yielded
either no effect, or reduced feather growth (e.g.
Grubb, Jr et al., 1991;
White et al., 1991
;
Nilsson et al., 1993
;
Jenkins et al., 2001
) and/or
increased laying intervals (Lemon,
1991
; Deerenberg and Overkamp,
1999
).
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Results |
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Experiment 2
Feather growth
In accordance with the results of the respirometry measurements
(Fig. 2), food consumption in
the home cages decreased significantly with increasing chaff/seed ratio
(F1,22=19.5, P<0.001; tested using cage as
random effect to accommodate repeated measurements). Quantitatively, the
effect was even stronger than in the respirometry measurements, with seed
consumption (in g bird-1 day-1, mean ±
S.E.M.) decreasing from 4.38±0.10 to
3.97±0.10 to 3.51±0.13 for chaff/seed ratio 0, 1 and 3,
respectively. Thus seed consumption at the maximum chaff/seed ratio was
decreased by 20%, considerably more than the 6.6% reduction observed at room
temperature during the respirometry sessions. This may be due to the fact that
in the holding cages the chaff/seed mixture was renewed every other day, while
the respirometry sessions always started with a fresh mixture. The chaff/seed
ratio increased over time because seeds were consumed; after 48 h the
chaff/seed ratios had increased from 1 to 2.7 and from 3 to 6.8 (excluding
potential effects of the new chaff produced when consuming seeds).
|
Reproduction
Food intake rates during the 3 days after termination of the food
manipulation tended to decrease over the course of those 3 days but, more
importantly, food intake increased with the chaff/seed ratio experienced in
the preceding 6 weeks, indicating that the birds were in a recuperating
condition (Fig. 6).
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Discussion |
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The fact that DEE decreased with decreasing intake rate is surprising,
because on the basis of simple theoretical considerations (see Introduction),
and the results we obtained with starlings (see companion paper,
Wiersma et al., 2005), an
increase in DEE would be an intuitively more plausible pattern. Moreover,
long-term training regimes in mammals generally result in an increase in RMR
(Speakman and Selman, 2003
),
but birds may differ in this respect
(Nudds and Bryant, 2001
). In
starlings, the effect of intake rate on DEE depended on whether a fixed or a
variable foraging reward rate was applied; DEE decreased when intake rate was
fixed but not when it was variable
(Fotheringham, 1998
). However,
it seems unlikely that zebra finches foraging for seeds mixed with chaff
experienced a fixed reward rate. To examine how our results compare to other
studies we searched the literature for papers in which effects of
manipulations of intake rate on activity and energy expenditure were reported,
separating between experiments using variable and fixed reward rates
(Table 1). In all studies
foraging activity increased when foraging reward rate was decreased, except
for one study of two rodent species where there was no significant change.
However, despite the increase in foraging activity observed in most studies,
only in our starling study (in which we used variable reward rates) did a
decrease in reward rate result in an increase in DEE. In a comparable study of
starlings that applied variable reward rates there was no effect of reward
rate on food consumption (Fotheringham,
1998
), probably because the range of reward rates was
substantially smaller. Thus rather than increasing foraging effort to meet
energy requirements, animals usually (10/13 studies) responded by consuming
less energy. This was achieved firstly by reducing non-foraging activity (see
also Wikelski et al., 1999
),
which was observed in all studies where this was quantified. Secondly, mass
decreased in 50% of the studies, which yields a saving on maintenance costs.
One way in which this bears out in the data is that BMR (or RMR) decreased in
all studies where mass decreased. Note, however, that the nocturnal energy
saving observed in the present study could not be attributed to mass changes,
possibly through mild hypothermia which is often observed when birds suffer
food shortage (McKechnie and Lovegrove,
2002
). Furthermore, independent of food access, exercise training
results in lower RMR in zebra finches
(Nudds and Bryant, 2001
).
Overall there does appear to be a difference between studies applying fixed
and variable reward rates. DEE (or food consumption) decreased in all studies
that used fixed reward rates, and some of these effects were quite strong
(e.g. Deerenberg et al., 1998
;
Bautista et al., 1998
), while
DEE decreased in only one out of four studies that applied variable reward
rates. This one exception is the present study, and why zebra finches
responded in this way remains unresolved.
|
Foraging and food consumption under natural conditions is associated with the risk of being depredated or parasitized, suggesting there are benefits associated with low energy expenditure. An important question emerging is therefore why birds do not always save energy, given that the results listed in Table 1 provide abundant evidence that this is a realistic option. We explored the hypothesis that animals save energy at the expense of somatic maintenance, thereby reducing fitness, which would explain why such savings are foregone in benign conditions. The length of replacement feathers decreased with increasing chaff/seed ratio (Fig. 5), in agreement with this hypothesis. This effect might have been caused by differences in growth rate (although we could not detect this), shape of the growth curves or length of the growth period, or a combination. Although this measure of somatic repair confirms our hypothesis, it is not known to what extent feather replacement is representative of all somatic repair processes. It is important therefore that chaff/seed ratio also had an effect on reproduction, in particular the laying interval (Fig. 7). Thus energy saving is an option for surviving periods in which foraging conditions are poor, but it is done at the expense of condition, which may explain why metabolic rates are generally higher than would be necessary for short-term survival alone.
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Acknowledgments |
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References |
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Bautista, L. M., Tinbergen, J., Wiersma, P. and Kacelnik, A. (1998). Optimal foraging and beyond: How starlings cope with changes in food availability. Am. Nat. 152,543 -561.[CrossRef]
Brody, S. (1945). Bioenergetics and Growth. New York: Hafner.
Calder, W. A. (1964). Gaseous metabolism and water relations of the zebra finch, Taeniopygia castanotis. Physiol. Zool. 37,400 -413.
Day, D. E. and Bartness, T. J. (2001). Effects of foraging effort on body fat and food hoarding in Siberian hamsters. J. Exp. Zool. 289,162 -171.[CrossRef][Medline]
Deerenberg, C. and Overkamp, G. J. F. (1999). Hard work impinges on fitness: an experimental study with zebra finches. Anim. Behav. 58,173 -179.[CrossRef][Medline]
Deerenberg, C., Overkamp, G. J. F., Visser, G. H. and Daan, S. (1998). Compensation in resting metabolism for experimentally increased activity. J. Comp. Physiol. B 168,507 -512.
Finch, C. E. (1990). Longevity, Senescence, and the Genome. Chicago: The University of Chicago Press.
Fotheringham, J. R. (1998). Starlings working for food in a closed economy: empirical studies of feeding regulation.PhD thesis , Oxford University, UK.
Grubb, T. C., Jr, Waite, T. A. and Wiseman, A. J. (1991). Ptilochronology: induced feather growth in Northern cardinals varies with age, sex, ambient temperature, and day length. Wilson Bull. 103,435 -445.
Jenkins, K. D., Hawley, D. M., Farabaugh, C. S. and Cristol, D. A. (2001). Ptilochronology reveals differences in condition of captive white-throated sparrows. Condor 103,579 -586.
Kacelnik, A. and Bateson, M. (1996). Risky theories - The effects of variance on foraging decisions. Am. Zool. 36,402 -434.
Lemon, W. C. (1991). Fitness consequences of foraging behaviour in the zebra finch. Nature 352,153 -155.[CrossRef]
Lemon, W. C. (1993). The energetics of lifetime reproductive success in the zebra finch Taeniopygia guttata. Physiol. Zool. 66,946 -963.
Lemon, W. C. and Barth, R. H. J. (1992). The effects of feeding rate on reproductive success in the zebra finch, Taeniopygia guttata. Anim. Behav. 44,851 -857.
Levy, A. (1964). The accuracy of the bubble meter method for gas flow measurements. J. Sci. Instr. 41,449 -453.[CrossRef]
McKechnie, A. E. and Lovegrove, B. G. (2002). Avian facultative hypothermic responses: a review. Condor 104,705 -724.
Nilsson, J.-Å., Källander, H. and Persson, O. (1993). A prudent hoarder: effects of long-term hoarding in the European nuthatch, Sitta europaea. Behav. Ecol. 4,369 -373.
Nudds, R. L. and Bryant, D. M. (2001). Exercise training lowers the resting metabolic rate of zebra finches, Taeniopygia guttata. Funct. Ecol. 15,458 -464.[CrossRef]
Perrigo, G. (1987). Breeding and feeding strategies in deer mice and house mice when females are challenged to work for their food. Anim. Behav. 35,1298 -1316.
Rashotte, M. E. and Henderson, D. (1988). Coping with rising food costs in a closed economy: feeding behaviour and nocturnal hypothermia in pigeons. J. Exp. Anal. Behav. 50,441 -456.[Medline]
Speakman, J. R. and Selman, C. (2003). Physical activity and resting metabolic rate. Proc. Nutr. Soc. 62, 1-14.[Medline]
Spencer, K. A., Buchanan, K. L., Goldsmith, A. R. and Catchpole, C. K. (2003). Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm. Behav. 44,132 -139.[CrossRef][Medline]
Tiebout, H. M., III (1991). Daytime energy management by tropical hummingbirds: responses to foraging constraint. Ecology 72,839 -851.
Verhulst, S., Riedstra, B. and Wiersma, P. (2005). Brood size and immunity costs in zebra finches. J. Avian Biol. 36,22 -30.[CrossRef]
Vézina, F. and Williams, T. D. (2005).
The metabolic cost of egg production is repeatable. J. Exp.
Biol. 208,2533
-2538.
White, D. W., Kennedy, E. D. and Stouffer, P. C. (1991). Feather regrowth in female European starlings rearing broods of different sizes. Auk 108,889 -895.
Wiersma, P., Selman, C., Speakman, J. R. and Verhulst, S. (2004). Birds sacrifice oxidative protection for reproduction. Proc. Biol. Lett. 271,S360 -S363.[CrossRef]
Wiersma, P., Salomons, H. M. and Verhulst, S. (2005). Metabolic adjustments to increasing foraging costs of starlings in a closed economy. J. Exp. Biol. 208,4099 -4108.[CrossRef]
Wikelski, M., Lynn, S., Breuner, C., Wingfield, J. C. and Kenagy, G. J. (1999). Energy metabolism, testosterone and corticosterone in white-crowned sparrows. J. Comp. Physiol. A 185,463 -470.