compensatory growth response in three-spined stickleback in relation to feed-deprivation protocols

Compensatory growth response in three-spinedstickleback in relation to feed-deprivation protocols

X. ZHU*, L.WU*, Y. CUI*†, Y.YANG* AND R. J.WOOTTON‡‰

*State KeyLaboratory of Freshwater EcologyandBiotechnology, Institute ofHydrobiology, Chinese Academyof Sciences,Wuhan,Hubei Province, P.R. China

and ‡Institute of Biological Sciences, University ofWales, Aberystwyth,SY233DA,Wales, U.K.

(Received 9 January 2002, Accepted 6 November 2002)

Different protocols of food deprivation were used to bring two groups of juvenile three-spinedsticklebacks Gasterosteus aculeatus to the same reduced body mass in comparison with a controlgroup fed daily ad libitum. One group experienced 1 week of deprivation then 2 weeks on main-tenance rations.The second group experienced1weekofad libitum feeding followed by 2 weeks ofdeprivation. The deprived groups were reduced to a mean mass of c. 80% of controls. The com-pensatory growth response shown when ad libitum feeding was resumed was independent of thetrajectory by which the three-spined sticklebacks had reached the reduced body mass. Thecompensatory response was sufficient to return the deprived groups to the mass and length trajec-tories shown by the control group within 4 weeks. There was full compensation for dry mass andtotal lipid, but incomplete compensation for lipid-free dry mass. Hyperphagia and increasedgrowth efficiency were present in the re-feeding phase, but there was a lag of a week before thehyperphagia was established. The consistency of the compensatory response of immature three-spined sticklebacks provides a potential model system for the analysis and prediction of appetiteand growth in teleosts. # 2003 The Fisheries Societyof the British Isles

Key words: compensatory growth; growth efficiency; homeostasis; hyperphagia; three-spined

stickleback.

INTRODUCTION

Compensatory or catch-up growth as a response to satiation re-feeding after aperiod of food deprivation has been reported for species from several teleost familiesincluding Salmonidae (Miglavs & Jobling, 1989; Quinton & Blake, 1990; Nicieza &Metcalfe, 1997), Cyprinidae (Russell & Wootton, 1992; Qian et al., 2000; Xieet al., 2001), Ictaluridae (Kim & Lovell, 1995; Gaylord & Gatlin, 2000; Gaylord &Gatlin, 2001), Gasterosteidae (Zhu et al., 2001) and Pleuronectidae (Paul et al.,1995; Saether & Jobling, 1999). In all these studies, the fishes were deprived offood or fed reduced rations for a fixed period before being supplied with foodad libitum. One study on common carp Cyprinus carpio L. in which growth

‰Author to whom correspondence should be addressed.Tel.: þ44 (0) 1970 622346; fax: þ44 (0) 1970 622350;email: [email protected]†ProfessorY. Cui1962^2000.

Journal of Fish Biology (2003) 62,195^205doi:10.1046/j.0022-1112.2003.00019.x, available online at http://www.blackwell-synergy.com

195# 2003 The Fisheries Society of the British Isles

compensationwas notobserved, used a different deprivation protocol (Schwarz etal.,1985). Their study used lowered rations with altered protein and energy content toreduce the treatment groups to the same body mass before re-feeding at controlrates. It is not clear whether the protocol used by Schwarz et al. (1985) contributed tothe failure to obtain compensatory growth.

Three-spined stickleback Gasterosteus aculeatus L. showed compensatorygrowth following periods of food deprivation of 1 or 2 weeks (Zhu et al., 2001) andin response to cycles of deprivation and re-feeding (Ali & Wootton, 2001; X. Zhu,pers. comm.). The present study compared the compensatory growth response oftwo groups of three-spined sticklebacks when reduced, by different feeding proto-cols, to the same mean body mass relative to control fish fed daily ad libitum.The aimwas to determine the role that previous feeding history had on the capacityof fish to show a compensatory response, and whether that previous historyinfluenced the characteristics of a compensatory response. A second aim wasto examine any compensatory response in relation to the effects of thedeprivation protocols on the body condition and lipid content of the three-spinedsticklebacks.

MATERIALS AND METHODS

Juvenile three-spined sticklebacks were collected from Llyn Frongoch in mid-Wales(52�210N; 3�520 W) in autumn 2000.They were housed communally in a 30 l aquarium heldat14� C andwith a natural photoperiod, and fed a mixture of live whiteworm (enchytraeids)and artificial food.The salt content of the water was raised to 5% seawater as a prophylacticagainst white spot Ichthyophthirius multifiliis Fouquet. In December 2000, fish were trans-ferred individually to tanks (320�220�200mm) held in constant circulating systems inenvironmentally controlled rooms maintained at 14� C and a photoperiod of 10L :14D.Thefish were fed ad libitum on live whiteworm for a week, then starved for 1day. Fish were thenweighed to the nearest mg andmeasured (total length,LT) to the nearest 0�1mmwithverniercallipers.Ten fish were assigned at random to one of three treatments. Control fish were feddaily ad libitum except for the 24 h that preceded the weekly weighings. Group 1 wasdeprived of food for1week, then held on a maintenance ration of 2% of body mass ofwhite-wormper day (Allen & Wootton,1982). Group 2 was fed ad libitum for1week, then deprivedof food until the mean body mass did not differ significantly from the mean for group1.Thisrequired 2 weeks of deprivation. Once the mean body masses of groups 1 and 2 hadconverged, they were then provided with whiteworms ad libitum daily until the end of theexperiment. For all fish, any food uneaten after 24 h was removed and reweighed, so dailyconsumption could be estimated. At weekly intervals, all fishwere deprived of food for 24 hto empty their guts, thenweighed andmeasured.The criteria for terminating the experimentwere that, firstly, on two successive weighings there was no significant difference in meanmass between the control and deprived groups, and secondly, therewas no significant differ-ence between the deprived groups.

At the end of the deprivation period, three fish from each treatment, and at the end of theexperiment, all surviving fishwereweighed,measured and killedwith an over-dose ofanaes-thetic, then freeze-dried, re-weighed and stored at �20� C until total lipid was extracted.Lipid was determined in triplicate using chloroform/methanol extraction (Bligh & Dyer,1959) as modified by Lambert & Dehnel (1974).

Mean specific growth rate, GM (% per day), was calculated for each week as:GM¼100[ln(Mf .Mi

�1)](tf� ti)�1, where Mf and Mi are the fresh fish masses at the end(tf) and beginning (ti; tf� ti¼ 7) of the week, and gross growth efficiency, K (%) as:K¼100(Mf�Mi)C

�1, whereC is the fresh mass ofworms consumed in aweek.Changes in mass, length,GMandmean daily food consumptionwere analysedby repeated

measures ANOVA or ANCOVA, with size as the covariate, where necessary. Mass, length

196 X. ZHU ET AL .

# 2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 62,195^205

and food consumption were log-transformed prior to analysis to stabilize variances, buthave been back-transformed for graphical presentation. Treatments were compared bytwo, pre-planned orthogonal contrasts: control v. the mean of groups 1 and 2, and group 1v. group 2.

RESULTS

GROWTH TRAJECTORY

The mass trajectory (Fig.1) showed that the deprivation schedules resulted in thedeprived groups having significantly lower mean body masses than the controlgroup at the start of the re-feeding period (week 5, F1,16¼5�130, P¼ 0�04). Meanmasses for group1 and group 2 were 77�8% and 79�8%, respectively, of mean massof controls. After 3 weeks of re-feeding, the difference between the control anddeprived groups approached significance (week 8, P¼ 0�06), and at the endof the experiment, there was no difference between control and deprived groups(week 10, P¼ 0�20). The deprived groups had achieved full compensation. Therewas a significant difference in mean mass between the deprived groups in week 4(F1,16¼7�031, P¼ 0�02), showing that the treatments had achieved different sched-ules of mass loss to the same mean mass at the start of re-feeding. There was nosignificant difference, however, in mean mass between the deprived groups forthe re-feeding period (P¼ 0�58) and the trajectories of growth in mass duringthe re-feeding period did not differ significantly between the deprived groups(treatment�week interaction, P¼ 0�89).

0

100

200

300

400

500

600

700

800

900

1 2 3 4 5 6 7 8 9 10 11

Weeks

Mea

n fr

esh

mas

s (m

g)

FIG.1. Effect of deprivation protocols on meanþ 95% CI growth in mass of juvenile three-spined stickle-backs. �, Controls (ad libitium daily) (n¼ 6); &, group 1 (1 week deprivation, 2 weeks maintenanceration) (n¼ 6); ~, group 2 (2 weeks deprivation) (n¼ 7).

GROWTH COMPENSATION IN STICKLEBACK 197


The pattern for LT was similar. The mean length for the deprived fish wassignificantly shorter than that of controls by week 6 (F1,16¼5�559, P¼ 0�03), butthere was no significant difference at the end of the experiment (P¼ 0�4).

MASS ^ LENGTH RELATIONSHIP

At the end of the deprivation period, there was a significant difference in themass^length relationship between the control and deprived groups (F2,15¼18�37,P¼ 0�00009), although the regression coefficient, [3�410�36 (95% CI)] didnot differ between groups. The deprived groups had a lower mean mass at a givenlength than the control group. After 2 weeks of re-feeding, no difference wasdetected (P¼ 0�70). There was also a significant difference between group 1 andgroup 2 at the end of the deprivation period (F1,10¼5�43, P¼ 0�03).When com-pared at a given length, group 2 had a lower mean mass than group1. No differencewas detected after aweekof re-feeding.

DRY MASS AND LIPID

ANCOVAusing LT as the size covariate was used to compare body composition(Table I). For fish sampled at the end of the deprivation period, there was a highlysignificant difference in total dry mass between the control and deprived groups,with the latter having a lower dry mass at a given length. The difference betweengroup 1 and group 2 approached significance. The total lipid content of controlfish was significantly higher than that of the deprived groups, but the deprivedgroups did not differ significantly.The lipid-free dry mass of the control group wassignificantly greater than of the deprived groups. Lipid-free dry mass of group 2was significantly greater than that of group1.

At the end of the experiment, after covariance adjustment to a common length,there were no significant differences in total dry mass or total lipid. Lipid-free drymass was still significantly higher in the controls than in the deprived groups, andwas still significantly higher in group 2 than group1 (Table I).

SPECIFIC GROWTH RATE

In the re-feeding weeks, the mean GM of the deprived groups was significantlyhigher than that of the control group, until the final week (Fig. 2). In the finalweek, mean GM of group 1 was significantly higher than that of group 2(F1,16¼ 4�910, P¼ 0�04), although in the previous weeks of re-feeding, the twodeprived groups did not differ significantly.

MEAN DAILY CONSUMPTION

Although the deprived groups had a lower meanbodymass than the control groupduring the re-feeding period, significantly so in the first 3 weeks of re-feeding,the mean daily consumption of the deprived groups was higher [Fig.3(a)].After covariance adjustment, the mean daily consumption did not differ betweenthe control and treatment groups in the first or last week of re-feeding (week 5,P¼ 0�45; week 9, P¼ 0�52), but in all other weeks, the difference was significant[Fig.3(b)]. There was no difference in mean daily consumption between deprivedgroups in any week of re-feeding.

198 X. ZHU ET AL .


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The lack of a difference in consumption in the first week of re-feeding (week 5)reflects the pattern of daily consumption in that week (Fig. 4). In the deprivedgroups, consumption was high on the first day of re-feeding, but then declined tobelow that of the control group, recovering to control levels by the end of the week.In the second week of re-feeding, apart from a drop on the second day, the con-sumption by deprived groups was consistently above that of the controls (Fig. 4).

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1 2 3 4 5

Weeks of re-feeding

GM

(% p

er d

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FIG. 2. Effect of ad libitum re-feeding on meanþ 95% CI specific growth rate of juvenile three-spinedsticklebacks. �, Controls (ad libitium daily) (n¼ 6); &, group 1 (1 week deprivation, 2 weeks main-tenance ration) (n¼ 6); ~, group 2 (2 weeks deprivation) (n¼ 7).

0

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ily c

onsu

mpt

ion

(mg)

Adj

uste

d m

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daily

con

sum

ptio

n (m

g)(a) (b)

FIG.3. Effect of ad libitum re-feeding on mean daily consumption of juvenile three-spined sticklebacks.(a) Mean 95% CI and (b) mean adjusted by covariance analysis, with mass at beginning of re-feedingweek as covariate. �, Controls (ad libitium daily) (n¼ 6); &, group1 (1week deprivation, 2 weeks main-tenance ration) (n¼ 6);~, group 2 (2weeks deprivation) (n¼ 7).

200 X. ZHU ET AL .


GROSS GROWTH EFFICIENCY

The meanKof the deprived groups was significantly higher than that of the con-trol group in the first 3 weeks of the re-feeding period (Fig. 5). In the last week ofthe re-feeding period, the mean efficiency of group 1was significantly higher thanthat of group 2 (F1,16¼5�036; P¼ 0�04).

0

10

20

30

40

50

60

70

1 2 3 4 5 6 7 8 9 10 11 12 13

Re-feeding days

Mea

n co

nsum

ptio

n (m

g pe

r da

y)

FIG.4. Unadjusted mean daily food consumption of juvenile three-spined sticklebacks over the first 2 weeksof ad libitum re-feeding (all fish without food on day 7 prior to weighing). �, Controls (ad libitiumdaily) (n¼ 6); &, group1 (1weekdeprivation, 2 weeks maintenance ration) (n¼ 6); ~, group 2 (2 weeksdeprivation) (n¼ 7).

0

5

10

15

20

25

30

1 2 3 4 5

Weeks of re-feeding

K(%

)

FIG.5. Effect of ad libitum re-feeding on meanþ 95% CI gross growth efficiency of juvenile three-spinedsticklebacks. �, Controls (ad libitium daily) (n¼ 6); &, group 1 (1 week deprivation, 2 weeks main-tenance ration) (n¼ 6); ~, group 2 (2 weeks deprivation) (n¼ 7).



DISCUSSION

Oneofthe fewstudies notto report compensatorygrowth in fishesused twodepriv-ation protocols by which the experimental common carp were brought to the samereduced mass compared with the control common carp (Schwarz et al., 1985). Thepurpose of the present study was to determine the nature of any compensatoryresponse by juvenile three-spined sticklebacks that had been brought to the samereduced mass by different trajectories of mass loss. One protocol applied starvationfor 1week followed by 2 weeks of feeding at a maintenance ration (group 1) and theother applied starvation for 2 weeks (group 2). On re-feeding with ad libitum rations,both deprived groups showed a homeostatic compensatory response that restoredtheir body mass, total length, dry mass and total lipid to that of the control groupwithin 4 weeks, thus showing full compensation as defined by Jobling (1994). Atthe end of the experiment, lipid-free dry mass had shown only partial com-pensation. The recovery trajectories in body mass of the two groups were virtuallyidentical; the previous nutritional history of the two deprived groups had no detect-able effect on the trajectory of their recovery, except possibly in the last week ofthe experiment.

Some models of compensatory growth in fishes have suggested that the associatedhyperphagia would abate as the body composition of the deprived fishes convergedon that of the controls. Broekhuizen et al. (1994) hypothesised that the hyperphagiarestored the ratio of reserve to structural material. The lipostat model for fishes(Jobling & Johansen, 1999; Johansen et al., 2002) proposes that lipid levels have aregulatory role in food intake. Supporting experimental evidence has been obtainedfrom salmonids displaying compensatory growth (Johansen et al., 2001) or fed highand low fat diets (Johansen et al., 2002). In the present study, the deprived three-spined sticklebacks had restored lipid levels by the end of the experiment, which sug-gests that at least part of the compensatory response reflected a lipostat regulation.The compensatory response, however, did persist after condition, as quantified bythe mass^length relationship, was restored. Fresh and dry mass and length werealso restored. These homeostatic responses suggest that, at least in some species,restoration of the growth trajectory of mass may also play a role (Russell & Wootton,1992). This suggestion is based on a model developed by Hubbell (1971), whichassumes there is an optimum trajectory for growth in mass. Any deviations fromthat trajectory evoke a compensatory change in food consumption to reduce themagnitude of the deviation. Protocols of deprivation that produced fishes with thesame mass but differing in proximate composition, especially lipid levels, wouldprovide further insight into the roles that body composition and deviations fromgrowth trajectories play in the form of the compensatory growth response.

Experiments in which juvenile three-spined sticklebacks were exposed to 1 or2 weeks of starvation have also demonstrated full growth compensation (Zhu et al.,2001), although in this experiment the recovery trajectories did differ dependingon the length of the starvation.

The compensatory growth response reflected the hyperphagia in the deprivedgroups and also a higher gross growth efficiency. In the few studies in which thefood consumption of individual fish has been monitored during a phase of compen-satory growth, hyperphagia has always been recorded, e.g. Salvelinus alpinus (L.)(Miglavs & Jobling, 1989), Phoxinus phoxinus (L.) (Russell & Wootton, 1992),

202 X. ZHU ET AL .


Lepomis macrochirus Rafinesque�Lepomis gibbosus (L.) hybrid (Hayward et al.,1997), Carassius auratus gibelio (L.) (Xie et al., 2001). The role of an increase ingrowth efficiency is less clear. This partly reflects differences in protocols, and theneed to distinguish clearly between food supplied and food consumed. In studiesin which the food consumed by an individual fish could be unambiguously relatedto the growth of that fish, most studies have demonstrated an increased growthefficiency at some stage in the compensatory growth response. In S. alpinus andP. phoxinus, the increase in growth efficiency tended to occur early in the compen-satory phase (Miglavs & Jobling, 1989; Russell & Wootton, 1992). In Lepomishybrids experiencing three periods of 14 days of food deprivation, increased growthefficiency was found in two out of the three re-feeding periods (Hayward et al.,1997). Juvenile three-spined sticklebacks showed higher growth efficiencies after1or2 weeks of deprivation (Zhu et al., 2001). The causal explanation for the observedimprovements in growth efficiency is unclear. It may reflect changes in the basalmetabolic rate during the deprivation period or differences in the composition ofthe body mass synthesized by deprived fishes and controls (Jobling,1994).

Although hyperphagia was a major factor in the compensatory growth, thisresponse did not develop until the secondweekof re-feeding.The pattern seen in thefirst week of re-feeding of a decline and then recovery of daily consumption hadbeen observed previously in three-spined sticklebacks re-feeding after 1 and 2 weeksof food deprivation (Ali et al., 2001). In that study it was suggested that it took timeto re-establish effective digestive processes in the stomach following a period offood deprivation. In the present study, however, the three-spined sticklebacks thathadbeen feddailyonamaintenance ration for2weeksbefore thead libitum re-feedingshowed the same pattern of consumption in the first week as fish deprived of food for2weeks.

The consistency of the compensatory growth response of the three-spinedstickleback (Zhu et al., 2001; present study) provides a potentially valuable modelsystem for causal analyses of the relationship between growth and food consump-tion. The response would allow studies of the physiological control of appetiteand growth in teleost fishes in relation to both short-term (e.g. 1 day) and long-termperiods (e.g. 2 weeks) of food deprivation. The consistency of the response alsosuggests that effective models for predicting growth and consumption can bedeveloped under conditions of fluctuating resource availability.

This research was supported by a Royal Society of London ^ Chinese Academyof Sciences Exchange award and by the Research Fund of the University of Wales,Aberystwyth and by the Research Fund of State Key Laboratory of Freshwater Ecologyand Biotechnology.We thank R. Pownall and G. Owen for help with the fish husbandry.N. Metcalfe and two anonymous referee provided constructive comments on the manuscript.

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compensatory growth response in three-spined stickleback in relation to feed-deprivation protocols

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