Causes and consequences of the trade-off between compensatory growth and swim performance in teleost fish

Lead Research Organisation: University of Glasgow
Department Name: School of Life Sciences

Abstract

For many animal species, bigger is better. Larger body size reduces the risk of being consumed by predators, and can also lead to an increase in the number of offspring that an animal is able to produce. Despite these apparent benefits of increased body size, mounting evidence suggests that most organisms do not grow at the maximum rates that are physiologically possible, and that there may actually be significant costs associated with rapid growth. Compensatory growth (the rapid growth which occurs in many organisms after a period of food deprivation) provides a useful means to study these potential costs, and in fish, individuals that have undergone a period of growth compensation tend to display reduced swimming performance later in life. While such a cost could have an important influence on both survival and reproductive success, the underlying mechanism responsible for this trade-off between compensatory growth and impaired swimming ability is not understood. There is also nothing known about individual variation in the compensatory growth response in fishes, and the extent to which the costs may differ between individuals. Overall, our lack of knowledge makes it impossible to accurately predict the consequences of compensatory growth for the survival and reproductive success of individual fish, and its effects on the dynamics of wild fish populations. Such information would be valuable, especially considering the increased likelihood of fluctuations in food availability due to factors such as climate change. The proposed research will examine muscle fibre structure, biochemistry, metabolism, and swim performance in individual fish to gain insights into the mechanisms responsible for the trade-off between growth rate and swim performance. Additional laboratory studies will be performed to examine the influence of predator presence on individual variation in the growth response, and also to study the consequences of compensatory growth for individual risk-taking behaviour and reproductive success. Finally, theoretical studies utilizing individual-based mathematical models will compliment these laboratory experiments by incorporating empirically-derived estimates of variability to investigate the implications of variation in growth rate for individual fitness. Overall, this interdisciplinary study will allow us to better understand the mechanistic underpinnings of the costs of rapid growth in fish, and also the consequences of this trade-off for behavioural and evolutionary ecology.

Publications

10 25 50
 
Description As outlined in the original project proposal, this NERC Fellowship had three main objectives:
1) To identify mechanisms responsible for the reduction in swim performance following a period of growth compensation. Severe parasitic infections present in the three-spine sticklebacks that were used in the first year of the fellowship lead to very small samples sizes for studies conducted during this time and necessitated a change to minnows as the study species the following season. These latter studies examining changes in the swim performance of growth manipulated minnows revealed several differences in aspects of swim performance not previously examined. These included differences in maximal sustainable swim speed and the speed at which fish display a gait transition from only steady swimming to the inclusion of burst-type swimming. Correspondingly, fish having undergone compensatory growth also showed reductions in aerobic scope, although anaerobic capacity appears to be unaffected by early nutrition and compensatory growth. Samples for histological and biochemical analyses of muscle fibre structure have been collected but are still awaiting analyses due to the compressed timeline stemming from difficulties during year one, and knock-on effects for the final two years of the project.
2) To quantify individual variation in compensatory growth and the extent to which it is costly. After a period of food deprivation, fish displayed wide variability in the degree of growth compensation exhibited - some fish grew very rapidly while other did not differ substantially from control individuals. There was evidence that the degree of growth compensation is dependent on the amount of mass loss during food deprivation, which in turn may be affected by baseline metabolic demand. Interestingly, however, fish that lose the largest amounts of mass during food deprivation actually showed little growth compensation, probably because they exceeded a physiological threshold beyond which their ability to recover is limited. The existence of these nuanced growth responses in relation to starvation tolerance and metabolic demand represent a major advance in our understanding of how fish of various phenotypes may respond to aspects of resource availability and environmental change.
3) To investigate the consequences of the trade-off between compensatory growth and swim performance for individual fitness. This project examined the consequences of compensatory growth on a wide range of behaviours that are not only relevant to the biology of stream dwelling fishes such as minnows but also to other animal taxa. Results from this project demonstrate that early food-deprivation and subsequent compensatory growth has long term effects on behavioural traits such as boldness, activity, and sociality, with animals having undergone compensatory growth generally displaying degrees of these behaviours which might allow them to feed more but that would also increase their risk of being killed by predators. The fellowship also included the first examination of the metabolic response to alarm substance in fishes, with growth compensated fish showing a decoupling of the physiological and behavioural responses to this cue as compared to controls. Growth compensated fish also displayed a preference for cooler temperatures, which likely acts to reduce their maintenance costs to allow an excess of energy for growth.
Exploitation Route The main beneficiaries of this project are other scientists working in the fields of physiological and behavioural ecology, and life history theory. Studying the costs of compensatory growth provides vital knowledge in these areas, especially considering that growing anthropogenic influence on the environment could cause increased fluctuations in resource availability and a greater preponderance of compensatory growth among wild fish populations. It should also be noted that the phenomenon of compensatory growth has long been of interest to the aquaculture industry, as it provides a means of manipulating growth trajectories and also homogenizing the sizes of individuals to be stocked in common holding tanks. However, the use of compensatory growth may have the potential to impact the flesh quality of cultured fishes if there are effects on muscle fibre structure. This fellowship included an examination of the effects of compensatory growth on muscle fibre structure, and could therefore provide insight in this area and be of benefit to the rapidly growing field of aquaculture.
Sectors Agriculture, Food and Drink,Environment

 
Description So far the findings of this project have been used to produce scientific publications and form the basis for long term collaborations. As additional publications emerge based on this work, the findings are also likely to be of interest to the aquaculture sector, where fast fish growth is key to production but could have consequences for meat quality.
Sector Agriculture, Food and Drink,Environment
Impact Types Cultural,Societal

 
Description Short-Term Scientific Mission
Amount € 1,500 (EUR)
Organisation European Cooperation in Science and Technology (COST) 
Sector Public
Country Belgium
Start 04/2012 
End 05/2012
 
Description Ecophysiology and Predator-Prey Interactions of Mediterranean Fishes 
Organisation National Research Council
Country Italy 
Sector Public 
PI Contribution Expertise in fish physiology, behavioural observation.
Collaborator Contribution Expertise in fish swimming measurements; access to respirometry equipment, fish, and holding facilities.
Impact Marras, S.*, Killen, S.S.*, Lindstrom, J., McKenzie, D.J, Steffensen, J.F., Domenici, P. In Press. Fish swimming in schools save energy regardless of their spatial position. Behavioural Ecology and Sociobiology. DOI: 10.1007/s00265-014-1834-4. *these authors contributed equally. IF = 3.05. Cooke, S.C., Killen, S.S., Metcalfe, J.D., McKenzie, D.J., Mouillot, D., Jørgensen, C., Peck, M.A. In Press. Conservation physiology across scales: insights from the marine realm. Conservation Physiology. DOI: 10.1093/conphys/cou024. IF = NA, new journal. Killen S.S., Marras, S., McKenzie, D.J. 2014. Fast growers sprint slower: effects of food deprivation and re-feeding on sprint swimming performance in individual juvenile European sea bass. Journal of Experimental Biology. 217: 859-865. DOI: 10.1242/jeb.097899. IF = 3.24 Killen S.S., Marras, S., Metcalfe, N.B., McKenzie, D.J., Domenici, P. 2013. Environmental stressors alter relationships between physiology and behaviour. Trends in Ecology and Evolution. 28:651-658. DOI: 10.1016/j.tree.2013.05.005. IF = 15.39 Marras S., Killen S.S., Domenici, D., Claireaux, G., McKenzie, D.J. 2013. Relationships among traits of aerobic and anaerobic swimming performance in individual European sea bass Dicentrarchus labrax. PLoS ONE 8(9): e72815. doi:10.1371/journal.pone.0072815. IF = 3.73 Killen, S.S., Marras, S., Steffensen, J.F., McKenzie, D.J. 2012. Aerobic capacity influences the spatial position of individuals within fish schools. Proceedings of the Royal Society B. 279: 357-364. Featured as a Research Highlight in Nature. IF = 5.68 Killen, S.S., Marras, S., Ryan, M.R., Domenici, P, McKenzie, D.J. 2012. A relationship between metabolic rate and risk-taking behaviour is revealed during hypoxia in juvenile European sea bass. Functional Ecology. 26: 134-143. IF = 4.86 Killen, S.S., Marras, S., McKenzie, D.J. 2011. Fuel, fasting, fear: routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass. Journal of Animal Ecology. 80: 1024-1033. One of 20 most cited papers in Journal of Animal Ecology in 2011. IF = 4.84 Marras, S., Killen, S.S., Claireaux, G., Domenici, P., McKenzie, D.J. 2011. Behavioural and kinematic components of the fast-start escape response in fish: individual variation and temporal repeatability. Journal of Experimental Biology. 214: 3102-3110. IF = 3.24
Start Year 2007
 
Description Ecophysiology and Predator-Prey Interactions of Mediterranean Fishes 
Organisation University of Technology of Compiègne
Department French National Centre for Scientific Research Lab (CNRS Lab)
Country France 
Sector Academic/University 
PI Contribution Expertise in fish physiology, behavioural observation.
Collaborator Contribution Expertise in fish swimming measurements; access to respirometry equipment, fish, and holding facilities.
Impact Marras, S.*, Killen, S.S.*, Lindstrom, J., McKenzie, D.J, Steffensen, J.F., Domenici, P. In Press. Fish swimming in schools save energy regardless of their spatial position. Behavioural Ecology and Sociobiology. DOI: 10.1007/s00265-014-1834-4. *these authors contributed equally. IF = 3.05. Cooke, S.C., Killen, S.S., Metcalfe, J.D., McKenzie, D.J., Mouillot, D., Jørgensen, C., Peck, M.A. In Press. Conservation physiology across scales: insights from the marine realm. Conservation Physiology. DOI: 10.1093/conphys/cou024. IF = NA, new journal. Killen S.S., Marras, S., McKenzie, D.J. 2014. Fast growers sprint slower: effects of food deprivation and re-feeding on sprint swimming performance in individual juvenile European sea bass. Journal of Experimental Biology. 217: 859-865. DOI: 10.1242/jeb.097899. IF = 3.24 Killen S.S., Marras, S., Metcalfe, N.B., McKenzie, D.J., Domenici, P. 2013. Environmental stressors alter relationships between physiology and behaviour. Trends in Ecology and Evolution. 28:651-658. DOI: 10.1016/j.tree.2013.05.005. IF = 15.39 Marras S., Killen S.S., Domenici, D., Claireaux, G., McKenzie, D.J. 2013. Relationships among traits of aerobic and anaerobic swimming performance in individual European sea bass Dicentrarchus labrax. PLoS ONE 8(9): e72815. doi:10.1371/journal.pone.0072815. IF = 3.73 Killen, S.S., Marras, S., Steffensen, J.F., McKenzie, D.J. 2012. Aerobic capacity influences the spatial position of individuals within fish schools. Proceedings of the Royal Society B. 279: 357-364. Featured as a Research Highlight in Nature. IF = 5.68 Killen, S.S., Marras, S., Ryan, M.R., Domenici, P, McKenzie, D.J. 2012. A relationship between metabolic rate and risk-taking behaviour is revealed during hypoxia in juvenile European sea bass. Functional Ecology. 26: 134-143. IF = 4.86 Killen, S.S., Marras, S., McKenzie, D.J. 2011. Fuel, fasting, fear: routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass. Journal of Animal Ecology. 80: 1024-1033. One of 20 most cited papers in Journal of Animal Ecology in 2011. IF = 4.84 Marras, S., Killen, S.S., Claireaux, G., Domenici, P., McKenzie, D.J. 2011. Behavioural and kinematic components of the fast-start escape response in fish: individual variation and temporal repeatability. Journal of Experimental Biology. 214: 3102-3110. IF = 3.24
Start Year 2007
 
Description Effects of Angling Pressure on Growth Trajectories and Metabolism in Fish 
Organisation Leibniz Association
Department Leibniz Institute of Freshwater Ecology and Inland Fisheries
Country Germany 
Sector Charity/Non Profit 
PI Contribution Expertise in animal physiology; respirometry equipment.
Collaborator Contribution Expertise in fisheries related issues; access to selected lines of fish.
Impact Uusi-Heikkilä, S., Whiteley, A.R., Kuparinen, A., Matsumura, S., Venturelli, P.A., Wolter, C., Slate, J., Primmer, C.R., Meinelt, C., Killen, S.S., Bierbach, D., Polverino, G., Ludwig, A., Arlinghaus, R. In review. The evolutionary legacy of size-selective harvest extends from genes to populations. Evolutionary Applications.
Start Year 2011
 
Description Supervision of School Students During Placements 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach Regional
Primary Audience Schools
Results and Impact I think that this project stimulated a genuine interest in science and biology for the student involved in the project.

I engaged in numerous discussions with school children about my research at the final regional Nuffield conference.
Year(s) Of Engagement Activity 2011
URL http://www.nuffieldfoundation.org/nuffield-research-placements