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Individual variation in foraging behavior reveals a trade-off between flexibility and performance of a top predator

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Abstract

There is increasing evidence that behavioral flexibility is associated with the ability to adaptively respond to environmental change. Flexibility can be advantageous in some contexts such as exploiting novel resources, but it may come at a cost of accuracy or performance in ecologically relevant tasks, such as foraging. Such trade-offs may, in part, explain why individuals within a species are not equally flexible. Here, we conducted a reversal learning task and predation experiment on a top fish predator, the Northern pike (Esox lucius), to examine individual variation in flexibility and test the hypothesis that an individual’s behavioral flexibility is negatively related with its foraging performance. Pikes were trained to receive a food reward from either a red or blue cup and then the color of the rewarded cup was reversed. We found that pike improved over time in how quickly they oriented to the rewarded cup, but there was a bias toward the color red. Moreover, there was substantial variation among individuals in their ability to overcome this red bias and switch from an unrewarded red cup to the rewarded blue cup, which we interpret as consistent variation among individuals in behavioral flexibility. Furthermore, individual differences in behavioral flexibility were negatively associated with foraging performance on ecologically relevant stickleback prey. Our data indicate that individuals cannot be both behaviorally flexible and efficient predators, suggesting a trade-off between these two traits.

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References

  • ABS/ASAB (2003) Guidelines for the treatment of animals in behavioral research and teaching. Anim Behav 65:249–255

    Article  Google Scholar 

  • Beaudoin CP, Tonn WM, Prepas EE, Wassenaar LI (1999) Individual specialization and trophic adaptability of northern pike (Esox lucius): an isotope and dietary analysis. Oecologia 120:386–396

    Article  Google Scholar 

  • Becker GC (1983) Fishes of Wisconsin. University of Wisconsin Press, Madison, WI

    Google Scholar 

  • Becker WC (1992) Manual of quantitative genetics. Academic Enterprises, Pullman, WA

    Google Scholar 

  • Bélisle C, Cresswell J (1997) The effects of a limited memory capacity on foraging behavior. Theor Popul Biol 52:78–90

    Article  PubMed  Google Scholar 

  • Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783

    Article  PubMed  PubMed Central  Google Scholar 

  • Blumroeder J, Eccard JA, Blaum N (2012) Behavioural flexibility in foraging mode of the spotted sand lizard (Pedioplanis l. lineoocellata) seems to buffer negative impacts of savanna degradation. J Arid Environ 77:149–152

    Article  Google Scholar 

  • Blumstein DT, Daniel JC (2007) Quantifying behavior the JWatcher way. Sinauer, Sunderland, MA

    Google Scholar 

  • Blumstein DT, Daniel JC, Evans CS (2006) JWatcher 1.0. http://www.jwatcher.ucla.edu/

  • Bolhuis JE, Schouten WGP, de Leeuw JA, Schrama JW, Wiegant VA (2004) Individual coping characteristics, rearing conditions and behavioural flexibility in pigs. Behav Brain Res 152:351–360

    Article  PubMed  Google Scholar 

  • Bolnick DI, Ingram T, Stutz WE, Snowberg LK, Lau OL, Paull JS (2010) Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proc R Soc Lond B 277:1789–1797

    Article  Google Scholar 

  • Bolnick DI, Amarasekare P, Araujo MS, Burger R, Levine JM, Novak M, Rudolf VHW, Schreiber SJ, Urban MC, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192

    Article  PubMed  PubMed Central  Google Scholar 

  • Boogert NJ, Reader SM, Laland KN (2006) The relation between social rank, neophobia and individual learning in starlings. Anim Behav 72:1229–1239

    Article  Google Scholar 

  • Boogert NJ, Monceau K, Lefebvre L (2010) A field test of behavioural flexibility in Zenaida doves (Zenaida aurita). Behav Process 85:135–141

    Article  Google Scholar 

  • Bry C (1996) Role of vegetation in the life cycle of pike. Fish Fish 19:45–67

  • Burns JG, Dyer AG (2008) Diversity of speed-accuracy strategies benefits social insects. Curr Biol 18:R953–R954

    Article  PubMed  CAS  Google Scholar 

  • Burns JG, Rodd FH (2008) Hastiness, brain size and predation regime affect the performance of wild guppies in a spatial memory task. Anim Behav 76:911–922

    Article  Google Scholar 

  • Casselman JM (1996) Age, growth and environmental requirements of pike. In: Craig JF (ed) Pike: biology and exploitation. Chapman & Hall, London, pp 69–101

    Chapter  Google Scholar 

  • Chittka L, Dyer AG, Bock F, Dornhaus A (2003) Psychophysics — bees trade off foraging speed for accuracy. Nature 424:388

    Article  PubMed  CAS  Google Scholar 

  • Chittka L, Skorupski P, Raine NE (2009) Speed-accuracy tradeoffs in animal decision making. Trends Ecol Evol 24:400–407

    Article  PubMed  Google Scholar 

  • Coppens CM, de Boer SF, Koolhaas JM (2010) Coping styles and behavioural flexibility: towards underlying mechanisms. Philos Trans R Soc B 365:4021–4028

    Article  Google Scholar 

  • Crossman EJ (1996) Taxonomy and distribution. In: Craig JF (ed) Pike: biology and exploitation. Chapman & Hall, London, pp 1–11

    Chapter  Google Scholar 

  • Dally JM, Clayton NS, Emry NJ (2008) Social influences of foraging by rooks (Corvus frugilegus). Behaviour 145:1101–1124

    Article  Google Scholar 

  • Danisman E, Bshary R, Bergmuller R (2010) Do cleaner fish learn to feed against their preference in a reverse reward contingency task? Anim Cogn 13:41–49

    Article  PubMed  Google Scholar 

  • Day LB, Crews D, Wilczynski W (1999) Spatial and reversal learning in congeneric lizards with different foraging strategies. Anim Behav 57:393–407

    Article  PubMed  Google Scholar 

  • Giesing ER, Suski CD, Warner RE, Bell AM (2011) Female sticklebacks transfer information via eggs: effects of maternal experience with predators on offspring. Proc R Soc Lond B 278:1753–1759

    Article  Google Scholar 

  • Hazlett BA (1995) Behavioral plasticity in crustacea: why not more? J Exp Mar Bio Ecol 193:57–66

  • Healy S (1992) Optimal memory: toward an evolutionary ecology of animal cognition? Trends Ecol Evol 7:399–400

    Article  PubMed  CAS  Google Scholar 

  • Hughes RN, O’Brien N (2001) Shore crabs are able to transfer learned handling skills to novel prey. Anim Behav 61:711–714

  • Hurtado-Gonzales JL, Baldassarre DT, Uy JAC (2010) Interaction between female mating preferences and predation may explain the maintenance of rare males in the pentamorphic fish Poecilia parae. J Evol Biol 23:1293–1301

    Article  PubMed  Google Scholar 

  • JMP®, version 9.0. SAS Institute Inc., Cary, NC, 1989–2007

  • Jokela-Maatta M, Smura T, Aaltonen A, Ala-Laurila P, Donner K (2007) Visual pigments of Baltic Sea fishes of marine and limnic origin. Visual Neurosci 24:389–398

    Article  Google Scholar 

  • Jonasson Z (2005) Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci Biobehav R 28:811–825

    Article  Google Scholar 

  • Jonsson M, Hylander S, Ranaker L, Nilsson PA, Bronmark C (2011) Foraging success of juvenile pike Esox lucius depends on visual conditions and prey pigmentation. J Fish Biol 79:290–297

    Article  PubMed  CAS  Google Scholar 

  • Koolhaas JM, Korte SM, de Boer SF, van der Vegt BJ, van Reenen CG, Hopster H, de Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav R 23:925–935

    Article  CAS  Google Scholar 

  • Laland KN, Reader SM (1999a) Foraging innovation in the guppy. Anim Behav 57:331–340

    Article  PubMed  Google Scholar 

  • Laland KN, Reader SM (1999b) Foraging innovation is inversely related to competitive ability in male but not in female guppies. Behav Ecol 10:270–274

    Article  Google Scholar 

  • Lefebvre L, Whittle P, Lascaris E, Finkelstein A (1997) Feeding innovations and forebrain size in birds. Anim Behav 53:549–560

    Article  Google Scholar 

  • Lessells CM, Boag PT (1986) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Article  Google Scholar 

  • Levin R (1968) Evolution in changing environments. Princeton University Press, Princeton, NJ

    Google Scholar 

  • MacArthur RH, Levin R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385

    Article  Google Scholar 

  • McGhee KE, Pintor LM, Surh EL, Bell AM (2012) Maternal exposure to predation risk decreases offspring antipredator behaviour and survival in threespined stickleback. Funct Ecol 26:932–940

    Article  PubMed  PubMed Central  Google Scholar 

  • McGhee KE, Pintor LM, Bell AM (2013) Reciprocal behavioral plasticity and behavioral types during predator–prey interactions. Am Nat 182:704–717

    Article  PubMed  PubMed Central  Google Scholar 

  • Milinski M, Lühti JH, Eggler R, Parker GA (1997) Cooperation under predation risk: experiments on costs and benefits. Proc R Soc Lond B 264:1239–1247

    Article  Google Scholar 

  • Miller AM, Pawlik JR (2013) Do coral reef fish learn to avoid unpalatable prey using visual cues? Anim Behav 85:339–347

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  • Nyqvist MJ, Gozlan RE, Cucherousset J, Britton JR (2012) Behavioural syndrome in a solitary predator is independent of body size and growth rate. PLoS ONE 7:e31619

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Olsen VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514

  • Overington SE, Griffin AS, Sol D, Lefebvre L (2011) Are innovative species ecological generalists? A test in North American birds. Behav Ecol 22:1286–1293

    Article  Google Scholar 

  • Page RA, Ryan MJ (2005) Flexibility in assessment of prey cues: frog-eating bats and frog calls. Proc R Soc Lond B 272:841–847

    Article  Google Scholar 

  • Patankar R, von Hippel FA, Bell MA (2006) Extinction of a weakly armoured threespine stickleback (Gasterosteus aculeatus) population in Prator Lake, Alaska. Ecol Freshw Fish 15:482–487

    Article  Google Scholar 

  • Pruitt JN, Cote J, Ferrari MCO (2012a) Behavioural trait variants in a habitat-forming species dictate the nature of its interactions with and among heterospecifics. Funct Ecol 26:29–36

    Article  Google Scholar 

  • Pruitt JN, Stachowicz JJ, Sih A (2012b) Behavioral types of predator and prey jointly determine prey survival: potential implications for the maintenance of within-species behavioral variation. Am Nat 179:217–227

    Article  PubMed  Google Scholar 

  • Reader SM, Laland KN (2002) Social intelligence, innovation, and enhanced brain size in primates. Proc Natl Acad Sci U S A 99:4436–4441

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Reader SM, MacDonald K (2003) Environmental variability and primate behavioural flexibility. In: Reader SM, Lanland KN (eds) Animal innovation. Oxford University Press, Oxford, pp 83–116

    Chapter  Google Scholar 

  • Reznick DN, Endler JA (1982) The impact of predation on life history evolution in Trindadian guppies (Poecilia reticulata). Evol 36:160–177

  • Ruiz-Gomez MD, Huntingford FA, Overli O, Thornqvist PO, Hoglund E (2011) Response to environmental change in rainbow trout selected for divergent stress coping styles. Physiol Behav 102:317–322

    Article  CAS  Google Scholar 

  • Sergio F, Blas J, Lopez L, Tanferna A, Diaz-Delgado R, Donazar JA, Hiraldo F (2011) Coping with uncertainty: breeding adjustments to an unpredictable environment in an opportunistic raptor. Oecologia 166:79–90

    Article  PubMed  Google Scholar 

  • Sih A (2013) Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim Behav 85:1077–1088

    Article  Google Scholar 

  • Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    Article  PubMed  Google Scholar 

  • Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 4:367–387

    Article  PubMed Central  Google Scholar 

  • Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289

    Article  PubMed  Google Scholar 

  • Smith C, Barber I, Wootton RJ, Chittka L (2004) A receiver bias in the origin of three-spined stickleback mate choice. Proc R Soc Lond B 271:949–955

    Article  Google Scholar 

  • Sol D, Lefebvre L (2000) Behavioural flexibility predicts invasion success in birds introduced to New Zealand. Oikos 90:599–605

    Article  Google Scholar 

  • Sol D, Timmermans S, Lefebvre L (2002) Behavioural flexibility and invasion success in birds. Anim Behav 63:495–502

    Article  Google Scholar 

  • Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, New Jersey

  • Tanner CJ, Salalt GD, Jackson AL (2011) Feeding and non-feeding aggression can be induced in invasive shore crabs by altering food distribution. Behav Ecol Sociobiol 65:249–256

    Article  Google Scholar 

  • Tebbich S, Stankewitz S, Teschke I (2012) The relationship between foraging, learning abilities and neophobia in two species of Darwin’s finches. Ethology 118:135–146

    Article  Google Scholar 

  • Timmermans S, Lefebvre L, Boire D, Basu P (2000) Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain Behav Evol 56:196–203

    Article  PubMed  CAS  Google Scholar 

  • Venturelli PA, Tonn WM (2006) Diet and growth of northern pike in the absence of prey fishes: initial consequences for persisting in disturbance-prone lakes. Trans Am Fish Soc 135:1512–1522

    Article  Google Scholar 

  • Verbeek MEM, Drent PJ, Wiepkema PR (1994) Consistent individual-differences in early exploratory behavior of male great tits. Anim Behav 48:1113–1121

    Article  Google Scholar 

  • Voyer D, Voyer S, Bryden MP (1995) Magnitude of sex differences in spatial abilities: a meta-analysis and consideration of critical variables. Psychol Bull 117:250–270

    Article  PubMed  CAS  Google Scholar 

  • Wilson DS, Yoshimura J (1994) On the coexistence of specialists and generalists. Am Nat 144:692–707

    Article  Google Scholar 

  • Wright TF, Eberhard JR, Hobson EA, Avery ML, Russello MA (2010) Behavioral flexibility and species invasions: the adaptive flexibility hypothesis. Ethol Ecol Evol 22:393–404

    Article  Google Scholar 

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Acknowledgments

We thank Becky Fuller for collection, analysis, and interpretation of reflection data. We also thank Suzanne Gray for interpretation and discussion of reflection data. We thank the Spirit Lake Fish Hatchery (Iowa) for providing the pike, the Jake Wolf Fish Hatchery (Illinois) for holding the pike, and B. Mommer and M. Schrader for help transporting the pike. We thank E. Suhr for help with fish care. KEM was supported by an NIH/NICHD fellowship (T32 HD007333) and an NSF grant to AMB and KEM (IOS 1121980). LMP was supported by University of Illinois start-up funds to AMB and The Ohio State University's, Ohio Agriculture Research and Development Center.

Ethical Standards

Experiments conducted as part of this paper were conducted in the USA and comply with the current laws in the USA and approved by the Animal Care and Use Committee of University of Illinois (protocol #09204).

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Authors and Affiliations

  1. School of Integrative Biology, University of Illinois, Urbana-Champaign, 505 S. Goodwin Ave., Urbana, IL, 61801, USA

    Lauren M. Pintor, Katie E. McGhee, Daniel P. Roche & Alison M. Bell

  2. School of Environment and Natural Resources, The Ohio State University, 2021 Coffey Road, 210 Kottman Hall, Columbus, OH, 43210, USA

    Lauren M. Pintor

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  1. Lauren M. Pintor
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  2. Katie E. McGhee
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Correspondence to Lauren M. Pintor.

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Communicated by K. Lindström

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Pintor, L.M., McGhee, K.E., Roche, D.P. et al. Individual variation in foraging behavior reveals a trade-off between flexibility and performance of a top predator. Behav Ecol Sociobiol 68, 1711–1722 (2014). https://doi.org/10.1007/s00265-014-1779-7

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