Abstract
Functional responses are per-capita feeding rate models whose parameters often scale with individual body size but the parameters may also be further influenced by behavioural traits consistently differing among individuals, i.e. behavioural types or animal personalities. Behavioural types may intrinsically lead to lower feeding rates when consistently shy, inactive and easily stressed individuals cannot identify or respond to risk-free environments or need less food due to lower metabolic rates linked to behaviour. To test how much variation in functional response parameters is explained by body size and how much by behavioural types, we estimated attack rate and handling time individually for differently sized female least killifish (Heterandria formosa) and repeatedly measured behavioural traits for each individual. We found that individual fish varied substantially in their attack rate and in their handling time. Behavioural traits were stable over time and varied consistently among individuals along two distinct personality axes. The individual variation in functional responses was explained solely by body size, and contrary to our expectations, not additionally by the existing behavioural types in exploration activity and co** style. While behavioural trait-dependent functional responses may offer a route to the understanding of the food web level consequences of behavioural types, our study is so far only the second one on this topic. Importantly, our results indicate in contrast to that previous study that behavioural types do not per se affect individual functional responses assessed in the absence of external biotic stressors.
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References
Abrams PA (2010) Implications of flexible foraging for interspecific interactions: lessons from simple models. Funct Ecol 24:7–17. doi:10.1111/j.1365-2435.2009.01621.x
Ahrens RNM, Walters CJ, Christensen V (2012) Foraging arena theory. Fish Fish 13:41–59. doi:10.1111/j.1467-2979.2011.00432.x
Aljetlawi AA, Sparrevik E, Leonardsson K (2004) Prey–predator size-dependent functional response: derivation and rescaling to the real world. J Anim Ecol 73:239–252. doi:10.1111/j.0021-8790.2004.00800.x
Arditi R, Ginzburg LR (1989) Coupling in predator-prey dynamics: ratio-dependence. J Theor Biol 139:311–326. doi:10.1016/S0022-5193(89)80211-5
Barrios-O’Neill D, Kelly R, Dick JTA, Ricciardi A, MacIsaac HJ, Emmerson MC (2016) On the context-dependent scaling of consumer feeding rates. Ecol Lett 19:668–678. doi:10.1111/ele.12605
Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473. doi:10.1111/j.1420-9101.2004.00817.x
Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834. doi:10.1111/j.1461-0248.2007.01081.x
Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783. doi:10.1016/j.anbehav.2008.12.022
Berlow EL, Neutel A-M, Cohen JE, de Ruiter PC, Ebenman B, Emmerson M, Fox JW, Jansen VAA, Jones JI, Kokkoris GD, Logofet DO, McKane AJ, Montoya JM, Petchey O (2004) Interaction strengths in food webs: issues and opportunities. J Anim Ecol 73:585–598. doi:10.1111/j.0021-8790.2004.00833.x
Biro PA, Post JR (2008) Rapid depletion of genotypes with fast growth and bold personality traits from harvested fish populations. Proc Natl Acad Sci 105:2919–2922. doi:10.1073/pnas.0708159105
Biro PA, Sampson P (2015) Fishing directly selects on growth rate via behaviour: implications of growth-selection that is independent of size. Proc R Soc B Biol Sci 282:20142283. doi:10.1098/rspb.2014.2283
Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25:653–659. doi:10.1016/j.tree.2010.08.003
Blake CA, Gabor CR (2014) Effect of prey personality depends on predator species. Behav Ecol 25:871–877. doi:10.1093/beheco/aru041
Bolker B (2016) emdbook: Ecological models and data in R. R package version 1.3.9
Bolnick DI, Amarasekare P, Araújo MS, Bürger 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. doi:10.1016/j.tree.2011.01.009
Boukal DS (2014) Trait- and size-based descriptions of trophic links in freshwater food webs: current status and perspectives. J Limnol. doi:10.4081/jlimnol.2014.826
Breck JE, Gitter MJ (1983) Effect of fish size on the reactive distance of bluegill (Lepomis macrochirus) sunfish. Can J Fish Aquat Sci 40:162–167. doi:10.1139/f83-026
Brodin T (2009) Behavioral syndrome over the boundaries of life—carryovers from larvae to adult damselfly. Behav Ecol 20:30–37. doi:10.1093/beheco/arn111
Brose U (2010) Body-mass constraints on foraging behaviour determine population and food-web dynamics. Funct Ecol 24:28–34. doi:10.1111/j.1365-2435.2009.01618.x
Brown C, Braithwaite VA (2004) Size matters: a test of boldness in eight populations of the poeciliid Brachyraphis episcopi. Anim Behav 68:1325–1329. doi:10.1016/j.anbehav.2004.04.004
Budaev SV (1997) “Personality” in the guppy (Poecilia reticulata): a correlational study of exploratory behavior and social tendency. J Comp Psychol 111:399–411. doi:10.1037//0735-7036.111.4.399
Budick SA, O’Malley DM (2000) Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. J Exp Biol 203:2565–2579
Burns JG (2008) The validity of three tests of temperament in guppies (Poecilia reticulata). J Comp Psychol 122:344–356. doi:10.1037/0735-7036.122.4.344
Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117:641–653. doi:10.1111/j.0030-1299.2008.16513.x
Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R (2013) Animal personality: what are behavioural ecologists measuring? Biol Rev 88:465–475. doi:10.1111/brv.12007
Conrad JL, Weinersmith KL, Brodin T, Saltz JB, Sih A (2011) Behavioural syndromes in fishes: a review with implications for ecology and fisheries management. J Fish Biol 78:395–435. doi:10.1111/j.1095-8649.2010.02874.x
Core Team R (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Crawley MJ (2007) The R book. Wiley, Chichester
David M, Salignon M, Perrot-Minnot M-J (2014) Sha** the antipredator strategy: flexibility, consistency, and behavioral correlations under varying predation threat. Behav Ecol 25:1148–1156. doi:10.1093/beheco/aru101
Davison A, Hinkley D (1997) Bootstrap methods and their application. Cambridge University Press, Cambridge
Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54. doi:10.1111/1365-2656.12013
Domenici P (2001) The scaling of locomotor performance in predator–prey encounters: from fish to killer whales. Comp Biochem Physiol A: Mol Integr Physiol 131:169–182. doi:10.1016/S1095-6433(01)00465-2
Dubois F, Giraldeau L-A (2014) How the cascading effects of a single behavioral trait can generate personality. Ecol Evol 4:3038–3045. doi:10.1002/ece3.1157
Dyer JRG, Croft DP, Morrell LJ, Krause J (2009) Shoal composition determines foraging success in the guppy. Behav Ecol 20:165–171. doi:10.1093/beheco/arn129
Englund G, Rydberg C, Leonardsson K (2008) Long-term variation of link strength in a simple benthic food web. J Anim Ecol 77:883–890. doi:10.1111/j.1365-2656.2008.01404.x
Higham TE (2007) The integration of locomotion and prey capture in vertebrates: morphology, behavior, and performance. Integr Comp Biol 47:82–95. doi:10.1093/icb/icm021
Holling CS (1959) The components of predation as revealed by a study of small-mammal predation of the European pine sawfly. Can Entomol 91:293–320
Jeschke JM, Kopp M, Tollrian R (2002) Predator functional responses: discriminating between handling and digesting prey. Ecol Monogr 72:95–112. doi:10.2307/3100087
Kalinkat G (2014) Bringing animal personality research into the food web arena. J Anim Ecol 83:1245–1247. doi:10.1111/1365-2656.12284
Kalinkat G, Schneider FD, Digel C, Guill C, Rall BC, Brose U (2013) Body masses, functional responses and predator-prey stability. Ecol Lett 16:1126–1134. doi:10.1111/ele.12147
Killen SS, Marras S, Metcalfe NB, McKenzie DJ, Domenici P (2013) Environmental stressors alter relationships between physiology and behaviour. Trends Ecol Evol 28:651–658. doi:10.1016/j.tree.2013.05.005
Klefoth T, Skov C, Krause J, Arlinghaus R (2011) The role of ecological context and predation risk-stimuli in revealing the true picture about the genetic basis of boldness evolution in fish. Behav Ecol Sociobiol 66:547–559. doi:10.1007/s00265-011-1303-2
Klefoth T, Pieterek T, Arlinghaus R (2013) Impacts of domestication on angling vulnerability of common carp, Cyprinus carpio: the role of learning, foraging behaviour and food preferences. Fish Manag Ecol 20:174–186. doi:10.1111/j.1365-2400.2012.00865.x
Kobler A, Klefoth T, Mehner T, Arlinghaus R (2009) Coexistence of behavioural types in an aquatic top predator: a response to resource limitation? Oecologia 161:837–847. doi:10.1007/s00442-009-1415-9
Kondoh M (2007) Anti-predator defence and the complexity-stability relationship of food webs. Proc R Soc B Biol Sci 274:1617–1624. doi:10.1098/rspb.2007.0335
Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ (1999) Co** styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935. doi:10.1016/S0149-7634(99)00026-3
Krause J, Loader SP, McDermott J, Ruxton GD (1998) Refuge use by fish as a function of body length-related metabolic expenditure and predation risks. Proc R Soc B Biol Sci 265:2373–2379. doi:10.1098/rspb.1998.0586
Laskowski KL, Bell AM (2013) Competition avoidance drives individual differences in response to a changing food resource in sticklebacks. Ecol Lett 16:746–753. doi:10.1111/ele.12105
Magnhagen C, Hellström G, Borcherding J, Heynen M (2012) Boldness in two perch populations: long-term differences and the effect of predation pressure. J Anim Ecol 81:1311–1318. doi:10.1111/j.1365-2656.2012.02007.x
Mikheev VN, Andreev OA (1993) Two-phase exploration of a novel environment in the guppy, Poecilia reticulata. J Fish Biol 42:375–383. doi:10.1111/j.1095-8649.1993.tb00340.x
Mittelbach GG, Ballew NG, Kjelvik MK (2014) Fish behavioral types and their ecological consequences. Can J Fish Aquat Sci 71:927–944. doi:10.1139/cjfas-2013-0558
Morozov A, Pasternak AF, Arashkevich EG (2013) Revisiting the role of individual variability in population persistence and stability. PLoS One. doi:10.1371/journal.pone.0070576
Murray GPD, Stillman RA, Gozlan RE, Britton JR (2013) Experimental predictions of the functional response of a freshwater fish. Ethology 119:751–761. doi:10.1111/eth.12117
Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956. doi:10.1111/j.1469-185X.2010.00141.x
Nakayama S, Fuiman LA (2010) Body size and vigilance mediate asymmetric interference competition for food in fish larvae. Behav Ecol 21:708–713. doi:10.1093/beheco/arq043
Novak M (2010) Estimating interaction strengths in nature: experimental support for an observational approach. Ecology 91:2394–2405. doi:10.1890/09-0275.1
Oaten A, Murdoch WW (1975) Switching, functional response, and stability in predator-prey systems. Am Nat 109:299–318
Oksanen L, Fretwell SD, Arruda J, Niemelä P (1981) Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261. doi:10.1086/283817
Okuyama T (2008) Individual behavioral variation in predator–prey models. Ecol Res 23:665–671. doi:10.1007/s11284-007-0425-5
Okuyama T (2012) Flexible components of functional responses. J Anim Ecol 81:185–189. doi:10.1111/j.1365-2656.2011.01876.x
Persson L, de Roos AM (2013) Symmetry breaking in ecological systems through different energy efficiencies of juveniles and adults. Ecology 94:1487–1498. doi:10.1890/12-1883.1
Persson L, Leonardsson K, de Roos AM, Gyllenberg M, Christensen B (1998) Ontogenetic scaling of foraging rates and the dynamics of a size-structured consumer-resource model. Theor Popul Biol 54:270–293. doi:10.1006/tpbi.1998.1380
Pettorelli N, Hilborn A, Duncan C, Durant SM (2015) Individual variability: the missing component to our understanding of predator-prey interactions. In: Adv Ecol Res. doi:10.1016/bs.aecr.2015.01.001
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2014) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-118
Rall BC, Brose U, Hartvig M, Kalinkat G, Schwarzmüller F, Vucic-Pestic O, Petchey OL (2012) Universal temperature and body-mass scaling of feeding rates. Philos Trans R Soc B Biol Sci 367:2923–2934. doi:10.1098/rstb.2012.0242
Réale D, Reader SM, Sol D, Bergeron P, Careau V, Montiglio P-O (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318. doi:10.1111/j.1469-185X.2007.00010.x
Réale D, Garant D, Humphries M, Bergeron P, Careau V, Montiglio P-O (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos Trans R Soc B Biol Sci 365:4051–4063. doi:10.1098/rstb.2010.0208
Rogers D (1972) Random search and insect population models. J Anim Ecol 41:369. doi:10.2307/3474
Rudolf VHW, Lafferty KD (2011) Stage structure alters how complexity affects stability of ecological networks. Ecol Lett 14:75–79. doi:10.1111/j.1461-0248.2010.01558.x
Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277. doi:10.1086/422893
Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289. doi:10.1111/j.1461-0248.2011.01731.x
Smallegange IM, van der Meer J (2007) Interference from a game theoretical perspective: shore crabs suffer most from equal competitors. Behav Ecol 18:215–221. doi:10.1093/beheco/arl071
Toscano BJ, Griffen BD (2014) Trait-mediated functional responses: predator behavioural type mediates prey consumption. J Anim Ecol 83:1469–1477. doi:10.1111/1365-2656.12236
Toscano BJ, Gownaris NJ, Heerhartz SM, Monaco CJ (2016) Personality, foraging behavior and specialization: integrating behavioral and food web ecology at the individual level. Oecologia. doi: 10.1007/s00442-016-3648-8
Tully T, Cassey P, Ferrière R (2005) Functional response: rigorous estimation and sensitivity to genetic variation in prey. Oikos 111:479–487. doi:10.1111/j.1600-0706.2005.14062.x
Valdovinos FS, Ramos-Jiliberto R, Garay-Narváez L, Urbani P, Dunne JA (2010) Consequences of adaptive behaviour for the structure and dynamics of food webs: adaptive behaviour in food webs. Ecol Lett 13:1546–1559. doi:10.1111/j.1461-0248.2010.01535.x
van Gils JA, van der Geest M, De Meulenaer B, Gillis H, Piersma T, Folmer EO (2015) Moving on with foraging theory: incorporating movement decisions into the functional response of a gregarious shorebird. J Anim Ecol 84:554–564. doi:10.1111/1365-2656.12301
Wahlström E, Persson L, Diehl S, Byström P (2000) Size-dependent foraging efficiency, cannibalism and zooplankton community structure. Oecologia 123:138–148. doi:10.1007/s004420050999
Ward AJW (2012) Social facilitation of exploration in mosquitofish (Gambusia holbrooki). Behav Ecol Sociobiol 66:223–230. doi:10.1007/s00265-011-1270-7
Webb PW (1984) Body form, locomotion and foraging in aquatic vertebrates. Am Zool 24:107–120. doi:10.1093/icb/24.1.107
Wennersten L, Forsman A (2012) Population-level consequences of polymorphism, plasticity and randomized phenotype switching: a review of predictions. Biol Rev 87:756–767. doi:10.1111/j.1469-185X.2012.00231.x
Wilson DS, Coleman K, Clark AB, Biederman L (1993) Shy-bold continuum in pumpkinseed sunfish (Lepomis gibbosus): an ecological study of a psychological trait. J Comp Psychol 107:250
Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461. doi:10.1016/j.tree.2012.05.001
Acknowledgments
We are grateful to the members of the B-Types group at IGB for discussions. Special thanks goes to Kate Laskowski, David Bierbach and Pep Alós for help with repeatability score calculations, video analysis in EthoVision, and multivariate regression analysis, respectively. We also like to thank two anonymous reviewers for their helpful comments.
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AS and GK designed the experiment, AS performed the feeding trials and behavioural assays, GK analysed the videos, AS analysed the data and wrote the manuscript, GK and RA commented on statistical analysis and manuscript.
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AS was supported by an IGB Postdoc Fellowship and a Marie Sklodowska Curie Fellowship (Horizon-2020-IEF, Grant # 660643). GK and RA were supported via the B-Types project through the Leibniz Competition Pact for Innovation and Research (SAW-2013-IGB-2). GK also acknowledges funding from the German Science Foundation DFG (KA-3029/2-1).
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Communicated by Joel Trexler.
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Schröder, A., Kalinkat, G. & Arlinghaus, R. Individual variation in functional response parameters is explained by body size but not by behavioural types in a poeciliid fish. Oecologia 182, 1129–1140 (2016). https://doi.org/10.1007/s00442-016-3701-7
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DOI: https://doi.org/10.1007/s00442-016-3701-7