Abstract
Settlement from the plankton ends the major dispersive stage of life for many marine organisms and exposes them to intense predation pressure in juvenile habitats. This predation mortality represents a life-history bottleneck that can determine recruitment success. At the level of individual predator–prey interactions, prey survival depends upon behavior, specifically how behavior affects prey conspicuousness and evasive ability. We conducted an experiment to identify behavioral traits and performance levels that are important determinants of which individuals survive or die soon after settlement. We measured a suite of behavioral traits on late stage, pre-settlement Ward's damsel (Pomacentrus wardi) collected using light traps. These behavioral traits included two measures of routine swimming (indicators of conspicuousness) and eight measures of escape performance to a visual startle stimulus. Fish were then released onto individual patch reefs, where divers measured an additional behavioral trait (boldness). We censused each patch reef until approximately 50% of the fish were missing (~24 h), which we assumed to be a result of predation. We used classification tree analysis to discriminate survivors from fish presumed dead based on poor behavioral performance. The classification tree revealed that individuals displaying the maladaptive combination of low escape response speed, low boldness on the reef, and high routine swimming speed were highly susceptible to predation (92.4% with this combination died within 24 h). This accounted for 55.2% of all fish that died. Several combinations of behavioral traits predicted likely survival over 24 h, but there was greater uncertainty about that prediction than there was for fish that were predicted to die. Thus maladaptive behavioral traits were easier to identify than adaptive traits.
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Almany GR, Webster MS (2006) The predation gauntlet: early post-settlement mortality in reef fishes. Coral Reefs 25:19–22. doi:10.1007/s00338-005-0044-y
Alvarez MC, Fuiman LA (2005) Environmental levels of atrazine and its degradation products impair survival skills and growth of red drum larvae. Aquat Toxicol 74:229–241. doi:10.1016/j.aquatox.2005.05.014
Alzaga V, Vicente J, Villanua D, Acevedo P, Casas F, Gortazar C (2008) Body condition and parasite intensity correlates with escape capacity in Iberian hares (Lepus granatensis). Behav Ecol Sociobiol 62:769–775. doi:10.1007/s00265-007-0502-3
Begon M, Townsend CR, Harper JL (2006) Ecology: from individuals to ecosystems, 4th edn. Blackwell, Malden, MA, USA
Bell MBV, Radford AN, Rose R, Wade HM, Ridley AR (2009) The value of constant surveillance in a risky environment. Proc R Soc Lond B 276:2997–3005. doi:10.1098/rspb.2009.0276
Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368. doi:10.1016/j.tree.2008.04.003
Cushing DH (1975) Marine ecology and fisheries. Cambridge University Press, Cambridge
Dahlberg MD (1979) A review of survival rates of fish eggs and larvae in relation to impact assessment. Mar Fish Rev 1979:1–12 March
Davis MW, Olla BL (1992) Comparison of growth, behavior and lipid concentrations of walleye pollock Theragra chalcogramma larvae fed lipid-enriched, lipid-deficient and field-collected prey. Mar Ecol Prog Ser 90:23–30
Doherty PJ, Sale PF (1985) Predation on juvenile coral reef fishes: an exclusion experiment. Coral Reefs 4:225–234. doi:10.1007/BF00298081
Doherty PJ, Dufour V, Galzin R, Hixon MA, Meekan MG, Planes S (2004) High mortality during settlement is a population bottleneck for a tropical surgeonfish. Ecology 85:2422–2428. doi:10.1890/04-0366
Endler JA (1986) Defense against predators. In: Feder ME, Lauder GV (eds) Predator-prey relationships: perspectives and approaches from the study of lower vertebrates. University of Chicago Press, Chicago, pp 109–134
Fuiman LA (1986) Burst-swimming performance of larval zebra danios and the effects of diel temperature-fluctuations. Trans Am Fish Soc 115:143–148. doi:10.1577/1548-8659
Fuiman LA (1989) Vulnerability of Atlantic herring larvae to predation by yearling herring. Mar Ecol Prog Ser 51:291–299
Fuiman LA (1993) Development of predator evasion in Atlantic herring, Clupea harengus L. Anim Behav 45:1101–1116. doi:10.1006/anbe.1993.1135
Fuiman LA, Cowan JH Jr (2003) Behavior and recruitment success in fish larvae: repeatability and covariation of survival skills. Ecology 84:53–67. doi:10.1890/0012-9658
Fuiman LA, Magurran AE (1994) Development of predator defences in fishes. Rev Fish Biol Fish 4:145–183. doi:10.1007/BF00044127
Fuiman LA, Ottey DR (1993) Temperature effects on spontaneous behavior of larval and juvenile red drum Sciaenops ocellatus, and implications for foraging. Fish Bull US 91:23–35
Fuiman LA, Cowan JH Jr, Smith ME, O’Neal JP (2005) Behavior and recruitment success in fish larvae: variation with growth rate and the batch effect. Can J Fish Aquat Sci 62:1337–1349
Fuiman LA, Rose KA, Cowan JH Jr, Smith EP (2006) Survival skills required for predator evasion by fish larvae and their relationship to laboratory measures of performance. Anim Behav 71:1389–1399. doi:10.1016/j.anbehav.2005.11.013
Gagliano M, McCormick MI (2009) Hormonally mediated maternal effects shape offspring survival potential in stressful environments. Oecologia 160:657–665. doi:10.1007/s00442-009-1335-8
Godin J-G J, Davis SA (1995) Who dares, benefits: predator approach behaviour in the guppy (Poecilia reticulata) deters predator pursuit. Proc R Soc Lond B 259:193–200
Gosselin LA, Qian P (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282. doi:10.3354/meps146265
Houde ED (1987) Fish early life dynamics and recruitment variability. Am Fish Soc Symp 2:17–29
Houde ED (2002) Mortality. In: Fuiman LA, Werner RG (eds) Fishery science: the unique contributions of early life stages. Blackwell, Oxford, pp 64–87
Jones KA, Krebs JR, Whittingham MJ (2009) Heavier birds react faster to predators: Individual differences in the detection of stalking and ambush predators. Behav Ecol Sociobiol 63:1319–1329. doi:10.1007/s00265-009-0778-6
Kaufman L, Ebersole J, Beets J, McIvor CC (1992) A key phase in the recruitment dynamics of coral reef fishes: post-settlement transition. Environ Biol Fish 34:109–118. doi:10.1007/BF00002386
Kullberg C, Fransson T, Jakobsson S (1996) Impaired predator evasion in fat blackcaps (Sylvia atricapilla). Proc R Soc Lond B 263:1671–1675. doi:10.1098/rspb.1996.0244
Lima SL (2002) Putting predators back into behavioral predator-prey interactions. Trends Ecol Evol 17:70–75. doi:10.1016/S0169-5347(01)02393-X
Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. doi:10.1139/z90-092
Lind J, Cresswell W (2005) Determining the fitness consequences of antipredation behavior. Behav Ecol 16:945–956. doi:10.1093/beheco/ari075
Mangel M (1991) Adaptive walks on behavioral landscapes and the evolution of optimal behavior by natural selection. Evol Ecol Res 5:30–39. doi:10.1007/BF02285243
Mayr E (1961) Cause and effect in biology. Science 134:1501–1506
McCormick MI (2009) Behaviourally mediated phenotypic selection in a disturbed coral reef environment. PLoS One 4:e7096. doi:10.1371/journal.pone.0007096
McCormick MI, Hoey AS (2004) Larval growth history determines juvenile growth and survival in a tropical marine fish. Oikos 106:225–242. doi:10.1111/j.0030-1299.2004.13131.x
McCormick MI, Makey LJ (1997) Post-settlement transition in coral reef fishes: overlooked complexity in niche shifts. Mar Ecol Prog Ser 153:247–257. doi:10.3354/meps153247
McCormick MI, Manassa R (2008) Predation risk assessment by olfactory and visual cues in a coral reef fish. Coral Reefs 27:105–113. doi:10.1007/s00338-007-0296-9
McCormick MI, Meekan MG (2007) Social facilitation of selective mortality. Ecology 88:1562–1570. doi:10.1890/06-0830
McGurk MP (1986) Natural mortality of marine pelagic fish eggs and larvae: role of spatial patchiness. Mar Ecol Prog Ser 34:227–242
Meekan MG, Wilson SG, Halford A, Retzel A (2001) A comparison of catches of fishes and invertebrates by two light trap designs, in tropical NW Australia. Mar Biol 139:373–381. doi:10.1007/s002270100577
Meekan MG, von Kuerthy C, McCormick MI, Radford B (2010) Behavioural mediation of the costs and benefits of fast growth in a marine fish. Anim Behav 79:803–809. doi:10.1016/j.anbehav.2009.12.002
Mero C (2009) The consistency and ecological effects of behaviour in juvenile damselfishes. BSc thesis, James Cook University, Townsville, Queensland, Australia
Nakayama S, Masuda R, Takeuchi T, Tanaka M (2003) Effects of highly unsaturated fatty acids on escape ability from moon jellyfish Aurelia aurita in red sea bream Pagrus major larvae. Fish Sci 69:903–909. doi:10.1046/j.1444-2906.2003.00706.x
O’Brien WJ (1979) The predator-prey interaction of planktivorous fish and zooplankton. Am Sci 67:572–581
Réale D, Festa-Blanchet M (2003) Predator-induced natural selection on temperament in bighorn ewes. Anim Behav 65:463–470. doi:10.1006/anbe.2003.2100
Roff DA (1998) The maintenance of phenotypic and genetic variation in threshold traits by frequency-dependent selection. J Evol Biol 11:513–529. doi:10.1046/j.1420-9101.1998.11040513.x
Santiago E (1998) Linkage and the maintenance of variation for quantitative traits by mutation-selection balance: an infinitesimal model. Genet Res 71:161–170
Scott DE, Casey ED, Donovan MF, Lynch TK (2007) Amphibian lipid levels at metamorphosis correlate to post-metamorphic terrestrial survival. Oecologia 153:521–532. doi:10.1007/s00442-007-0755-6
Sperry JH, Weatherhead PJ (2009) Sex differences in behavior associated with sex-biased mortality in an oviparous snake species. Oikos 118:627–633. doi:10.1111/j.1600-0706.2008.17404.x
Stamps JA (2007) Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecol Lett 10:355–363. doi:10.1111/j.1461-0248.2007.01034.x
Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc Lond B 272:2627–2634. doi:10.1098/rspb.2005.3251
Teacher AGF, Garner TWJ, Nichols RA (2009) Population genetic patterns suggest a behavioural change in wild common frogs (Rana temporaria) following disease outbreaks (Ranavirus). Mol Ecol 18:3163–3172. doi:10.1111/j.1365-294X.2009.04263.x
Tinbergen N (1963) On aims and methods in ethology. Z Tierpsychol 20:410–433
Utne-Palm AC (2000) Prey visibility, activity, size and catchability’s (evasiveness) influence on Gobiusculus flavescens prey choice. Sarsia 85:157–165
Vigliola L, Meekan MG (2002) Size at hatching and planktonic growth determines post-settlement survivorship of a coral reef fish. Oecologia 131:89–93. doi:10.1007/s00442-001-0866-4
Ware DM (1973) Risk of epibenthic prey to predation by rainbow trout (Salmo gairdneri). J Fish Res Bd Can 32:2503–2512
Werner EE (1988) Size, scaling, and the evolution of complex life cycles. In: Ebenman B, Persson L (eds) Size-structured populations. Springer, Berlin, pp 61–81
Wilbur HM (1980) Complex life cycles. Ann Rev Ecol Syst 11:67–93. doi:10.1146/annurev.es.11.110180.000435
Zaret TM (1980) The effect of prey motion on planktivore choice. In: Kerfoot WC (ed) Evolution and ecology of zooplankton communities. American Society of Limnology and Oceanography, Special Symposium 3, pp 594–603
Acknowledgments
Thanks to Ann Hogget, Lyle Vail and the staff of the Lizard Island Research Station, Queensland, Australia, for providing facilities and support for this research. We appreciate the assistance of students and researchers who sorted and shared their light trap catches: J. Moore, T. Holmes, J. Scannell, C. Goatley, S. DeJong, and P. Biro. At the University of Texas Marine Science Institute, Judy Mayo, Sid Aaron, and Lisa Havel analyzed video recordings. We thank A. Ojanguren, S. Nakayama, L. Havel, and E. Farrell for comments on the manuscript. This work was financially supported by the (U.S.) National Science Foundation to L.A.F. (grant number OCE-0425241), the Nancy Lee and Perry R. Bass Endowment at the University of Texas Marine Science Institute, and the ARC Centre of Excellence for Coral Reef Studies. Experiments conducted in this study comply with the current laws of Australia where the work was conducted.
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Fuiman, L.A., Meekan, M.G. & McCormick, M.I. Maladaptive behavior reinforces a recruitment bottleneck in newly settled fishes. Oecologia 164, 99–108 (2010). https://doi.org/10.1007/s00442-010-1712-3
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DOI: https://doi.org/10.1007/s00442-010-1712-3