Skip to main content

Shoaling behaviour enhances risk of predation from multiple predator guilds in a marine fish

Abstract

Predicting the consequences of predator biodiversity loss on prey requires an understanding of multiple predator interactions. Predators are often assumed to have independent and additive effects on shared prey survival; however, multiple predator effects can be non-additive if predators foraging together reduce prey survival (risk enhancement) or increase prey survival through interference (risk reduction). In marine communities, juvenile reef fish experience very high mortality from two predator guilds with very different hunting modes and foraging domains—benthic and pelagic predator guilds. The few previous predator manipulation studies have found or assumed that mortality is independent and additive. We tested whether interacting predator guilds result in non-additive prey mortality and whether the detection of such effects change over time as prey are depleted. To do so, we examined the roles of benthic and pelagic predators on the survival of a juvenile shoaling zooplanktivorous temperate reef fish, Trachinops caudimaculatus, on artificial patch reefs over 2 months in Port Phillip Bay, Australia. We observed risk enhancement in the first 7 days, as shoaling behaviour placed prey between predator foraging domains with no effective refuge. At day 14 we observed additive mortality, and risk enhancement was no longer detectable. By days 28 and 62, pelagic predators were no longer significant sources of mortality and additivity was trivial. We hypothesize that declines in prey density led to reduced shoaling behaviour that brought prey more often into the domain of benthic predators, resulting in limited mortality from pelagic predators. Furthermore, pelagic predators may have spent less time patrolling reefs in response to declines in prey numbers. Our observation of the changing interaction between predators and prey has important implications for assessing the role of predation in regulating populations in complex communities.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Anderson TW (2001) Predator responses, prey refuges, and density-dependent mortality of a marine fish. Ecology 82:245–257

    Article  Google Scholar 

  • Anderson TW, Carr MH, Hixon MA (2007) Patterns and mechanisms of variable settlement and recruitment of a coral reef damselfish, Chromis cyanea. Mar Ecol Prog Ser 350:109–116. doi:10.3354/meps07135

    Article  Google Scholar 

  • Billick I, Case TJ (1994) Higher order interactions in ecological communities: what are they and how can they be detected? Ecology 75:1529

    Article  Google Scholar 

  • Bruno JF, O’Connor MI (2005) Cascading effects of predator diversity and omnivory in a marine food web. Ecol Lett 8:1048

    Article  Google Scholar 

  • Carey MP, Wahl DH (2010) Interactions of multiple predators with different foraging modes in an aquatic food web. Oecologia 162:443

    PubMed  Article  Google Scholar 

  • Carr MH, Hixon MA (1995) Predation effects on early post-settlement survivorship of coral reef fishes. Mar Ecol Prog Ser 124:31–42

    Article  Google Scholar 

  • Chase JM, Abrams PA, Grover JP, Diehl S, Chesson P, Holt RD, Richards SA, Nisbet RM, Case TJ (2002) The interaction between predation and competition: a review and synthesis. Ecol Lett 5:302–315

    Article  Google Scholar 

  • Connell SD (1997) The relationship between large predatory fish and recruitment and mortality of juvenile coral reef-fish on artificial reefs. J Exp Mar Biol Ecol 209:261–278

    Article  Google Scholar 

  • Connell SD (2000) Is there safety-in-numbers for prey? Oikos 88:527–532

    Article  Google Scholar 

  • Department of Primary Industries (2008) Fishery status report 2008. Fisheries Victoria, Melbourne

    Google Scholar 

  • DeWitt TJ, Langerhans RB (2003) Multiple prey traits, multiple predators: keys to understanding complex community dynamics. J Sea Res 49:143–155. doi:10.1016/S1385-1101(02)00220-4

    Article  Google Scholar 

  • Dobson A, Lodge D, Alder J, Cumming GS, Keymer J, McGlade J, Mooney H, Rusak JA, Sala O, Wolters V, Wall D, Winfree R, Xenopoulos MA (2006) Habitat loss, trophic collapse, and the decline of ecosystem services. Ecology 87:1915

    PubMed  Article  Google Scholar 

  • Doherty PJ, Sale PF (1985) Predation on juvenile coral reef fishes: an exclusion experiment. Coral Reefs 4:225–234. doi:10.1007/BF00298081

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Edgar GJ, Shaw C (1995) The production and trophic ecology of shallow-water fish assemblages in southern Australia. II. Diets of fishes and trophic relationships between fishes and benthos at Western Port, Victoria. J Exp Mar Biol Ecol 194:83–106. doi:10.1016/0022-0981(95)00084-4

    Article  Google Scholar 

  • Fumei S (2011) Growing together: group living behaviour and the relationship between density and growth in a shoaling fish. Masters of Science thesis, Melbourne University

    Google Scholar 

  • Godin J, Classon L, Abrahams M (1988) Group vigilance and shoal size in a small characin fish. Behaviour 104:29–40. doi:10.1163/156853988X00584

    Article  Google Scholar 

  • Griffen BD (2006) Detecting emergent effects of multiple predator species. Oecologia 148:702–709. doi:10.1007/s00442-006-0414-3

    PubMed  Article  Google Scholar 

  • Griffen BD, Byers JE (2006a) Intraguild predation reduces redundancy of predator species in multiple predator assemblage. J Anim Ecol 75:959–966. doi:10.1111/j.1365-2656.2006.01115.x

    PubMed  Article  Google Scholar 

  • Griffen BD, Byers JE (2006b) Partitioning mechanisms of predator interference in different habitats. Oecologia 146:608–614. doi:10.1007/s00442-005-0211-4

    PubMed  Article  Google Scholar 

  • Griffen BD, Williamson T (2008) Influence of predator density on nonindependent effects of multiple predator species. Oecologia 155:151–159. doi:10.1007/s00442-007-0889-6

    PubMed  Article  Google Scholar 

  • Grubert MA (1999) Diet and feeding strategy of Octopus maorum in southeast Tasmania. Bull Mar Sci 65:441

    Google Scholar 

  • Gurevitch J, Morrison JA, Hedges LV (2000) The interaction between competition and predation: a meta-analysis of field experiments. Am Nat 155(4):435–453

    PubMed  Article  Google Scholar 

  • Hindell JS (2006) Assessing the trophic link between seagrass habitats and piscivorous fishes. Mar Freshwater Res 57:121. doi:10.1071/MF05082

    Article  Google Scholar 

  • Hixon MA, Carr MH (1997) Synergistic predation, density dependence, and population regulation in marine fish. Science 277:946–949

    Article  CAS  Google Scholar 

  • Holbrook SJ, Schmitt RJ (2002) Competition for shelter space causes density-dependent predation mortality in damselfishes. Ecology 83:2855–2868

    Article  Google Scholar 

  • Hunt TL, Ford JR, Swearer SE (2011) Ecological determinants of recruitment to populations of a temperate reef fish, Trachinops caudimaculatus (Plesiopidae). Mar Freshwater Res 62:502–509. doi:10.1071/MF10262

    Article  Google Scholar 

  • Ioannou CC, Krause J (2008) Searching for prey: the effects of group size and number. Anim Behav 75:1383–1388. doi:10.1016/j.anbehav.2007.09.012

    Article  Google Scholar 

  • Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford

    Google Scholar 

  • Krause J, Ruxton GD, Rubenstein D (1998) Is there always an influence of shoal size on predator hunting success? J Fish Biol 52:494–501. doi:10.1111/j.1095-8649.1998.tb02012.x

    Article  Google Scholar 

  • Krupa JJ, Sih A (1998) Fishing spiders, green sunfish, and a stream-dwelling water strider: male-female conflict and prey responses to single versus multiple predator environments. Oecologia 117:258

    Article  Google Scholar 

  • Liley N, Seghers B (1975) Factors affecting the morphology and behaviour of guppies in Trinidad. Funct Evol Behav 6:92–118

    Google Scholar 

  • Lima SL (1998) Nonlethal effects in the ecology of predator-prey interactions. Bioscience 48:25

    Article  Google Scholar 

  • Losey JE, Denno RF (1998) Positive predator–predator interactions: enhance predation rates and synergistic suppression of aphid populations. Ecology 79:2143–2152. doi:10.1890/0012-9658(1998)079[2143:PPPIEP]2.0.CO;2

    Google Scholar 

  • Madin EMP, Gaines SD, Warner RR (2010) Field evidence for pervasive indirect effects of fishing on prey foraging behavior. Ecology 91:3563

    PubMed  Article  Google Scholar 

  • Magurran AE, Pitcher TJ (1987) Provenance, shoal size and the sociobiology of predator-evasion behaviour in minnow shoals. Proc R Soc Lond B Biol Sci 229:439–465. doi:10.1098/rspb.1987.0004

    Article  Google Scholar 

  • Magurran AE, Oulton WJ, Pitcher T (1985) Vigilant behaviour and shoal size in minnows. J Comp Ethol 64:167–178

    Google Scholar 

  • Maher CR, Lott DF (2000) A review of ecological determinants of territoriality within vertebrate species. Midl Nat 143:1–29. doi:10.1674/0003-0031(2000)143[0001:AROEDO]2.0.CO;2

    Article  Google Scholar 

  • Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757

    Article  Google Scholar 

  • Milinski M (1979) Can an experienced predator overcome the confusion of swarming prey more easily? Anim Behav 27:1122–1126. doi:10.1016/0003-3472(79)90060-5

    Article  Google Scholar 

  • Morgan MJ (1988) The influence of hunger, shoal size and predator presence on foraging in bluntnose minnows. Anim Behav 36:1317–1322. doi:10.1016/S0003-3472(88)80200-8

    Article  Google Scholar 

  • Overholtzer-McLeod KL (2004) Variance in reef spatial structure masks density dependence in coral-reef fish populations on natural versus artificial reefs. Mar Ecol Prog Ser 276:269–280

    Article  Google Scholar 

  • Parsons TR (1992) The removal of marine predators by fisheries and the impact of trophic structure. Mar Pollut Bull 25:51

    Article  Google Scholar 

  • Pitcher TJ, Parrish JK (1993) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) Behaviour of teleost fishes, 2nd edn. Chapman and Hall, London

    Chapter  Google Scholar 

  • Pitcher TJ, Magurran AE, Winfield IJ (1982) Fish in larger shoals find food faster. Behav Ecol Sociobiol 10:149–151. doi:10.1007/BF00300175

    Article  Google Scholar 

  • Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167

    PubMed  Article  CAS  Google Scholar 

  • Samhouri JF, Vance RR, Forrester GE, Steele MA (2009) Musical chairs mortality functions: density-dependent deaths caused by competition for unguarded refuges. Oecologia 160:257–265. doi:10.1007/s00442-009-1307-z

    PubMed  Article  Google Scholar 

  • Sandin SA, Pacala SW (2005a) Demographic theory of coral reef fish populations with stochastic recruitment: comparing sources of population regulation. Am Nat 165:107–119

    PubMed  Article  Google Scholar 

  • Sandin SA, Pacala SW (2005b) Fish aggregation results in inversely density-dependent predation on continuous coral reefs. Ecology 86:1520–1530

    Article  Google Scholar 

  • Schmitt RJ, Holbrook SJ (1999a) Mortality of juvenile damselfish: implications for assessing processes that determine abundance. Ecology 80:35–50

    Article  Google Scholar 

  • Schmitt RJ, Holbrook SJ (1999b) Settlement and recruitment of three damselfish species: larval delivery and competition for shelter space. Oecologia 118:76–86

    PubMed  Article  CAS  Google Scholar 

  • Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88:2415

    PubMed  Article  Google Scholar 

  • Schmitz OJ, Suttle KB (2001) Effects of top predator species on direct and indirect interactions in a food web. Ecology 82:2072–2081

    Article  Google Scholar 

  • Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388

    Article  Google Scholar 

  • Shima JS (1999) Variability in relative importance of determinants of reef fish recruitment. Ecol Lett 2:304–310

    Article  Google Scholar 

  • Sih A, Crowley P, McPeek M, Petranka J, Stroheimer K (1985) Predation, competition, and prey communities: a review of field experiments. Annu Rev Ecol Syst 16:269

    Article  Google Scholar 

  • Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355. doi:10.1016/S0169-5347(98)01437-2

    PubMed  Article  CAS  Google Scholar 

  • Smith CD (2003) Diet of Octopus vulgaris in False Bay, South Africa. Mar Biol 143:1127

    Article  Google Scholar 

  • Sokol-Hessner L, Schmitz OJ (2002) Aggregate effects of multiple predator species on a shared prey. Ecology 83:2367–2372

    Article  Google Scholar 

  • Stachowicz JJ, Bruno JF, Duffy JE (2007) Understanding the effects of marine biodiversity on communities and ecosystems. Annu Rev Ecol Evol Syst 38:739

    Article  Google Scholar 

  • Steele MA (1996) Effects of predators on reef fishes: separating cage artifacts from effects of predation. J Exp Mar Biol Ecol 198:249–267. doi:10.1016/0022-0981(96)00011-1

    Article  Google Scholar 

  • Stewart BD, Jones GP (2001) Associations between the abundance of piscivorous fishes and their prey on coral reefs: implications for prey-fish mortality. Mar Biol 138:383–397

    Article  Google Scholar 

  • Stier AC, Geange SW, Bolker BM (2012) Predator density and competition modify the benefits of group formation in a shoaling reef fish. Oikos:no–no. doi:10.1111/j.1600-0706.2012.20726.x

  • Van Buskirk J (2001) Specific induced responses to different predator species in anuran larvae. J Evol Biol 14:482–489. doi:10.1046/j.1420-9101.2001.00282.x

    Article  Google Scholar 

  • Vance-Chalcraft HD, Soluk DA (2005a) Multiple predator effects result in risk reduction for prey across multiple prey densities. Oecologia 144:472

    PubMed  Article  Google Scholar 

  • Vance-Chalcraft HD, Soluk DA (2005b) Estimating the prevalence and strength of non-independent predator effects. Oecologia 146:452–460. doi:10.1007/s00442-005-0201-6

    PubMed  Article  Google Scholar 

  • Vance-Chalcraft HD, Soluk DA, Ozburn N (2004) Is prey predation risk influenced more by increasing predator density or predator species richness in stream enclosures? Oecologia 139:117

    PubMed  Article  Google Scholar 

  • Vance-Chalcraft HD, Rosenheim JA, Vonesh JR, Osenberg CW, Sih A (2007) The influence of intraguild predation on prey suppression and prey release: a meta-analysis. Ecology 88:2689

    PubMed  Article  Google Scholar 

  • Vonesh JR, Osenberg CW (2003) Multi-predator effects across life-history stages: non-additivity of egg- and larval-stage predation in an African treefrog. Ecol Lett 6:503–508. doi:10.1046/j.1461-0248.2003.00470.x

    Article  Google Scholar 

  • White JW, Samhouri JF, Stier AC, Wormald CL, Hamilton SL, Sandin SA (2010) Synthesizing mechanisms of density dependence in reef fishes: behavior, habitat configuration, and observational scale. Ecology 91:1949–1961

    PubMed  Article  Google Scholar 

  • Wooton JT (1994) Putting the pieces together: testing the independence of interactions among organisms. Ecology 75:1544–1551

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Christian Jung, Dean Chamberlain, Matt Le Feuvre, Madhavi Colton, Mal Lindsay and Jessica Smith for the back-breaking construction of artificial reefs, these again plus Evan Hallein, Simon Pahor, Dan Corrie and Seann Chia for setups and surveys, and John Ahern for boat and technical support. We thank Craig Osenberg for his helpful guidance on determining non-additivity in the system. Operational costs were covered by grants from the Holsworth Wildlife Research Endowment to J. R. F. and the Australia and Pacific Science Foundation to S. E. S. Animal ethics approval was granted under Melbourne University AEC0810932. The authors declare they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John R. Ford.

Additional information

Communicated by Craig Osenberg.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 304 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Ford, J.R., Swearer, S.E. Shoaling behaviour enhances risk of predation from multiple predator guilds in a marine fish. Oecologia 172, 387–397 (2013). https://doi.org/10.1007/s00442-012-2508-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-012-2508-4

Keywords

  • Non-additive mortality
  • Predator–prey theory
  • Shoaling
  • Ecosystem stability
  • Multiple predator effects