, Volume 162, Issue 4, pp 893–902 | Cite as

Differential habitat use and antipredator response of juvenile roach (Rutilus rutilus) to olfactory and visual cues from multiple predators

  • Charles W. Martin
  • F. Joel Fodrie
  • Kenneth L. HeckJr.
  • Johanna Mattila
Behavioral ecology - Original Paper


The indirect, behavioral effects of predation and predator–predator interactions can significantly alter the trophic ecology of many communities. In numerous instances, the strength of these effects may be determined by the ability of prey to identify predation risk through predator-specific cues and respond accordingly to avoid capture. We exposed juvenile roach (Rutilus rutilus), a common forage fish in many brackish and freshwater environments, to vision and/or olfactory cues from two predators with different hunting methods: northern pike (Esox lucius, an ambush predator) and European perch (Perca fluviatilis, a roving predator). Our results demonstrated that responses of roach to perceived risk (as evidenced by their selection of structured or open-water habitats) were highly dependent on cue type and predator identity. For instance, roach responded to olfactory cues of pike by entering open-water habitat, but entered structured habitat when presented with a vision cue of this predator. Opposite responses were elicited from roach for both olfactory and visual cues of perch. Interestingly, roach defaulted to selection of structured habitat when presented with vision + olfaction cues of either predator. Moreover, when presented individual cues of both predators together, roach responded by choosing open-water habitat. Upon being presented with vision + olfaction cues of both predators, however, roach strongly favored structured habitat. Differences in habitat selection of roach were likely in response to the alternative foraging strategies of the two predators, and suggest that prey species may not always use structured habitats as protection. This appears particularly true when a threat is perceived, but cannot immediately be located. These results provide insight to the complex and variable nature by which prey respond to various cues and predators, and offer a mechanistic guide for how behaviorally mediated and predator–predator interactions act as structuring processes in aquatic systems.


Antipredator behavior Predator–prey interactions Olfaction Vision Multiple predator effects Non-consumptive effects 



Support for this project was provided through general funds from the University of South Alabama’s Department of Marine Science, as well as Husö Biological Station, Åbo Akademi University. We thank S. Scyphers, M. Scheinin, M. Ajemian, and M. Kenworthy for assistance in collecting fish and running trials, as well as the staff and students at Husö Biological Station for their logistical support throughout our visit. We also thank J. Valentine, M. Ajemian, B. Toscano, and two anonymous reviewers for their constructive criticism and improvements to this manuscript. All experiments were in compliance with the laws of Finland.


  1. Ådjers K, Appelberg M, Eschbaum R, Lappalainen A, Minde A, Repecka R, Thoresson G (2006) Trends in coastal fish stocks of the Baltic Sea. Bor Env Res 11:13–25Google Scholar
  2. Amo L, Lopez P, Martin J (2004) Chemosensory recognition and behavioural responses of wall lizards, Podarcis muralis, to scents of snakes that pose different risks of predation. Copeia 2004:691–696CrossRefGoogle Scholar
  3. Baden S, Boström C (2001) The leaf canopy of seagrass beds: faunal community structure and function in a salinity gradient along the Swedish coast. Ecol Stud 151:214–236Google Scholar
  4. Bonsdorff E, Blomqvist EM (1993) Biotic couplings on shallow water soft bottoms: examples from the northern Baltic Sea. Oceanogr Mar Biol Annu Rev 31:153–176Google Scholar
  5. Brown G (2003) Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish 4:227–234Google Scholar
  6. Brown GE, Chivers DP (2006) Learning about danger: chemical alarm cues and local risk assessment in prey fishes. In: Brown C, Laland KN, Krause J (eds) Fish cognition and behaviour. Blackwell, London, pp 49–69Google Scholar
  7. Brown GE, Cowan J (2000) Foraging trade-offs and predator inspection in an Ostariophysan fish: switching from chemical to visual cues. Behaviour 137:181–196CrossRefGoogle Scholar
  8. Brown GE, Rive AC, Ferrari MCO, Chivers DP (2006) The dynamic nature of anti-predator behaviour: prey fish integrate threat-sensitive anti-predator responses within background levels of predation risk. Behav Ecol Sociobiol 61:9–16CrossRefGoogle Scholar
  9. Brown GE, Harvey MC, Leduc AOHC, Ferrari MCO, Chivers DP (2009) Social context, competitive interactions and the dynamic nature of antipredator responses of juvenile rainbow trout. J Fish Biol 75:552–562CrossRefPubMedGoogle Scholar
  10. Chivers DP, Smith RJF (1998) Chemical alarm signaling in aquatic predator–prey systems: a review and prospectus. Eucoscience 5:338–352Google Scholar
  11. Christensen B, Persson L (1993) Species-specific antipredatory behaviours: effects on prey choice in different habitats. Behav Ecol Sociobiol 32:1–9CrossRefGoogle Scholar
  12. Crowder L, Squires D, Rice J (1997) Non-additive effects of terrestrial and aquatic predators on juvenile estuarine fish. Ecology 78:1796–1804CrossRefGoogle Scholar
  13. Dill LM, Heithaus MR, Walters CJ (2003) Behaviorally mediated indirect interactions in marine communities and their conservation implications. Ecology 84:1151–1157CrossRefGoogle Scholar
  14. Eklöv P, Persson L (1995) Species-specific antipredator capacities and prey refuges: interactions between piscivorous perch (Perca fluviatilis) and juvenile perch and roach (Rutilus rutilus). Behav Ecol Sociobiol 37:169–178CrossRefGoogle Scholar
  15. Engström-Öst J, Mattila J (2008) Foraging, growth and habitat choice in turbid water: an experimental study with fish larvae in the Baltic Sea. Mar Ecol Prog Ser 359:275–281CrossRefGoogle Scholar
  16. Ferrari MCO, Trowell JJ, Brown GE, Chivers DP (2005) The role of learning in the development of threat-sensitive predator avoidance by fathead minnows. Anim Behav 70:777–784CrossRefGoogle Scholar
  17. Finke DL, Denno RF (2002) Intraguild predation diminished in complex-structured vegetation: implications for prey suppression. Ecology 83:643–652CrossRefGoogle Scholar
  18. Fischhoff IR, Sundaresan SR, Cordingley J, Rubenstein DI (2007) Habitat use and movement of plains zebra (Equus burchelli) in response to predation danger from lions. Behav Ecol 18(4):725–729CrossRefGoogle Scholar
  19. Fodrie FJ, Kenworthy MK, Powers SP (2008) Unintended facilitation between marine consumers generates enhanced mortality for their shared prey. Ecology 89(12):3268–3274CrossRefPubMedGoogle Scholar
  20. Grabowski JH (2004) Habitat complexity disrupts predator-prey interactions yet preserves the trophic cascade in oyster-reef communities. Ecology 85:995–1004CrossRefGoogle Scholar
  21. Griffen BD (2006) Detecting emergent effects of multiple predator species. Oecologia 148:702–709CrossRefPubMedGoogle Scholar
  22. Hager MC, Helfman GS (1991) Safety in numbers: shoal size choice by minnows under predatory threat. Behav Ecol Sociobiol 29:271–276CrossRefGoogle Scholar
  23. Heithaus MR, Dill LM, Marshall GJ, Buhleier B (2002) Habitat use and foraging behavior of tiger sharks (Baleocerdo cuvier) in a seagrass ecosystem. Mar Biol 140:237–248CrossRefGoogle Scholar
  24. Heithaus MR, Hamilton IM, Wirsing AJ, Dill LM (2006) Validation of a randomization procedure to assess animal habitat preferences: microhabitat use of tiger sharks in a seagrass ecosystem. J Anim Ecol 75:666–676CrossRefPubMedGoogle Scholar
  25. Hickman CR, Stone MD, Mathis A (2004) Priority use of chemical over visual cues for detection of predators by neotenic graybelly salamanders, Eurycea multiplicata griseogaster. Herpetologica 60:203–210CrossRefGoogle Scholar
  26. Horinouchi MN, Jo Y, Fujita M, Sano M, Suzuki Y (2009) Seagrass habitat complexity does not always decrease foraging efficiencies of piscivorous fishes. Mar Ecol Prog Ser 377:43–49CrossRefGoogle Scholar
  27. James PL, Heck KL (1994) The effects of habitat complexity and light intensity on ambush predation within a simulated seagrass habitat. J Exp Mar Biol Ecol 176:187–200CrossRefGoogle Scholar
  28. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
  29. Kim J, Brown GE, Dolinsek IJ, Brodeur NN, Leduc AOHC, Grant JWA (2009) Additive and interactive effects of chemical and visual information in eliciting antipredator behaviour in juvenile Atlantic salmon, Salmo salar L. J Fish Biol 74:1280–1290CrossRefPubMedGoogle Scholar
  30. Kusch RC, Mirza RS, Chivers DP (2004) Making sense of predator scents: investigating the sophistication of predator assessment abilities of fathead minnows. Behav Ecol Sociobiol 55:551Google Scholar
  31. Lang A (2003) Intraguild interference and biocontrol effects of generalist predators in a winter wheat field. Oecologia 134:144–153CrossRefPubMedGoogle Scholar
  32. Leduc AOHC, Roh E, Breau C, Brown GE (2007) Learned recognition of a novel odour by wild juvenile Atlantic salmon (Salmo salar) under fully natural conditions. Anim Behav 73:471–477CrossRefGoogle Scholar
  33. Lehtiniemi M, Engström-Öst J, Viitasalo M (2005) Turbidity decreases anti-predator behaviour in pike larvae (Esox lucius). Environ Biol Fish 73:1–8CrossRefGoogle Scholar
  34. Lindquist SB, Bachmann MD (1982) The role of visual and olfactory cues in the prey catching behavior of the tiger salamander, Ambystoma tigrinum. Copeia 1982(1):81–90CrossRefGoogle Scholar
  35. Magurran AE, Seghers BH (1994) Predator inspection behaviour covaries with schooling tendency amongst wild guppy, Poecilia reticulata, populations in Trinidad. Behaviour 128:121–134CrossRefGoogle Scholar
  36. Mathis A, Smith RJF (1993) Fathead minnows (Pimephales promelas) learn to recognize pike (Esox lucius) as predators on the basis of chemical stimuli from minnows in the pike’s diet. Anim Behav 46:645–656CrossRefGoogle Scholar
  37. Mathis A, Vincent F (2000) Differential use of visual and chemical cues in predator recognition and threat-sensitive antipredator behaviour by larval central newts, Notophthalmus viridescens. Can J Zool 78:1646–1652CrossRefGoogle Scholar
  38. Mathis A, Chivers DC, Smith RJF (1993) Population differences in responses of fathead minnows (Pimephales promelas) to chemical and visual stimuli from predators. Ethology 93:31–40CrossRefGoogle Scholar
  39. Mattila J (1992) The effect of habitat complexity on predation efficiency of perch (Perca fluviatilis L.) and ruffe (Gymnocephalus cernuus L.). J Exp Mar Biol Ecol 157:55–67CrossRefGoogle Scholar
  40. Mikheev VN, Wanzenböck J, Pasternak AF (2006) Effects of predator-induced visual and olfactory cues on 0+ perch (Perca fluviatilis L.) foraging behavior. Ecol Freshwater Fish 15:111–117CrossRefGoogle Scholar
  41. Montgomery JC, MacDonald JA (1987) Sensory tuning of lateral line receptors in antarctic fish to movement of planktonic prey. Science 235:195–196CrossRefPubMedGoogle Scholar
  42. Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405CrossRefGoogle Scholar
  43. Nelson WG, Bonsdorff E (1990) Fish predation and habitat complexity: are complexity thresholds real? J Exp Mar Biol Ecol 141:183–194CrossRefGoogle Scholar
  44. Pimm SL, Lawton JH (1978) On feeding on more than one trophic level. Nature 275:542–544CrossRefGoogle Scholar
  45. Pressier EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509CrossRefGoogle Scholar
  46. Rilov G, Figueira WF, Lyman SJ, Crowder L (2007) Complex habitats may not always benefit prey: linking visual field, reef fish behavior and distribution. Mar Ecol Prog Ser 329:225–238CrossRefGoogle Scholar
  47. Savino JF, Stein RA (1989) Behavioural interactions between fish predators and their prey: effects of plant density. Anim Behav 37:311–321CrossRefGoogle Scholar
  48. Schmitz OJ, Sokol-Hessner L (2002) Linearity in the aggregate effects of multiple predators in a food web. Ecol Lett 5:168–172CrossRefGoogle Scholar
  49. Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163CrossRefGoogle Scholar
  50. Schultz ST, Kruschel C, Bakran-Petricioli T (2009) Influence of seagrass meadows on predator-prey habitat segregation in an Adriatic lagoon. Mar Ecol Prog Ser 374:85–99CrossRefGoogle Scholar
  51. Shivik JA (1998) Brown tree snake response to visual and olfactory cues. J Wildl Manage 62(1):105–111CrossRefGoogle Scholar
  52. Sih A (1997) To hide or not to hide? Refuge use in a fluctuating environment. Trends Ecol Evol 10:375–376CrossRefGoogle Scholar
  53. Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355CrossRefGoogle Scholar
  54. Smith RJF (1992) Alarm signals in fishes. Rev Fish Biol Fish 2:33–63CrossRefGoogle Scholar
  55. Trussell GC, Ewanchuk PJ, Bertness MD (2002) Field evidence of trait-mediated indirect interactions in a rock intertidal food web. Ecol Lett 5:241–245CrossRefGoogle Scholar
  56. Utne-Palm AC (2002) Visual feeding of fish in a turbide environment: physical and behavioural aspects. Mar Freshwater Behav Physiol 35:111–128CrossRefGoogle Scholar
  57. Valeix M, Loveridge AJ, Chamaillé-Jammes S, Davidson Z, Murindagomo F, Fritz H, MacDonald DW (2009) Behavioral adjustments of African herbivores to predation risk by lions: spatiotemporal variations influence habitat use. Ecology 90:23–30CrossRefPubMedGoogle Scholar
  58. 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 139:117–122CrossRefPubMedGoogle Scholar
  59. Vincent SE, Shine R, Brown GP (2005) Does foraging mode influence sensory modalites for prey detection? A comparison between males and female filesnakes (Acrochordus arafurae Acrochordidae). Anim Behav 70:715–721CrossRefGoogle Scholar
  60. Wahle RA (1992) Body-size dependent anti-predator mechanisms of the American lobster. Oikos 65:52–60CrossRefGoogle Scholar
  61. Warfe DM, Barmuta LA (2004) Habitat structural complexity mediates the foraging success of multiple predator species. Oecologia 141:171–178CrossRefPubMedGoogle Scholar
  62. Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL Jr, Hughes AR, Kendrick GA, Kenworthy WJ, Short FT, Williams SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci 106(30):12377–12381CrossRefPubMedGoogle Scholar
  63. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions. Ecology 84:1083–1100CrossRefGoogle Scholar
  64. Wirsing AJ, Heithaus MR, Dill LM (2007) Living on the edge: dugongs prefer to forage in microhabitats that allow escape from rather than avoidance of predators. Anim Behav 74:93–101CrossRefGoogle Scholar
  65. Ylönen H, Kortet R, Myntti J, Vainikka A (2007) Predator odor recognition and antipredatory response in fish: does the prey know the predator diel rhythm? Acta Oecol 31:1–7CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Charles W. Martin
    • 1
    • 2
  • F. Joel Fodrie
    • 3
  • Kenneth L. HeckJr.
    • 1
    • 2
  • Johanna Mattila
    • 4
  1. 1.Dauphin Island Sea LabDauphin IslandUSA
  2. 2.University of South AlabamaMobileUSA
  3. 3.Department of Marine Sciences, Institute of Marine SciencesUniversity of North Carolina at Chapel HillMorehead CityUSA
  4. 4.Husö Biological StationÅbo Akademi UniversityTurkuFinland

Personalised recommendations