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Oecologia

, Volume 181, Issue 4, pp 947–958 | Cite as

Predator-induced neophobia in juvenile cichlids

  • Denis MeuthenEmail author
  • Sebastian A. Baldauf
  • Theo C. M. Bakker
  • Timo Thünken
Highlighted Student Research

Abstract

Predation is an important but often fluctuating selection factor for prey animals. Accordingly, individuals plastically adopt antipredator strategies in response to current predation risk. Recently, it was proposed that predation risk also plastically induces neophobia (an antipredator response towards novel cues). Previous studies, however, do not allow a differentiation between general neophobia and sensory channel-specific neophobic responses. Therefore, we tested the neophobia hypothesis focusing on adjustment in shoaling behavior in response to a novel cue addressing a different sensory channel than the one from which predation risk was initially perceived. From hatching onwards, juveniles of the cichlid Pelvicachromis taeniatus were exposed to different chemical cues in a split-clutch design: conspecific alarm cues which signal predation risk and heterospecific alarm cues or distilled water as controls. At 2 months of age, their shoaling behavior was examined prior and subsequent to a tactical disturbance cue. We found that fish previously exposed to predation risk formed more compact shoals relative to the control groups in response to the novel disturbance cue. Moreover, the relationship between shoal density and shoal homogeneity was also affected by experienced predation risk. Our findings indicate predator-induced, increased cross-sensory sensitivity towards novel cues making neophobia an effective antipredator mechanism.

Keywords

Pelvicachromis taeniatus Pelvicachromis kribensis Alarm cues Shoaling Predation risk 

Notes

Acknowledgments

We thank the Bakker research group for discussion of the manuscript. Furthermore, we are grateful to Douglas Chivers and two anonymous referees for helpful comments.

Author contribution statement

DM, SAB, TCMB and TT conceived the study; DM, SAB and TT designed the experiments; DM carried out the research; DM and TT analysed the data and wrote the paper. All authors read and improved the manuscript and agreed to the final content.

Compliance with ethical standards

Funding

This research was funded by the Deutsche Forschungsgemeinschaft (DFG: BA 2885/5-1, TH 1615/1-1).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All work reported here was conducted in accordance with § 4, § 8b and § 9(2) of the German animal welfare act (BGB l. I S. 1207, 1313) which constitute all applicable institutional and national guidelines for the care and use of animals.

References

  1. Adler FR, Harvell CD (1990) Inducible defenses, phenotypic variability and biotic environments. Trends Ecol Evol 5:407–410. doi: 10.1016/0169-5347(90)90025-9 CrossRefPubMedGoogle Scholar
  2. Andörfer B (1980) The school behavior of Leucaspius delineatus (Heckel) in relation to ambient space and the presence of a pike (Esox lucius). Oecologia 47:137–140. doi: 10.1007/bf00541789 CrossRefGoogle Scholar
  3. Baldauf SA, Kullmann H, Schroth SH, Thünken T, Bakker TCM (2009) You can’t always get what you want: size assortative mating by mutual mate choice as a resolution of sexual conflict. BMC Evol Biol 9:129. doi: 10.1186/1471-2148-9-129 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barlow GW (2000) The cichlid fishes, 1st edn. Perseus Publishing, CambridgeGoogle Scholar
  5. Barreto RE, Miyai CA, Sanches FHC, Giaquinto PC, Delicio HC, Volpato GL (2013) Blood cues induce antipredator behavior in Nile tilapia conspecifics. PLoS ONE 8:e54642. doi: 10.1371/journal.pone.0054642 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Belyayev N, Zuyev GV (1969) Hydrodynamic hypothesis of school formation in fishes. Probl Ichthyol 9:578–584Google Scholar
  7. Bernays EA, Wcislo WT (1994) Sensory capabilities, information-processing and resource specialization. Q Rev Biol 69:187–204. doi: 10.1086/418539 CrossRefGoogle Scholar
  8. Blaxter JHS (1987) Structure and development of the lateral line. Biol Rev Camb Philos Soc 62:471–514. doi: 10.1111/j.1469-185X.1987.tb01638.x CrossRefGoogle Scholar
  9. Bourdeau PE, Johansson F (2012) Predator-induced morphological defences as by-products of prey behaviour: a review and prospectus. Oikos 121:1175–1190. doi: 10.1111/j.1600-0706.2012.20235.x CrossRefGoogle Scholar
  10. Briffa M (2013) Plastic proteans: reduced predictability in the face of predation risk in hermit crabs. Biol Lett 9:20130592. doi: 10.1098/rsbl.2013.0592 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Brown GE, Foam PE, Cowell HE, Fiore PG, Chivers DP (2004) Production of chemical alarm cues in convict cichlids: the effects of diet, body condition and ontogeny. Ann Zool Fenn 41:487–499Google Scholar
  12. Brown GE, Ferrari MCO, Elvidge CK, Ramnarine I, Chivers DP (2013) Phenotypically plastic neophobia: a response to variable predation risk. Proc R Soc B 280:20122712. doi: 10.1098/rspb.2012.2712 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Brown GE, Chivers DP, Elvidge CK, Jackson CD, Ferrari MCO (2014) Background level of risk determines the intensity of predator neophobia in juvenile convict cichlids. Behav Ecol Sociobiol 68:127–133. doi: 10.1007/s00265-013-1629-z CrossRefGoogle Scholar
  14. Carreau-Green ND, Mirza RS, Martinez ML, Pyle GG (2008) The ontogeny of chemically mediated antipredator responses of fathead minnows Pimephales promelas. J Fish Biol 73:2390–2401. doi: 10.1111/j.1095-8649.2008.02092.x CrossRefGoogle Scholar
  15. Chapman BB, Morrell LJ, Benton TG, Krause J (2008) Early interactions with adults mediate the development of predator defenses in guppies. Behav Ecol 19:87–93. doi: 10.1093/beheco/arm111 CrossRefGoogle Scholar
  16. Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5:338–352Google Scholar
  17. Chivers DP, Brown GE, Ferrari MCO (2012) The evolution of alarm substances and disturbance cues in aquatic animals. In: Brönmark C, Hansson LA (eds) Chemical ecology in aquatic systems. Oxford University Press, OxfordGoogle Scholar
  18. Chivers DP, Dixson DL, White JR, McCormick MI, Ferrari MCO (2013) Degradation of chemical alarm cues and assessment of risk throughout the day. Ecol Evol 3:3925–3934. doi: 10.1002/ece3.760 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Chivers DP, McCormick MI, Mitchell MD, Ramasamy RA, Ferrari MCO (2014) Background level of risk determines how prey categorize predators and non-predators. Proc R Soc B 281:20140355. doi: 10.1098/rspb.2014.0355 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Clark CW, Harvell CD (1992) Inducible defenses and the allocation of resources: a minimal model. Am Nat 139:521–539. doi: 10.1086/285342 CrossRefGoogle Scholar
  21. Clark CW, Mangel M (1986) The evolutionary advantages of group foraging. Theor Popul Biol 30:45–75. doi: 10.1016/0040-5809(86)90024-9 CrossRefGoogle Scholar
  22. Conradt L, Roper TJ (2000) Activity synchrony and social cohesion: a fission-fusion model. Proc R Soc B 267:2213–2218. doi: 10.1098/rspb.2000.1271 CrossRefPubMedPubMedCentralGoogle Scholar
  23. DeWitt TJ, Langerhans RB (2004) Integrated solutions to environmental heterogeneity: theory of multimoment reaction norms. In: DeWitt TJ, Scheiner SM (eds) Phenotypic plasticity—functional and conceptual approaches. Oxford University Press, Oxford, pp 98–111Google Scholar
  24. Dix TL, Hamilton PV (1993) Chemically mediated escape behavior in the marsh periwinkle Littoraria irrorata Say. J Exp Mar Biol Ecol 166:135–149. doi: 10.1016/0022-0981(93)90082-Y CrossRefGoogle Scholar
  25. Dudley CA, Moss RL (1999) Activation of an anatomically distinct subpopulation of accessory olfactory bulb neurons by chemosensory stimulation. Neuroscience 91:1549–1556. doi: 10.1016/S0306-4522(98)00711-8 CrossRefPubMedGoogle Scholar
  26. Eggers DM (1976) Theoretical effect of schooling by planktivorous fish predators on rate of prey consumption. J Fish Res Board Can 33:1964–1971. doi: 10.1139/f76-250 CrossRefGoogle Scholar
  27. Ferrari MCO (2014) Short-term environmental variation in predation risk leads to differential performance in predation-related cognitive function. Anim Behav 95:9–14. doi: 10.1016/j.anbehav.2014.06.001 CrossRefGoogle Scholar
  28. Ferrari MCO, Crane AL, Brown GE, Chivers DP (2015a) Getting ready for invasions: can background level of risk predict the ability of naive prey to survive novel predators? Sci Rep 5:8309. doi: 10.1038/srep08309 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ferrari MCO, McCormick MI, Allan BJM, Choi RB, Ramasamy RA, Chivers DP (2015b) The effects of background risk on behavioural lateralization in a coral reef fish. Funct Ecol. doi: 10.1111/1365-2435.12483 Google Scholar
  30. Ferrari MCO, McCormick MI, Meekan MG, Chivers DP (2015c) Background level of risk and the survival of predator-naive prey: can neophobia compensate for predator naivety in juvenile coral reef fishes? Proc R Soc B 282:20142197. doi: 10.1098/rspb.2014.2197 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Foam PE, Mirza RS, Chivers DP, Brown GE (2005) Juvenile convict cichlids (Archocentrus nigrofasciatus) allocate foraging and antipredator behaviour in response to temporal variation in predation risk. Behaviour 142:129–144. doi: 10.1163/1568539053627631 CrossRefGoogle Scholar
  32. Foster WA, Treherne JE (1981) Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 293:466–467. doi: 10.1038/293466a0 CrossRefGoogle Scholar
  33. Fuiman LA, Magurran AE (1994) Development of predator defences in fishes. Rev Fish Biol Fish 4:145–183. doi: 10.1007/bf00044127 CrossRefGoogle Scholar
  34. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407. doi: 10.1111/j.1365-2435.2007.01283.x CrossRefGoogle Scholar
  35. Godin J-GJ, Classon LJ, Abrahams MV (1988) Group vigilance and shoal size in a small characin fish. Behaviour 104:29–40. doi: 10.1163/156853988x00584 CrossRefGoogle Scholar
  36. Heczko EJ, Seghers BH (1981) Effects of alarm substance on schooling in the common shiner (Notropis cornutus, Cyprinidae). Environ Biol Fish 6:25–29. doi: 10.1007/bf00001796 CrossRefGoogle Scholar
  37. Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58. doi: 10.1007/bf00300117 CrossRefGoogle Scholar
  38. Helfman GS, Winkelman DL (1997) Threat sensitivity in bicolor damselfish: effects of sociality and body size. Ethology 103:369–383. doi: 10.1111/j.1439-0310.1997.tb00153.x CrossRefGoogle Scholar
  39. Hesse S, Thünken T (2014) Growth and social behavior in a cichlid fish are affected by social rearing environment and kinship. Naturwissenschaften 101:273–283. doi: 10.1007/s00114-014-1154-6 CrossRefPubMedGoogle Scholar
  40. Hesse S, Bakker TCM, Baldauf SA, Thünken T (2012) Kin recognition by phenotype matching is family-rather than self-referential in juvenile cichlid fish. Anim Behav 84:451–457. doi: 10.1016/j.anbehav.2012.05.021 CrossRefGoogle Scholar
  41. Hesse S, Anaya-Rojas JM, Frommen JG, Thünken T (2015a) Social deprivation affects cooperative predator inspection in a cichlid fish. R Soc Open Sci 2:140451. doi: 10.1098/rsos.140451 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hesse S, Anaya-Rojas JM, Frommen JG, Thünken T (2015b) Kinship reinforces cooperative predator inspection in a cichlid fish. J Evol Biol 28:2088–2096. doi: 10.1111/jeb.12736 CrossRefPubMedGoogle Scholar
  43. Houston AI, McNamara JM, Hutchinson JMC (1993) General results concerning the trade-off between gaining energy and avoiding predation. Philos Trans R Soc B 341:375–397. doi: 10.1098/rstb.1993.0123 CrossRefGoogle Scholar
  44. Hoverman JT, Auld JR, Relyea RA (2005) Putting prey back together again: integrating predator-induced behavior, morphology, and life history. Oecologia 144:481–491. doi: 10.1007/s00442-005-0082-8 CrossRefPubMedGoogle Scholar
  45. Kalmijn AJ (1989) Functional evolution of lateral line and inner ear sensory systems. In: Coombs S, Görner P, Münz H (eds) The mechanosensory lateral line. Springer, New York, pp 187–215CrossRefGoogle Scholar
  46. Kelley JL, Phillips B, Cummins GH, Shand J (2012) Changes in the visual environment affect colour signal brightness and shoaling behaviour in a freshwater fish. Anim Behav 83:783–791. doi: 10.1016/j.anbehav.2011.12.028 CrossRefGoogle Scholar
  47. Krakauer DC (1995) Groups confuse predators by exploiting perceptual bottlenecks: a connectionist model of the confusion effect. Behav Ecol Sociobiol 36:421–429. doi: 10.1007/bf00177338 CrossRefGoogle Scholar
  48. Krause J, Ruxton GD (2002) Living in groups, 1st edn. Oxford University Press, OxfordGoogle Scholar
  49. Kröger RHH, Bowmaker JK, Wagner HJ (1999) Morphological changes in the retina of Aequidens pulcher (Cichlidae) after rearing in monochromatic light. Vis Res 39:2441–2448. doi: 10.1016/S0042-6989(98)00256-9 CrossRefPubMedGoogle Scholar
  50. Lamboj A (2004) Die Cichliden des westlichen Afrikas, 1st edn. Birgit Schmettkamp, BornheimGoogle Scholar
  51. Lamboj A (2014) Revision of the Pelvicachromis taeniatus-group (Perciformes), with revalidation of the taxon Pelvicachromis kribensis (Boulenger, 1911) and description of a new species. Cybium 38:205–222Google Scholar
  52. Landeau L, Terborgh J (1986) Oddity and the confusion effect in predation. Anim Behav 34:1372–1380. doi: 10.1016/S0003-3472(86)80208-1 CrossRefGoogle Scholar
  53. Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv Stud Behav 27:215–290. doi: 10.1016/S0065-3454(08)60366-6 CrossRefGoogle Scholar
  54. Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659. doi: 10.1086/303202 CrossRefGoogle Scholar
  55. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. doi: 10.1139/z90-092 CrossRefGoogle Scholar
  56. Lindström K, Ranta E (1993) Social preferences by male guppies, Poecilia reticulata, based on shoal size and sex. Anim Behav 46:1029–1031. doi: 10.1006/anbe.1993.1289 CrossRefGoogle Scholar
  57. Magurran AE (1990) The adaptive significance of schooling as an antipredator defense in fish. Ann Zool Fenn 27:51–66Google Scholar
  58. Magurran AE, Oulton WJ, Pitcher TJ (1985) Vigilant behavior and shoal size in minnows. Z Tierpsychol 67:167–178. doi: 10.1111/j.1439-0310.1985.tb01386.x CrossRefGoogle Scholar
  59. Magurran AE, Seghers BH, Carvalho GR, Shaw PW (1992) Behavioral consequences of an artificial introduction of guppies (Poecilia reticulata) in N-Trinidad: evidence for the evolution of antipredator behavior in the wild. Proc R Soc B 248:117–122. doi: 10.1098/rspb.1992.0050 CrossRefGoogle Scholar
  60. Magurran AE, Seghers BH, Shaw PW, Carvalho GR (1995) The behavioral diversity and evolution of guppy, Poecilia reticulata, populations in Trinidad. Adv Stud Behav 24:155–202. doi: 10.1016/S0065-3454(08)60394-0 CrossRefGoogle Scholar
  61. Martel G, Dill LM (1993) Feeding and aggressive behaviors in juvenile coho salmon (Oncorhynchus kisutch) under chemically-mediated risk of predation. Behav Ecol Sociobiol 32:365–370. doi: 10.1007/bf00168819 CrossRefGoogle Scholar
  62. Meuthen D, Baldauf SA, Bakker TCM, Thünken T (2011) Substrate-treated water: a method to enhance fish activity in laboratory experiments. Aquat Biol 13:35–40. doi: 10.3354/ab00348 CrossRefGoogle Scholar
  63. Meuthen D, Baldauf SA, Thünken T (2014) Evolution of alarm cues: a test of the kin selection hypothesis. F1000Research 1:27. doi: 10.12688/f1000research.1-27.v2 Google Scholar
  64. Meuthen D, Baldauf SA, Bakker TCM, Thünken T (2015) Conspecific alarm cues affect interspecific aggression in cichlid fishes. Hydrobiologia. doi: 10.1007/s10750-015-2473-0 Google Scholar
  65. Mikolajewski DJ, Wohlfahrt B, Joop G, Suhling F (2006) Are behavioural traits in prey sensitive to the risk imposed by predatory fish? Freshw Biol 51:76–84. doi: 10.1111/j.1365-2427.2005.01475.x CrossRefGoogle Scholar
  66. Milinski M (1984) Competitive resource sharing: an experimental test of a learning rule for ESSs. Anim Behav 32:233–242. doi: 10.1016/S0003-3472(84)80342-5 CrossRefGoogle Scholar
  67. Milinski M (1986) A review of competitive resource sharing under constraints in sticklebacks. J Fish Biol 29:1–14. doi: 10.1111/j.1095-8649.1986.tb04994.x CrossRefGoogle Scholar
  68. Mirza RS, Scott JJ, Chivers DP (2001) Differential responses of male and female red swordtails to chemical alarm cues. J Fish Biol 59:716–728. doi: 10.1111/j.1095-8649.2001.tb02375.x CrossRefGoogle Scholar
  69. Montgomery J, Coombs S, Halstead M (1995) Biology of the mechanosensory lateral line in fishes. Rev Fish Biol Fish 5:399–416. doi: 10.1007/bf01103813 CrossRefGoogle Scholar
  70. Nordell SE (1998) The response of female guppies, Poecilia reticulata, to chemical stimuli from injured conspecifics. Environ Biol Fish 51:331–338. doi: 10.1023/a:1007464731444 CrossRefGoogle Scholar
  71. Partridge BL, Johansson J, Kalish J (1983) The structure of schools of giant bluefin tuna in cape cod bay. Environ Biol Fish 9:253–262. doi: 10.1007/bf00692374 CrossRefGoogle Scholar
  72. Pitcher TJ, Parrish JK (1993) Functions of shoaling behavior in teleosts. In: Pitcher TJ (ed) Behaviour of teleost fishes. Chapman & Hall, London, pp 363–439CrossRefGoogle Scholar
  73. Pitcher TJ, Magurran AE, Edwards JI (1985) Schooling mackerel and herring choose neighbors of similar size. Mar Biol 86:319–322. doi: 10.1007/bf00397518 CrossRefGoogle Scholar
  74. Pitcher TJ, Magurran AE, Allan JR (1986) Size-segregative behavior in minnow shoals. J Fish Biol 29:83–95. doi: 10.1111/j.1095-8649.1986.tb05001.x CrossRefGoogle Scholar
  75. Pollock MS, Zhao XX, Brown GE, Kusch RC, Pollock RJ, Chivers DP (2005) The response of convict cichlids to chemical alarm cues: an integrated study of behaviour, growth and reproduction. Ann Zool Fenn 42:485–495Google Scholar
  76. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  77. Ranta E, Peuhkuri N, Laurila A (1994) A theoretical exploration of antipredatory and foraging factors promoting phenotype-assorted fish schools. Ecoscience 1:99–106Google Scholar
  78. Rüppell G, Gösswein E (1972) Die Schwärme von Leucaspius delineatus (Cyprinidae, Teleostei) bei Gefahr im Hellen und im Dunkeln. Z Vgl Physiol 76:333–340. doi: 10.1007/BF00303237 CrossRefGoogle Scholar
  79. Schutz F (1956) Vergleichende Untersuchungen über die Schreckreaktion bei Fischen und deren Verbreitung. Z Vgl Physiol 38:84–135. doi: 10.1007/BF00338623 CrossRefGoogle Scholar
  80. Shand J, Davies WL, Thomas N, Balmer L, Cowing JA, Pointer M, Carvalho LS, Tresize AEO, Collin SP, Beaszley LD, Hunt DM (2008) The influence of ontogeny and light environment on the expression of visual pigment opsins in the retina of the black bream, Acanthopagrus butcheri. J Exp Biol 211:1495–1503. doi: 10.1242/Jeb.012047 CrossRefPubMedGoogle Scholar
  81. Sih A (1980) Optimal behavior: can foragers balance two conflicting demands? Science 210:1041–1043. doi: 10.1126/science.210.4473.1041 CrossRefPubMedGoogle Scholar
  82. Sih A (1992) Prey uncertainty and the balancing of antipredator and feeding needs. Am Nat 139:1052–1069. doi: 10.1086/285372 CrossRefGoogle Scholar
  83. Sih A, McCarthy TM (2002) Prey responses to pulses of risk and safety: testing the risk allocation hypothesis. Anim Behav 63:437–443. doi: 10.1006/anbe.2001.1921 CrossRefGoogle Scholar
  84. Sih A, Ziemba R, Harding KC (2000) New insights on how temporal variation in predation risk shapes prey behavior. Trends Ecol Evol 15:3–4. doi: 10.1016/s0169-5347(99)01766-8 CrossRefPubMedGoogle Scholar
  85. Smith ME (2000) Alarm response of Arius felis to chemical stimuli from injured conspecifics. J Chem Ecol 26:1635–1647. doi: 10.1007/bf00028275 CrossRefGoogle Scholar
  86. Theodorakis CW (1989) Size segregation and the effects of oddity on predation risk in minnow schools. Anim Behav 38:496–502. doi: 10.1016/s0003-3472(89)80042-9 CrossRefGoogle Scholar
  87. Thünken T, Meuthen D, Bakker TCM, Baldauf SA (2012) A sex-specific trade-off between mating preferences for genetic compatibility and body size in a cichlid fish with mutual mate choice. Proc R Soc B 279:2959–2964. doi: 10.1098/rspb.2012.0333 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Thünken T, Hesse S, Bakker TCM, Baldauf SA (2015) Benefits of kin shoaling in a cichlid fish: familiar and related juveniles show better growth. Behav Ecol. doi: 10.1093/beheco/arv166 Google Scholar
  89. Valone TJ (1989) Group foraging, public information, and patch estimation. Oikos 56:357–363. doi: 10.2307/3565621 CrossRefGoogle Scholar
  90. Vickery WL, Giraldeau LA, Templeton JJ, Kramer DL, Chapman CA (1991) Producers, scroungers, and group foraging. Am Nat 137:847–863. doi: 10.1086/285197 CrossRefGoogle Scholar
  91. Wagner HJ, Kröger RHH (2000) Effects of long-term spectral deprivation on the morphological organization of the outer retina of the blue acara (Aequidens pulcher). Philos Trans R Soc B 355:1249–1252. doi: 10.1098/rstb.2000.0677 CrossRefGoogle Scholar
  92. Weihs D (1973) Hydromechanics of fish schooling. Nature 241:290–291. doi: 10.1038/241290a0 CrossRefGoogle Scholar
  93. Wisenden BD, Rugg ML, Korpi NL, Fuselier LC (2009) Lab and field estimates of active time of chemical alarm cues of a cyprinid fish and an amphipod crustacean. Behaviour 146:1423–1442. doi: 10.1163/156853909x440998 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Denis Meuthen
    • 1
    Email author
  • Sebastian A. Baldauf
    • 1
  • Theo C. M. Bakker
    • 1
  • Timo Thünken
    • 1
  1. 1.Institute for Evolutionary Biology and EcologyUniversity of BonnBonnGermany

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