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Cue recognition and behavioural responses in the three-spined stickleback (Gasterosteus aculeatus) under risk of fish predation

  • A. Landeira-DabarcaEmail author
  • J. Näslund
  • J. I. Johnsson
  • M. Álvarez
Original Article
  • 5 Downloads

Abstract

To effectively respond to predation risk, prey must assess the risk associated with different predation cues. Predation cues can stem either from the predator or from conspecifics and indicate different predation risk levels, thus eliciting different anti-predation responses. The three-spined stickleback is a well-studied fish species often found in gregarious formations. Previous studies show that sticklebacks perform a variety of anti-predation behaviours; however, little is known about how they respond to multiple simultaneous predator cues, characteristic of heterogeneous natural habitats. Here, we experimentally compare the relative importance of three types of predation cues (visual predator cue, chemical predator odour cue and chemical alarm cue from injured conspecifics) and their interactions, on anti-predation and foraging behaviour of sticklebacks. Results showed that (1) individual sticklebacks responded most strongly to visual predator cues, which resulted in reduced foraging activity, increased spine erection and increased predator inspection; (2) the presence of chemical cues (predator odour and/or conspecific alarm cues) stimulates freezing behaviour to a minor extent; and (3) anti-predation behaviour manifests as a trade-off with foraging-related activities. Overall, the results indicate that sticklebacks could assess risk and modify their behavioural responses depending on which cues are present in the environment. The experimental approach of using factorial combinations of different predatory cues can increase our understanding of the role of multimodal cues in aquatic ecosystems.

Keywords

Predator Multimodal cues Anti-predation behaviour Chemical cues Alarm cues Visual cues 

Notes

Acknowledgements

Our co-author J. I. Johnsson sadly passed away during the final process of writing this manuscript, his contributions to the field were major and he will be missed and remembered as a great mentor and collaborator. The work was finalised with support from University of South Bohemia, Faculty of Science, Dept. Ecosystem Biology & SoWa (MEYS; projects LM2015075, EF16_0130001782-SoWa Ecosystems Research) to ALD and JN.

Authors’ contribution

MA and ALD conceived and designed the investigation. ALD, JN and JIJ performed the field and laboratory work. JN analysed the data. JIJ and MA contributed materials, reagents and analysis tools. ALD wrote the manuscript and all other authors widely contributed and provided editorial advice.

Funding information

This study was supported by funding from the Spanish Ministry of Science and Innovation through the National Program for Fundamental Research (ref. CGL 2009-07904) to MA, and the Swedish Research Council Formas to JIJ.

Compliance with ethical standards

The experiment was approved by the Ethical Committee for Animal Research in Gothenburg (Licence 8-2011) and complied with current laws in Sweden and the European Directive 2010/63/EU.

Supplementary material

10211_2019_324_MOESM1_ESM.docx (65 kb)
ESM 1 (DOCX 65 kb)

References

  1. Åbjörnsson K, Wagner BM, Axelsson A, Bjerselius R, Olsén KH (1997) Responses of Acilius sulcatus (Coleoptera: Dytiscidae) to chemical cues from perch (Perca fluviatilis). Oecologia 111:166–171.  https://doi.org/10.1007/s004420050221 CrossRefGoogle Scholar
  2. Ajemian MJ, Sohel S, Mattila J (2015) Effects of turbidity and habitat complexity on antipredator behavior of three-spined sticklebacks (Gasterosteus aculeatus). Environ Biol Fish 98:45–55.  https://doi.org/10.1007/s10641-014-0235-x CrossRefGoogle Scholar
  3. Bartoń K (2017) Package ‘MuMIn’: multi-model inference. https://cran.r-project.org/web/packages/MuMIn/
  4. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783.  https://doi.org/10.1016/j.anbehav.2008.12.022 CrossRefGoogle Scholar
  5. Bouwma P, Hazlett BA (2001) Integration of multiple predator cues by the crayfish Oronectes propinquus. Anim Behav 61:771–776.  https://doi.org/10.1006/anbe.2000.1649 CrossRefGoogle Scholar
  6. Brönmark C, Hansson L-A (2000) Chemical communication in aquatic systems: an introduction. Oikos 88:103–109.  https://doi.org/10.1034/j.1600-0706.2000.880112.x CrossRefGoogle Scholar
  7. Brown GE (2003) Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish 4:227–234.  https://doi.org/10.1046/j.1467-2979.2003.00132.x CrossRefGoogle Scholar
  8. Brown GE, Godin J-GJ (1997) Anti-predator responses to conspecific and heterospecific skin extracts by threespine sticklebacks: alarm pheromones revisited. Behaviour 134:1123–1134.  https://doi.org/10.1163/156853997X00098 CrossRefGoogle Scholar
  9. Brown GE, Chivers DP, Smith RJF (1995) Fathead minnows avoid conspecific and heterospecific alarm pheromone in the faeces of northern pike. J Fish Biol 47:387–393.  https://doi.org/10.1111/j.1095-8649.1995.tb01908.x Google Scholar
  10. Brown GE, Paige JA, Godin J-GJ (2000) Chemically mediated predator inspection behaviour in the absence of predator visual cues by a characin fish. Anim Behav 60:315–332.  https://doi.org/10.1006/anbe.2000.1496 CrossRefGoogle Scholar
  11. Brown GE, Rive AC, Ferrari MC, Chivers DP (2006) The dynamic nature of antipredator behavior: prey fish integrate threat-sensitive antipredator responses within background levels of predation risk. Behav Ecol Sociobiol 61:9–16.  https://doi.org/10.1007/s00265-006-0232-y CrossRefGoogle Scholar
  12. Brown GE, Elvidge CK, Ramnarine I, Chivers DP, Ferrari MC (2014) Personality and the response to predation risk: effects of information quantity and quality. Anim Cogn 17:1063–1069.  https://doi.org/10.1007/s10071-014-0738-z CrossRefGoogle Scholar
  13. Brown GE, Jackson CD, Joyce BJ, Chivers DP, Ferrari MC (2016) Risk-induced neophobia: does sensory modality matter? Anim Cogn 19(6):1143–1150.  https://doi.org/10.1007/s10071-016-1021-2 CrossRefGoogle Scholar
  14. Bryer PJ, Mirza RS, Chivers DP (2001) Chemosensory assessment of predation risk by slimy sculpins (Cottus cognatus): responses to alarm, disturbance, and predator cues. J Chem Ecol 27:533–546.  https://doi.org/10.1023/A:1010332820944 CrossRefGoogle Scholar
  15. Chivers DP, Mirza RS (2001) Predator diet cues and the assessment of predation risk by aquatic vertebrates: a review and prospectus. In: Marchlewska-Koj A, Lepri JJ, Müller-Schwarze D (eds) Chemical signals in vertebrates 9. Springer, Boston, MA, pp 277–284CrossRefGoogle Scholar
  16. Chivers DP, Brown GE, Ferrari MC (2012) The evolution of alarm substances and disturbance cues in aquatic animals. In: Brönmark C, Hansson L-A (eds) Chemical ecology in aquatic systems. Oxford University Press, New York, NY, pp 127–139CrossRefGoogle Scholar
  17. Cowan J, Brown GE (2000) Foraging trade-offs and predator inspection in an ostariophysan fish: switching from chemical to visual cues. Behaviour 137:181–195.  https://doi.org/10.1163/156853900502015 CrossRefGoogle Scholar
  18. Dall SR, Giraldeau L-A, Olsson O, McNamara JM, Stephens DW (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20:187–193.  https://doi.org/10.1016/j.tree.2005.01.010 CrossRefGoogle Scholar
  19. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54.  https://doi.org/10.1111/1365-2656.12013 CrossRefGoogle Scholar
  20. Dinno A (2015) Package ‘paran’: Horn’s test of principal components/factors. https://cran.r-project.org/web/packages/paran/
  21. Døving KB, Lastein S (2009) The alarm reaction in fishes—odorants, modulations of responses, neural pathways. Ann N Y Acad Sci 1170:413–423.  https://doi.org/10.1111/j.1749-6632.2009.04111.x CrossRefGoogle Scholar
  22. Elvidge CK, MacNaughton CJ, Brown GE (2013) Sensory complementation and antipredator behavoural compensation in acid impacted juvenile Atlantic salmon. Oecologia 172:69–78.  https://doi.org/10.1007/s00442-012-2478-6 CrossRefGoogle Scholar
  23. Ferrari MC, Chivers DP (2006) Learning threat-sensitive predator avoidance: how do fathead minnows incorporate conflicting information? Anim Behav 71:19–26.  https://doi.org/10.1016/j.anbehav.2005.02.016 CrossRefGoogle Scholar
  24. Ferrari MCO, Messier F, Chivers DP (2008) Can prey exhibit threat-sensitive generalization of predator recognition? Extending the predator recognition continuum hypothesis. Proc R Soc B 275:1811–1816.  https://doi.org/10.1098/rspb.2008.0305 CrossRefGoogle Scholar
  25. Ferrari MC, Wisenden BD, Chivers DP (2010) Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724.  https://doi.org/10.1139/Z10-029 CrossRefGoogle Scholar
  26. FitzGerald GJ, Wootton RJ (1993) The behavioural ecology of sticklebacks. In: Pitcher TJ (ed) Behaviour of teleost fishes. Chapman & Hall, London, pp 537–572CrossRefGoogle Scholar
  27. Frommen JG, Herder F, Engqvist L, Mehlis M, Bakker TC, Schwarzer J, Thünken T (2011) Costly plastic morphological responses to predator specific odour cues in three-spined sticklebacks (Gasterosteus aculeatus). Evol Ecol 25:641–656.  https://doi.org/10.1007/s10682-010-9454-6 CrossRefGoogle Scholar
  28. Giesing ER, Suski CD, Warner RE, Bell AM (2010) Female sticklebacks transfer information via eggs: effects of maternal experience with predators on offspring. Proc R Soc B 278:1753–1759.  https://doi.org/10.1098/rspb.2010.1819 CrossRefGoogle Scholar
  29. Gonzalo A, Cabido C, López P, Martín J (2012) Conspecific alarm cues, but not predator cues alone, determine antipredator behavior of larval southern marbled newts, Triturus pygmaeus. Acta Ethol 15:211–216.  https://doi.org/10.1007/s10211-012-0123-3 CrossRefGoogle Scholar
  30. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22.  https://doi.org/10.18637/jss.v033.i02 CrossRefGoogle Scholar
  31. Hall AE, Clark TD (2016) Seeing is believing: metabolism provides insight into threat perception for a prey species of coral reef fish. Anim Behav 115:117–126.  https://doi.org/10.1016/j.anbehav.2016.03.008 CrossRefGoogle Scholar
  32. Hartman EJ, Abrahams MV (2000) Sensory compensation and the detection of predators: the interaction between chemical and visual information. Proc R Soc Lond B 267:571–575.  https://doi.org/10.1098/rspb.2000.1039 CrossRefGoogle Scholar
  33. Hettyey A, Tóth Z, Thonhauser KE, Frommen JG, Penn DJ, Van Buskirk J (2015) The relative importance of prey-borne and predator-borne chemical cues for inducible antipredator responses in tadpoles. Oecologia 179:699–710.  https://doi.org/10.1007/s00442-015-3382-7 CrossRefGoogle Scholar
  34. Hoogland R, Morris D, Tinbergen N (1956) The spines of sticklebacks (Gasterosteus and Pygosteus) as means of defence against predators (Perca and Esox). Behaviour 10:205–236.  https://doi.org/10.1163/156853956X00156 CrossRefGoogle Scholar
  35. Huntingford FA (1976) A comparison of the reaction of sticklebacks in different reproductive conditions towards conspecifics and predators. Anim Behav 24:694–697.  https://doi.org/10.1016/S0003-3472(76)80083-8 CrossRefGoogle Scholar
  36. Huntingford F, Giles N (1987) Individual variation in anti-predator responses in the three-spined stickleback (Gasterosteus aculeatus L.). Ethology 74:205–210.  https://doi.org/10.1111/j.1439-0310.1987.tb00933.x CrossRefGoogle Scholar
  37. Huntingford FA, Ruiz-Gomez M (2009) Three-spined sticklebacks Gasterosteus aculeatus as a model for exploring behavioural biology. J Fish Biol 75:1943–1976.  https://doi.org/10.1111/j.1095-8649.2009.02420.x CrossRefGoogle Scholar
  38. Huntingford FA, Wright PJ, Tierney JF (1994) Adaptive variation in antipredator behaviour in threespine stickleback. In: Bell MA, Foster SA (eds) The evolutionary biology of the Threespine stickleback. Oxford University Press, New York, NY, pp 277–296Google Scholar
  39. Jolles JW, Taylor BA, Manica A (2016) Recent social conditions affect boldness repeatability in individual sticklebacks. Anim Behav 112:139–145.  https://doi.org/10.1016/j.anbehav.2015.12.010 CrossRefGoogle Scholar
  40. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Écoscience 5:361–394.  https://doi.org/10.1080/11956860.1998.11682468 CrossRefGoogle Scholar
  41. Kelley JL, Magurran AE (2003) Learned predator recognition and antipredator responses in fishes. Fish Fish 4:216–226.  https://doi.org/10.1046/j.1467-2979.2003.00126.x CrossRefGoogle Scholar
  42. Kim SY (2016) Fixed behavioural plasticity in response to predation risk in the three-spined stickleback. Anim Behav 112:147–152.  https://doi.org/10.1016/j.anbehav.2015.12.004 CrossRefGoogle Scholar
  43. Kim JW, Brown GE, Dolinsek IJ, Brodeur NN, Leduc AOHC, Grant JWA (2009) Combined effects of chemical and visual information in eliciting antipredator behavior in juvenile Atlantic salmon Salmo salar. J Fish Biol 74:1280–1290.  https://doi.org/10.1111/j.1095-8649.2009.02199.x CrossRefGoogle Scholar
  44. Krause J, Godin J-GJ (1996) Influence of prey foraging posture on flight behavior and predation risk: predators take advantage of unwary prey. Behav Ecol 7:264–271.  https://doi.org/10.1093/beheco/7.3.264 CrossRefGoogle Scholar
  45. Laundré JW, Hernández L, Ripple WJ (2010) The landscape of fear: ecological implications of being afraid. Open Ecol J 3:1–7.  https://doi.org/10.2174/1874213001003030001 CrossRefGoogle Scholar
  46. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640.  https://doi.org/10.1139/z90-092 CrossRefGoogle Scholar
  47. Manassa RP, Dixson DL, McCormick MI, Chivers DP (2013) Coral reef fish incorporate multiple sources of visual and chemical information to mediate predation risk. Anim Behav 86:717–722.  https://doi.org/10.1016/j.anbehav.2013.07.003 CrossRefGoogle Scholar
  48. Martin CW, Fodrie FJ, Heck KL, Mattila J (2010) Differential habitat use and antipredator response of juvenile roach (Rutilus rutilus) to olfactory and visual cues from multiple predators. Oecologia 162:893–902.  https://doi.org/10.1007/s00442-010-1564-x CrossRefGoogle Scholar
  49. McLean EB, Godin J-GJ (1989) Distance to cover and fleeing from predators in fish with different amounts of defensive Armour. Oikos 55:281–290.  https://doi.org/10.2307/3565586 CrossRefGoogle Scholar
  50. Meuthen D, Flege P, Brandt R, Thünken T (2018) The location of damage-released alarm cues in a cichlid fish. Evol Ecol Res 19:529–546Google Scholar
  51. Mikheev VN, Wanzenböck J, Pasternak AF (2006) Effects of predator-induced visual and olfactory cues on 0+ perch (Perca fluviatilis L.) foraging behavior. Ecol Freshw Fish 15:111–117.  https://doi.org/10.1111/j.1600-0633.2006.00140.x CrossRefGoogle Scholar
  52. Milinski M, Heller R (1978) Influence of a predator on the optimal foraging behavior of sticklebacks (Gasterosteus aculeatus L.). Nature 275:642–664.  https://doi.org/10.1038/275642a0 CrossRefGoogle Scholar
  53. Mirza RS, Chivers DP (2003) Fathead minnows learn to recognize heterospecific alarm cues they detect in the diet of a known predator. Behav 140:1359–1370CrossRefGoogle Scholar
  54. Mitchell MD, Bairos-Novak KR, Ferrari MC (2017) Mechanisms underlying the control of responses to predator odours in aquatic prey. J Exp Biol 220:1937–1946.  https://doi.org/10.1242/jeb.135137 CrossRefGoogle Scholar
  55. Moll RJ, Redilla KM, Mudumba T, Muneza AB, Gray SM, Abade L, Hayward MW, Millspaugh JJ, Montgomery RA (2017) The many faces of fear: a synthesis of the methodological variation in characterizing predation risk. J Anim Ecol 86:749–765.  https://doi.org/10.1111/1365-2656.12680 CrossRefGoogle Scholar
  56. Näslund J, Lindström E, Lai F, Jutfelt F (2015) Behavioural responses to simulated bird attacks in marine three-spined sticklebacks after exposure to high CO2 levels. Mar Freshw Res 66:877–885.  https://doi.org/10.1071/MF14144 CrossRefGoogle Scholar
  57. Näslund J, Pettersson L, Johnsson JI (2016) Behavioural reactions of three-spined sticklebacks to simulated risk of predation – effects of predator distance and movement. FACETS 1:55–66.  https://doi.org/10.1139/facets-2015-0015 CrossRefGoogle Scholar
  58. Östlund-Nilsson S, Mayer I, Huntingford FA (2006) Biology of the three-spined stickleback. CRC Press, Boca Raton, FLCrossRefGoogle Scholar
  59. Pitcher TJ, Green DA, Magurran AE (1986) Dicing with death: predator inspection behaviour in minnow shoals. J Fish Biol 28:439–448.  https://doi.org/10.1111/j.1095-8649.1986.tb05181.x CrossRefGoogle Scholar
  60. Pollock MS, Chivers DP, Mirza RS, Wisenden BD (2003) Fathead minnows learn to recognize chemical alarm cues of introduced brook stickleback. Environ Biol Fish 66:313–319CrossRefGoogle Scholar
  61. R Core Team (2017) R: A Language and Environment for Statistical Computing. https://www.r-project.org/
  62. Roberts LJ, de Leaniz CG (2011) Something smells fishy: predator-naïve salmon use diet cues, not kairomones, to recognize a sympatric mammalian predator. Anim Behav 82:619–625.  https://doi.org/10.1016/j.anbehav.2011.06.019 CrossRefGoogle Scholar
  63. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals, and mimicry. Oxford University Press, OxfordCrossRefGoogle Scholar
  64. Šmejkal M, Ricard D, Sajdlová Z, Čech M, Vejřík L, Blabolil P, Vejříková I, Prchalová M, Vašek M, Souza AT, Brönmark C, Peterka J (2017) Can species-specific prey responses to chemical cues explain prey susceptibility to predation? Ecol Evol 8:4544–4551.  https://doi.org/10.1002/ece3.4000 CrossRefGoogle Scholar
  65. Smith ME, Belk MC (2001) Risk assessment in western mosquitofish (Gambusia affinis): do multiple cues have additive effects? Behav Ecol Sociobiol 51:101–107.  https://doi.org/10.1007/s002650100415 CrossRefGoogle Scholar
  66. Soluk DA (1993) Multiple predator effects: predicting combined functional response of stream fish and invertebrate predators. Ecology 74:219–225.  https://doi.org/10.2307/1939516 CrossRefGoogle Scholar
  67. Stauffer H-P, Semlitsch RD (1993) Effects of visual, chemical and tactile cues of fish on the behavioural responses of tadpoles. Anim Behav 46:355–364.  https://doi.org/10.1006/anbe.1993.1197 CrossRefGoogle Scholar
  68. Teplitsky C, Plenet S, Joly P (2004) Hierarchical responses of tadpoles to multiple predators. Ecology 85:2888–2894.  https://doi.org/10.1890/03-3043 CrossRefGoogle Scholar
  69. Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, NJGoogle Scholar
  70. Tollrian R, Duggen S, Weiss LC, Laforsch C, Kopp M (2015) Density-dependent adjustment of inducible defenses. Sci Rep 5:12736.  https://doi.org/10.1038/srep12736 CrossRefGoogle Scholar
  71. Tulley JJ, Huntingford FA (1987) Age, experience and the development of adaptive variation in anti-predator responses in three-spined sticklebacks (Gasterosteus aculeatus). Ethology 75:285–290.  https://doi.org/10.1111/j.1439-0310.1987.tb00660.x CrossRefGoogle Scholar
  72. Vainikka A, Jokelainen T, Kortet R, Ylönen H (2005) Predation risk allocation or direct vigilance response in the predator interaction between perch (Perca fluviatilis L.) and pike (Esox lucius L.)? Ecol Freshw Fish 14:225–232.  https://doi.org/10.1111/j.1600-0633.2005.00095.x CrossRefGoogle Scholar
  73. Walling CA, Dawnay N, Kazem AJ, Wright J (2004) Predator inspection behavior in three-spined sticklebacks (Gasterosteus aculeatus): body size, local predation pressure and cooperation. Behav Ecol Sociobiol 56:164–170.  https://doi.org/10.1007/s00265-004-0763-z CrossRefGoogle Scholar
  74. Weissburg M, Smee DL, Ferner MC (2014) The sensory ecology of non-consumptive predator effects. Am Nat 184:141–157.  https://doi.org/10.1086/676644 CrossRefGoogle Scholar
  75. Wisenden BD (2000) Scents of danger: the evolution of olfactory ornamentation in chemically-mediated predator-prey interactions. In: Espmark Y, Amundsen T, Rosenqvist G (eds) Animal signals: Signalling and signal Design in Animal Communication. Tapir Academic Press, Trondheim, pp 3645–3386Google Scholar
  76. Wisenden BD, Chivers DP (2006) The role of public chemical information in antipredator behaviour. In: Ladich F (ed) Communication in fishes. Science Publisher, Enfield, NH, pp 259–278Google Scholar
  77. Wootton RJ (1984) A functional biology of sticklebacks. University of California Press, California, FLCrossRefGoogle Scholar

Copyright information

© ISPA, CRL 2019

Authors and Affiliations

  1. 1.Department of Ecology and Animal BiologyUniversity of VigoVigoSpain
  2. 2.Department of Ecosystem Biology & SoWaUniversity of South BohemiaČeské BudějoviceCzech Republic
  3. 3.Department of Biological and Environmental SciencesUniversity of GothenburgGothenburgSweden
  4. 4.Department of ZoologyStockholm UniversityStockholmSweden

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