Korean Journal of Ecology and Environment (생태와환경)

The Korean Society of Limnology (한국수생태학회)
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Change of Predator Recognition Depends on Exposure of Predation Risk Source in Captive Breed Endangered Freshwater Fish, Microphysogobio rapidus

인공증식된 멸종위기종 여울마자의 포식 위험원 노출에 따른 포식자 인지 변화

  • Moon-Seong Heo (Research Center for Endangered Species, National Institute of Ecology) ;
  • Min-Ho Jang (Department Biology Education, Kongju National University) ;
  • Ju-Duk Yoon (Research Center for Endangered Species, National Institute of Ecology)
  • 허문성 (국립생태원 멸종위기종복원센터) ;
  • 장민호 (공주대학교 생물교육과) ;
  • 윤주덕 (국립생태원 멸종위기종복원센터)
  • Received : 2023.12.13
  • Accepted : 2023.12.19
  • Published : 2023.12.31
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Abstract

Captive breeding and reintroduction are crucial strategies for conserving endangered species populations. However, fish raised in predator-free environments, show a lack of recognition of predationrelated stimuli such as chemical and visual signals. It is critical to recognize chemical signals from injured conspecifics, also known as alarm signals, and the order or shape of predators to indicate the spread of predation risk in the habitat. We conducted a laboratory experiment to determine and adjust the optimal exposure period to induce appropriate anti-predator behavior response to different types of stimuli (Chemical, Visual and Chemical+Visual) for the endangered species Microphysogobio rapidus. Our results demonstrate that predator avoidance behavior varies depending on the types of stimuli and the duration of predation risk exposure. First, the results showed captive-breed M. rapidus show lack of response against conspecific alarm signal (Chemical cue) before the predation risk exposure period and tend to increase response over predation risk exposure time. Second, response to predator (visual cue) tend to peak at 48 hours cumulative exposure, but show dramatic decrease after 72 hours cumulative exposure. Finally, response to the mixed cue (Chemical+visual) tend to peak prior to the predation risk exposure period and show reduced response during subsequent exposure periods. This experiment confirms the lack of responsiveness to conspecific alarm signals in captive-bred M. rapidus and the need for an optimal nature behavior enhancement program prior to release of endangered species. Furthermore, responsiveness to predator visual signal peak at 48 hours cumulative exposure, suggest an optimal predation risk exposure period of up to 48 hours.

어류의 시각적 및 화학적 정보를 토대로 포식자를 인지하는 능력은 개체가 자연에서 생활하는 동안 학습을 통해서 확보된다. 하지만 인공증식된 멸종위기종들의 경우 자연적응력 부족으로 인한 복원효율성 저하가 지속적으로 발생하고 있다. 따라서 본 연구에서는 복원을 위해 인공증식된 멸종위기종 여울마자의 자연적응력 증진을 위해 포식자 인지 능력 증진을 수행하였다. 연구결과 포식자 인지 훈련 기간에 따라 자극원에 대한 반응성이 달라짐을 확인할 수 있었으며, 인공증식된 여울마자는 동종의 알람신호를 통해 위험을 인지하는 능력이 떨어져 있었으며, 이는 포식 위험원 노출을 통한 훈련으로 개선이 가능하였고, 포식자에 노출되었을 때 포식자와 알람신호에 동시에 노출 되었을 경우 훈련 기간이 길어짐에 따라 자극에 대한 반응성이 줄어드는 것을 확인하였다. 알람신호에 대한 반응은 시간이 지날수록 커지는 경향을, 포식자에 대한 반응은 훈련 48시간 후 가장 높은 반응을 보이고 72시간 후 반응성이 떨어지는 경향을, 알람신호와 포식자 동시 노출에 대한 반응은 훈련 이전 가장 높은 반응을 보인 뒤 반응성이 낮아진 채로 유지되는 경향을 보였다. 따라서 방류 전 인공증식 개체의 동종의 알람신호(화학적 자극)에 대한 반응성을 높이기 위한 프로그램이 필요하며, 포식자(시각적 자극)에 대한 반응성도 높게 나타난 48시간가량의 포식 위험원 노출이 적합하다고 판단된다. 본 실험을 통해 인공증식 여울마자의 동족 알람신호 자극에 대한 반응성 부족이 확인되었으며 멸종위기종 방류전 자연성 증진 프로그램의 운용의 필요성이 확인되었다.

Keywords

Acknowledgement

본 논문은 환경부의 지원을 받아 수행하였습니다 (NIE-고유연구-2023-47).

References

  1. Alvarez, D. and A.G. Nicieza. 2003. Predator avoidance behaviour in wild and hatchery-reared brown trout: the role of experience and domestication. Journal of Fish Biology 63: 1565-1577. https://doi.org/10.1111/j.1095-8649.2003.00267.x
  2. Archer, S.K. and T.A. Crowl. 2014. Retention of learned predator recognition in an endangered sucker Chasmistes liorus liorus. Aquatic Biology 20: 195-202. https://doi.org/10.3354/ab00558
  3. Bairos-Novak, K.R., M.C.O. Ferrari and D.P. Chivers. 2019. A novel alarm signal in aquatic prey: Familiar minnows coordinate group defences against predators through chemical disturbance cues. Journal of Animal Ecology 88: 1281-1290. https://doi.org/10.1111/1365-2656.12986
  4. Berejikian, B.A., R.J.F. Smith, E.P. Tezak, S.L. Schroder and C.M. Knudsen. 1999. Chemical alarm signals and complex hatchery rearing habitats affect antipredator behavior and survival of chinook salmon (Oncorhynchus tshawytscha) juveniles. Canadian Journal of Fisheries and Aquatic Sciences 56(5): 830-838. https://doi.org/10.1139/f99-010
  5. Berejikian, B.A., E.P. Tezak and A.L. LaRae. 2003. Innate and enhanced predator recognition in hatchery-reared chinook salmon. Environmental Biology of Fishes 67: 241-251. https://doi.org/10.1023/A:1025887015436
  6. Bergendahl, A.I., A.G.V. Salvanes and V.A. Braithwaite. 2016. Determining the effects of duration and recency of exposure to environmental enrichment. Applied Animal Behaviour Science 176: 163-169. https://doi.org/10.1016/j.applanim.2015.11.002
  7. Bergendahl, A.I., S. Miller, C. Depasquale, L. Giralico and V.A. Braithwaite. 2017. Becoming a better swimmer: structural complexity enhances agility in a captive-reared fish. Journal of Fish Biology 90(3): 1112-1117. https://doi.org/10.1111/jfb.13232
  8. Billman, E.J., J.E. Rasmussen and J. Watson. 2011. Evaluation of Release Strategies for Captive-Reared June Sucker Based on Poststocking Survival. Western North American Naturalist 71(4): 481-489. https://doi.org/10.3398/064.071.0405
  9. Brown, C. and K. Laland. 2001. Social learning and life skills training for hatchery reared fish. Journal of Fish Biology 59: 471-493. https://doi.org/10.1111/j.1095-8649.2001.tb02354.x
  10. Brown, G.E., A.C. Rive, M.C.O. Ferrari and D.P. Chivers. 2006. The dynamic nature of antipredator behavior: prey fish integrate threat-sensitive antipredator responses within background levels of predation risk. Behavioral Ecology Sociobiology 61: 9-16. https://doi.org/10.1007/s00265-006-0232-y
  11. Bruton, M.N. 1995. Have fishes had their chips? The dilemma of threatened fishes. Environmental Biology of Fishes 43: 1-27. https://doi.org/10.1007/BF00001812
  12. Clarke, C.N., D.J. Fraser and C.F. Purchase. 2015. Lifelong and carry-over effects of early captive exposure in a recovery program for Atlantic salmon (Salmo salar). Animal Conservation 19(4): 350-359. https://doi.org/10.1111/acv.12251
  13. D'Anna, G., V.M. Giacalone, T.V. Fernandez, A.M. Vaccaro, C. Pipitone, S. Mirto, S. Mazzola and F. Badalamenti. 2012. Effects of predator and shelter conditioning on hatchery-reared white seabream Diplodus sargus (L., 1758) released at sea. Aquaculture 356-357: 91-97. https://doi.org/10.1016/j.aquaculture.2012.05.032
  14. Day, J.L., J.L. Jacobs and J. Rasmussen. 2017. Considerations for the Propagation and Conservation of Endangered Lake Suckers of the Western United States. Journal of Fish and Wildlife Management 8(1): 301-312.
  15. Edwards, M.C., C. Ford, J.M. Hoy, S. FitzGibbon and P.J. Murray. 2021. How to train your wildlife: A review of predator avoidance training. Applied Animal Behaviour Science 234: 105170.
  16. Ferrari, M.C.O., C.K. Elvidge, C.D. Jackson, D.P. Chivers and G.E. Brown. 2010. The responses of prey fish to temporal variation in predation risk: Sensory habituation or risk assessment? Behavioral Ecology 21(3): 532-536. https://doi.org/10.1093/beheco/arq023
  17. Fraser, D.J. 2008. How well can captive breeding programs conserve biodiversity? A review of salmonids. Evolutionary Applications 1(4): 535-586. https://doi.org/10.1111/j.1752-4571.2008.00036.x
  18. Geist, J. and S.J. Hawkins. 2016. Habitat recovery and restoration in aquatic ecosystems: current progress and future challenges. Aquatic Conservation: Marine and Freshwater Ecosystem 26: 942-962. https://doi.org/10.1002/aqc.2702
  19. Goz, H. 1941. uber den Art-und Individualgeruch bei Fischen. Zeitschrift Vergleichende Physiologie 29: 1-45. https://doi.org/10.1007/BF00304444
  20. Hawkins, L.A., A.E. Magurran and J.D. Armstrong. 2008. Ontogenetic learning of predator recognition in hatchery-reared Atlantic salmon, Salmo salar. Animal Behaviour 75: 1663-1671. https://doi.org/10.1016/j.anbehav.2007.10.019
  21. Hutchison, M., D. Stewart, K. Chilcott, A. Butcher, A. Henderson, M. McLennan and P. Smith. 2012. Strategies to improve post release survival of hatchery-reared threatened fish species. Murray-Darling Basin Authority, Publication 135(11).
  22. Imre, I., R.T. Di Rocco, G.E. Brown and N.S. Johnson. 2016. Habituation of adult sea lamprey repeatedly exposed to damage-released alarm and predator cues. Environmental Biology of Fishes 99: 613-620. https://doi.org/10.1007/s10641-016-0503-z
  23. Johnsson, J.I., S. Brockmark and J. Naslund. 2014. Environmental effects on behavioural development consequences for fitness of captive-reared fishes in the wild. Journal of Fish Biology 85: 1946-1971. https://doi.org/10.1111/jfb.12547
  24. Kopack, C.J., E.D. Broder, E.R. Fetherman, J.M. Lepak and L.M. Angeloni. 2016. The effect of a single prerelease exposure to conspecific alarm cue on poststocking survival in three strains of rainbow trout (Oncorhynchus mykiss). Canadian Journal of Zoology 94(9): 661-664. https://doi.org/10.1139/cjz-2016-0086
  25. Lamothe, K.A., D.A.R. Drake, T.E. Pitcher, J.E. Broome, A.J. Dextrase, A. Gillespie, N.E. Mandrak, M.S. Poesch, S.M. Reid and N. Vachon. 2019. Reintroduction of fishes in Canada: a review of research progress for SARA-listed species. Environmental Reviews 27(4): 575-599. https://doi.org/10.1139/er-2019-0010
  26. Larson, J.K. and M.I. McCormick. 2005. The role of chemical alarm signals in facilitating learned recognition of novel chemical cues in a coral reef fish. Animal Behaviour 69(1): 51-57. https://doi.org/10.1016/j.anbehav.2004.04.005
  27. Malavasi, S., V. Georgalas, M. Lugli, P. Torricelli and D. Mainardi. 2004. Differences in the pattern of antipredator behaviour between hatchery-reared and wild European sea bass juveniles. Journal of Fish Biology 65: 143-155. https://doi.org/10.1111/j.0022-1112.2004.00545.x
  28. Maximino, C., R.X. do Carmo Silva, K. dos Santos Campos, J.S. de Oliveira, S.P. Rocha, M.P. Pyterson, D.P. dos Santos Souza, L.M. Feitosa, S.R. Ikeda, A.F. Pimentel and P.N. Ramos. 2019. Sensory ecology of ostariophysan alarm substances. Journal of Fish Biology 95(1): 274-286. https://doi.org/10.1111/jfb.13844
  29. Michael, H., B. Adam and N. Andrew. 2023. Conditioning to predators improves survival of stocked Murray cod (Maccullochella peelii) fingerlings. Marine and Freshwater Research 74: 1039-1049. https://doi.org/10.1071/MF22242
  30. Mirza, R.S. and D.P. Chivers. 2000. Predator-recognition training enhances survival of brook trout: evidence from laboratory and field-enclosure studies. Canadian Journal of Zoology 78(12): 2198-2208. https://doi.org/10.1139/z00-164
  31. Olson, J.A., J.M. Olson, R.E. Walsh and B.D. Wisenden. 2012. A Method to Train Groups of Predator-Naive Fish to Recognize and Respond to Predators When Released into the Natural Environment. North American Journal of Fisheries Management 32(1): 77-81. https://doi.org/10.1080/02755947.2012.661390
  32. Salvanes, A.G.V. and Braithwaite, V. 2006. The need to understand the behaviour of fish reared for mariculture or restocking. ICES Journal of Marine Science 63(2): 345-354. https://doi.org/10.1016/j.icesjms.2005.11.010
  33. Shively, R.S., T.P. Poe and S.T. Sauter. 1996. Feeding Response by Northern Squawfish to a Hatchery Release of Juvenile Salmonids in the Clearwater River, Idaho. Transactions of the American Fisheries Society 125(2): 230-236. https://doi.org/10.1577/1548-8659(1996)125<0230:FRBNST>2.3.CO;2
  34. Stunz, G.W. and T.J. Minello. 2001. Habitat-related predation on juvenile wild-caught and hatchery-reared red drum Sciaenops ocellatus (Linnaeus). Journal of Experimental Marine Biology and Ecology 260(1): 13-25. https://doi.org/10.1016/S0022-0981(01)00248-9
  35. Vilhunen, S. 2006. Repeated antipredator conditioning: a pathway to habituation or to better avoidance?. Journal of Fish Biology 68: 25-43. https://doi.org/10.1111/j.0022-1112.2006.00873.x
  36. Wisenden, B.D. 2011. Quantifying anti-predator response to chemical alarm cues, p. 49-60. In: Zebrafish Behavioral Protocols(Kalueff, A.V., P. Hart, J. LaPorte, eds.). Humana Press(Springer Science).
  37. Wishingrad, V., M.C. Ferrari and D.P. Chivers. 2014. Behavioural and morphological defences in a fish with a complex antipredator phenotype. Animal Behaviour 95: 137-143. https://doi.org/10.1016/j.anbehav.2014.07.006