Antipredator defences of young are independently determined by genetic inheritance, maternal effects and own early experience in mouthbrooding cichlids

Functional Ecology

Volumn 28, Issue 4, 2014, Pages 944-953

  Stratmann, Ariane ^a   Taborsky, Barbara ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Cichlids; Developmental plasticity; Growth; Innate predator defences; Maternal effects; Predator recognition

Indexed keywords

ANTIPREDATOR DEFENSE; CICHLID; GENE EXPRESSION; GROWTH RATE; HABITAT TYPE; HERITABILITY; JUVENILE; LIFE HISTORY TRAIT; MATERNAL CARE; NATURAL SELECTION; PARENT-OFFSPRING INTERACTION; PREDATION RISK; VULNERABILITY;

AFRICA;

AFRICAN CICHLIDS; CICHLIDAE; CTENOCHROMIS HOREI; SIMOCHROMIS;

EID: 84904339524     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12224     Document Type: Article

References (54)

1. Abjörnsson, K., Hansson, L.A. & Brönmark, C. (2004) Responses of prey from habitats with different predator regimes: local adaptation and heritability. Ecology, 85, 1859-1866.
2. Adriaenssens, B. & Johnsson, J.I. (2009) Personality and life-history productivity: consistent or variable association? Trends in Ecology & Evolution, 24, 179-180.
3. Bize, P., Diaz, C. & Lindström, J. (2012) Experimental evidence that adult antipredator behaviour is heritable and not influenced by behavioural copying in a wild bird. Proceedings of the Royal Society B-Biological Sciences, 279, 1380-1388.
4. Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H. et al. (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution, 24, 127-135.
5. Brown, G.E., Ferrari, M.C.O. & Chivers, D.P. (2011) Learning about Danger: chemical alarm cues and threat-sensitive assessment of predation risk by fishes. Fish cognition and behavior (eds C. Brown, K.N. Laland & J. Krause), pp. 59-80. Wiley-Blackwell, Oxford.
6. Brown, C., Gardner, C. & Braithwaite, V.A. (2005) Differential stress responses in fish from areas of high- and low-predation pressure. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology, 175, 305-312.
7. Coleman, K. & Wilson, D.S. (1998) Shyness and boldness in pumpkinseed sunfish: individual differences are context-specific. Animal Behaviour, 56, 927-936.
8. Colombelli-Negrel, D., Hauber, M.E., Robertson, J., Sulloway, F.J., Hoi, H., Griggio, M. et al. (2012) Embryonic learning of vocal passwords in superb fairy-wrens reveals intruder cuckoo nestlings. Current Biology, 22, 2155-2160.
9. Coslovsky, M. & Richner, H. (2011) Predation risk affects offspring growth via maternal effects. Functional Ecology, 25, 878-888.
10. Dingemanse, N.J., Wright, J., Kazem, A.J., Thomas, D.K., Hickling, R. & Dawnay, N. (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. Journal of Animal Ecology, 76, 1128-1138.
11. Dzialowski, A.R., Lennon, J.T., O'Brien, W.J. & Smith, V.H. (2003) Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi. Freshwater Biology, 48, 1593-1602.
12. Espmark, Y. & Langvatn, R. (1985) Development and habituation of cardiac and behavioral responses in young red deer calves (Cervus elaphus) exposed to alarm stimuli. Journal of Mammalogy, 66, 702-711.
13. Fendt, M. (2006) Exposure to urine of canids and felids, but not of herbivores, induces defensive behavior in laboratory rats. Journal of Chemical Ecology, 32, 2617-2627.
14. Ferrari, M.C.O., Wisenden, B.D. & Chivers, D.P. (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Canadian Journal of Zoology, 88, 698-724.
15. Ferrari, M.C., Gonzalo, A., Messier, F. & Chivers, D.P. (2007) Generalization of learned predator recognition: an experimental test and framework for future studies. Proceedings of the Royal Society B-Biological Sciences, 274, 1853-1859.
16. Giesing, E.R., Suski, C.D., Warner, R.E. & Bell, A.M. (2011) Female sticklebacks transfer information via eggs: effects of maternal experience with predators on offspring. Proceedings of the Royal Society B-Biological Sciences, 278, 1753-1759.
17. Gosselin, L.A. & Qian, P.Y. (1997) Juvenile mortality in benthic marine invertebrates. Marine Ecology-Progress Series, 146, 265-282.
18. Göth, A. (2001) Innate predator-recognition in Australian brush-turkey (Alectura lathami, Megapodiidae) hatchlings. Behaviour, 138, 117-136.
19. Hawkins, L.A., Magurran, A.E. & Armstrong, J.D. (2007) Innate abilities to distinguish between predator species and cue concentration in Atlantic salmon. Animal Behaviour, 73, 1051-1057.
20. Hirvonen, H., Ranta, E., Piironen, J., Laurila, A. & Peuhkuri, N. (2000) Behavioural responses of naive Arctic charr young to chemical cues from salmonid and non-salmonid fish. Oikos, 88, 191-199.
21. Husak, J.F. (2006) Does speed help you survive? A test with Collared Lizards of different ages. Functional Ecology, 20, 174-179.
22. Jones, D.R. (1971) Theoretical analysis of factors which may limit maximum oxygen uptake of fish - oxygen cost of cardiac and branchial pumps. Journal of Theoretical Biology, 32, 341-349.
23. Kaplan, R.H. & Phillips, P.C. (2006) Ecological and developmental context of natural selection: maternal effects and thermally induced plasticity in the frog Bombina orientalis. Evolution, 60, 142-156.
24. Kempster, R.M., Hart, N.S. & Collin, S.P. (2013) Survival of the stillest: predator avoidance in shark embryos. PLoS ONE 8, e52551.
25. Kotrschal, A. & Taborsky, B. (2010) Resource defence or exploded lek? - A question of perspective. Ethology, 116, 1189-1198.
26. Kotrschal, A., Heckel, G., Bonfils, D. & Taborsky, B. (2012) Life-stage specific environments in a cichlid fish: implications for inducible maternal effects. Evolutionary Ecology, 26, 123-137.
27. Laurila, A., Kujasalo, J. & Ranta, E. (1997) Different antipredator behaviour in two anuran tadpoles: effects of predator diet. Behavioral Ecology and Sociobiology, 40, 329-336.
28. Lima, S.L. & Dill, L.M. (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology, 68, 619-640.
29. Lindholm, A.K., Hunt, J. & Brooks, R. (2006) Where do all the maternal effects go? Variation in offspring body size through ontogeny in the live-bearing fish Poecilia parae. Biology Letters, 2, 586-589.
30. Magurran, A.E. (1990) The inheritance and development of minnow antipredator behavior. Animal Behaviour, 39, 834-842.
31. Mathis, A., Ferrari, M.C.O., Windel, N., Messier, F. & Chivers, D.P. (2008) Learning by embryos and the ghost of predation future. Proceedings of the Royal Society B-Biological Sciences, 275, 2603-2607.
32. McCormick, M.I. (1998) Behaviorally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology, 79, 1873-1883.
33. McCormick, M.I. (2006) Mothers matter: crowding leads to stressed mothers and smaller offspring in marine fish. Ecology, 87, 1104-1109.
34. McGhee, K.E., Pintor, L.M., Suhr, E.L. & Bell, A.M. (2012) Maternal exposure to predation risk decreases offspring antipredator behaviour and survival in threespined stickleback. Functional Ecology, 26, 932-940.
35. Metcalfe, N.B. & Monaghan, P. (2001) Compensation for a bad start: grow now, pay later? Trends in Ecology & Evolution, 16, 254-260.
36. Ochi, H. (1993) Mate monopolization by a dominant male in a multi-male social group of a mouthbrooding cichlid, Ctenochromis horei. Japanese Journal of Ichthyology, 40, 209-218.
37. Scheurer, J.A., Berejikian, B.A., Thrower, F.P., Ammann, E.R. & Flagg, T.A. (2007) Innate predator recognition and fright response in related populations of Oncorhynchus mykiss under different predation pressure. Journal of Fish Biology, 70, 1057-1069.
38. Schürch, R. & Taborsky, B. (2005) The functional significance of buccal feeding in the mouthbrooding cichlid Tropheus moorii. Behaviour, 142, 265-281.
39. Sefc, K., Hermann, C. & Koblmueller, S. (2009) Mating system variability in a mouthbrooding cichlid fish from a tropical lake. Molecular Ecology, 18, 3508-3517.
40. Segers, F.H.I.D., Berishvili, G. & Taborsky, B. (2012) Egg size-dependent expression of growth hormone receptor accompanies compensatory growth in fish. Proceedings of the Royal Society B-Biological Sciences, 279, 592-600.
41. Segers, F.H.I.D., Gerber, B. & Taborsky, B. (2011) Do maternal food deprivation and offspring predator cues interactively affect maternal effort in fish? Ethology, 117, 708-721.
42. Segers, F.H.I.D. & Taborsky, B. (2011) Egg size and food abundance interactively affect juvenile growth and behaviour. Functional Ecology, 25, 166-176.
43. Segers, F.H.I.D. & Taborsky, B. (2012) Juvenile exposure to predator cues induces a larger egg size in fish. Proceedings of the Royal Society B-Biological Sciences, 279, 1241-1248.
44. Sheriff, M.J., Krebs, C.J. & Boonstra, R. (2010) The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk. Ecology, 91, 2983-2994.
45. Smith, E.N. & Woodruff, R.A. (1980) Fear bradycardia in free-ranging woodchucks, Marmota monax. Journal of Mammalogy, 61, 750-753.
46. Sogard, S.M. (1997) Size-selective mortality in the juvenile stage of teleost fishes: a review. Bulletin of Marine Sciences, 60, 1129-1157.
47. Storm, J.J. & Lima, S.L. (2010) Mothers forewarn offspring about predators: a transgenerational maternal effect on behavior. American Naturalist, 175, 382-390.
48. Taborsky, B. (2006a) Mothers determine offspring size in response to own juvenile growth conditions. Biology Letters, 2, 225-228.
49. Taborsky, B. (2006b) The influence of juvenile and adult environments on life-history trajectories. Proceedings of the Royal Society B-Biological Sciences, 273, 741-750.
50. Tollrian, R. (1995) Predator-induced morphological defenses - costs, life-history shifts, and maternal effects in Daphnia-pulex. Ecology, 76, 1691-1705.
51. Uller, T. (2008) Developmental plasticity and the evolution of parental effects. Trends in Ecology & Evolution, 23, 432-438.
52. Veen, T., Richardson, D.S., Blaakmeer, K. & Komdeur, J. (2000) Experimental evidence for innate predator recognition in the Seychelles warbler. Proceedings of the Royal Society B-Biological Sciences, 267, 2253-2258.
53. Verhoeven, K.J.F., Simonsen, K.L. & McIntyre, L.M. (2005) Implementing false discovery rate control: increasing your power. Oikos, 108, 643-647.
54. Vilhunen, S. & Hirvonen, H. (2003) Innate antipredator responses of Arctic charr (Salvelinus alpinus) depend on predator species and their diet. Behavioral Ecology and Sociobiology, 55, 1-10.