To eat or not to eat: Egg-based assessment of paternity triggers fine-tuned decisions about filial cannibalism

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1694, 2010, Pages 2627-2635

  Mehlis, Marion ^a   Bakker, Theo C M ^a   Engqvist, Leif ^a,b   Frommen, Joachim G ^a,c  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c KONRAD LORENZ INSTITUTE FOR ETHOLOGY   (Austria)

Author keywords

Aggression; Brood care; Kin recognition; Oophagy; Parent offspring conflict; Three spined stickleback

Indexed keywords

AGGREGATION BEHAVIOR; BREEDING SEASON; BROOD REARING; CANNIBALISM; EGG; KIN RECOGNITION; PATERNITY; SURVIVAL; TELEOST;

ANIMALIA; GASTEROSTEUS ACULEATUS; HEXAPODA; MAMMALIA; TELEOSTEI;

EID: 77956944283     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.0234     Document Type: Conference Paper

References (70)

1. Allen, J. R. M. & Wootton, R. J. 1982 Age, growth and rate of food consumption in an upland population of the three-spined stickleback, Gasterosteus aculeatus L. J. Fish Biol. 21, 95-105. (doi:10.1111/j.1095-8649. 1982.tb02827.x)
2. Bakker, T. C. M. 1986 Aggressiveness in sticklebacks (Gasterosteus aculeatus L.): a behaviour-genetic study. Behaviour 98, 1-144. (doi:10.1163/156853986X00937)
3. Bakker, T. C. M. & Mundwiler, B. 1994 Female mate choice and male red coloration in a natural three-spined stickleback (Gasterosteus aculeatus) population. Behav. Ecol. 5, 74-80. (doi:10.1093/beheco/5.1.74)
4. Bakker, T. C. M., Mazzi, D. & Kraak, S. B. M. 2006a Broods of attractive three-spined stickleback males require greater paternal care. J. Fish Biol. 69, 1164-1177. (doi:10.1111/j. 1095-8649.2006.01194.x)
5. Bakker, T. C. M., Zbinden, M., Frommen, J. G., Weiss, A. & Largiadèr, C. R. 2006b Slow fertilization of stickleback eggs: the result of sexual conflict? BMC Ecol. 6, 7. (doi:10.1186/1472-6785-6-7) (Pubitemid 43938740)
6. Bates, D. & Maechler, M. 2009 lme4: linear mixed-effects models using S4 classes. R package version 0.999375-31.
7. Belles-Isles, J. C. & FitzGerald, G. J. 1991 Filial cannibalism in sticklebacks: a reproductive management strategy? Ethol. Ecol. Evol. 3, 49-62.
8. Bolger, T. & Connolly, P. L. 1989 The selection of suitable indices for the measurement and analysis of fish condition. J. Fish Biol. 34, 171-182. (doi:10.1111/j.1095-8649.1989.tb03300.x)
9. Chin-Baarstad, A., Klug, H. & Lindström, K. 2009 Should you eat your offspring before someone else does? Effect of an egg predator on filial cannibalism in the sand goby. Anim. Behav. 78, 203-208. (doi:10.1016/j.anbe-hav. 2009.04.022)
10. Clutton-Brock, T. H. 1991 The evolution of parental care. Princeton, NJ: Princeton University Press.
11. Collins, L. A. & Nelson, S. G. 1993 Effects of temperature on oxygen consumption, growth, and development of embryos and yolk-sac larvae of Siganus randalli (Pisces, Siganidae). Mar. Biol. 117, 195-204. (doi:10.1007/ BF00345663)
12. Davies, N. B., Hatchwell, B. J., Robson, T. & Burke, T. 1992 Paternity and parental effort in dunnocks Prunella modularis: how good are male chick-feeding rules? Anim. Behav. 43, 729-745. (doi:10.1016/S0003-3472(05)80197- 6)
13. Dumont, H. J. & Ali, A. J. 2004 Stage-specific cannibalism and spontaneous cyst hatching in the freshwater fairy shrimp Streptocephalus proboscideus Frauenfeld. Hydrobiologia 524, 103-113. (doi:10.1023/B:HYDR. 0000036125.34891.12)
14. Elwood, R. W. 1991 Ethical implications of studies on infanticide and maternal aggression in rodents. Anim. Behav. 42, 841-849. (doi:10.1016/S0003- 3472(05)80128-9)
15. FitzGerald, G. J. 1992 Egg cannibalism by sticklebacks: spite or selfishness? Behav. Ecol. Sociobiol. 30, 201-206. (doi:10.1007/BF00166704)
16. Fletcher, D. A. & Wootton, R. J. 1995 A hierarchical response to differences in ration size in the reproductive performance of female three-spined sticklebacks. J. Fish Biol. 46, 657-668. (doi:10.1111/j.1095-8649. 1995. tb01102.x)
17. Forsgren, E., Karlsson, A. & Kvarnemo, C. 1996 Female sand gobies gain direct benefits by choosing males with eggs in their nests. Behav. Ecol. Sociobiol. 39, 91-96. (doi:10.1007/s002650050270) (Pubitemid 26311649)
18. Frommen, J. G. & Bakker, T. C. M. 2006 Inbreeding avoidance through non-random mating in sticklebacks. Biol. Lett. 2, 232-235. (doi:10.1098/rsbl. 2005.0432) (Pubitemid 43938641)
19. Frommen, J. G., Brendler, C. & Bakker, T. C. M. 2007 The tale of the bad stepfather: male three-spined sticklebacks (Gasterosteus aculeatus L.) recognize foreign eggs in their manipulated nest by egg cues alone. J. Fish Biol. 70, 1295-1301. (doi:10.1111/j.1095-8649.2007. 01390.x)
20. Gilbert, W. M., Nolan, P. M., Stoehr, A. M. & Hil, G. E. 2005 Filial cannibalism at a house finch nest. Wilson Bull. 117, 413-415. (doi:10.1676/04-003.1)
21. Gomagano, D. & Kohda, M. 2008 Partial filial cannibalism enhances initial body condition and size in paternal care fish with strong male-male competition. Ann. Zool. Fenn. 45, 55-65.
22. Gray, S. M., Dill, L. M. & McKinnon, J. S. 2007 Cuckoldry incites cannibalism: male fish turn to cannibalism when perceived certainty of paternity decreases. Am. Nat. 169, 258-263. (doi:10.1086/510604) (Pubitemid 46184978)
23. Green, W. W., Mirza, R. S. & Pyle, G. G. 2008 Kin recognition and cannibalistic behaviours by adult male fathead minnows (Pimephales promelas). Naturwissenschaften 95, 269-272. (doi:10.1007/s00114-007-0319-y)
24. Griffith, S. C., Owens, I. P. F. & Thuman, K. A. 2002 Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 11, 2195-2212. (doi:10.1046/j.1365-294X.2002.01613.x) (Pubitemid 35301894)
25. Heckel, G., Zbinden, M., Mazzi, D., Kohler, A., Reckeweg, G., Bakker, T. C. M. & Largiadèr, C. R. 2002 Microsatel-lite markers for the three-spined stickleback (Gasterosteus aculeatus L.) and their applicability in a freshwater and an anadromous population. Conserv. Genet. 3, 79-81.
26. Huang, W. S. 2008 Predation risk of whole-clutch filial cannibalism in a tropical skink with maternal care. Behav. Ecol. 19, 1069-1074. (doi:10.1093/beheco/arn109)
27. Jamieson, I. G. & Colgan, P. W. 1992 Sneak spawning and egg stealing by male threespine sticklebacks. Can. J. Zool. 70, 963-967. (doi:10.1139/z92- 137)
28. Kamler, E., Keckeis, H. & Bauer-Nemeschkal, E. 1998 Temperature-induced changes of survival, development and yolk partitioning in Chondrostoma nasus. J. Fish Biol. 53, 658-682. (doi:10.1111/j.1095-8649.1998. tb01009.x)
29. Klug, H. & Bonsall, M. B. 2007 When to care for, abandon, or eat your offspring: the evolution of parental care and filial cannibalism. Am. Nat. 170, 886-901. (doi:10. 1086/522936) (Pubitemid 350211438)
30. Kraak, S. B. M. & Bakker, T. C. M. 1998 Mutual mate choice in sticklebacks: attractive males choose big females, which lay big eggs. Anim. Behav. 56, 859-866. (doi:10. 1006/anbe.1998.0822)
31. Kraak, S. B. M., Bakker, T. C. M. & Mundwiler, B. 1997 How to quantify embryo survival in nest-building fishes, exemplified with three-spined sticklebacks. J. Fish Biol. 51, 1262-1264. (doi:10.1111/j.1095-8649.1997. tb01141.x)
32. Kraak, S. B. M., Bakker, T. C. M. & Mundwiler, B. 1999a Correlates of the duration of the egg collecting phase in the three-spined stickleback. J. Fish Biol. 54, 1038-1049. (doi:10.1111/j.1095-8649.1999.tb00856.x)
33. Kraak, S. B. M., Bakker, T. C. M. & Mundwiler, B. 1999b Sexual selection in sticklebacks in the field: correlates of reproductive, mating, and paternal success. Behav. Ecol. 10, 696-706. (doi:10.1093/beheco/10.6.696)
34. Kvarnemo, C., Svensson, O. & Forsgren, E. 1998 Parental behaviour in relation to food availability in the common goby. Anim. Behav. 56, 1285-1290. (doi:10.1006/anbe. 1998.0899) (Pubitemid 28548072)
35. Kynard, B. E. 1978 Breeding behavior of a lacustrine population of threespine sticklebacks (Gasterosteus aculeatus L.). Behaviour 67, 178-207. (doi:10.1163/ 156853978X00323)
36. Largiadèr, C. R., Fries, V. & Bakker, T. C. M. 2001 Genetic analysis of sneaking and egg-thievery in a natural population of the three-spined stickleback (Gasterosteus aculeatus L.). Heredity 86, 459-468. (doi:10.1046/j. 1365-2540.2001.00850.x) (Pubitemid 32745307)
37. Larson, G. L. 1976 Social behavior and feeding ability of two phenotypes of Gasterosteus aculeatus in relation to their spatial and trophic segregation in a temperate lake. Can. J. Zool. 54, 107-121. (doi:10.1139/z76-012)
38. Lavery, R. J. & Keenleyside, M. H. A. 1990 Parental investment of a biparental cichlid fish, Cichlasoma nigrofasciatum, in relation to brood size and past investment. Anim. Behav. 40, 1128-1137. (doi:10.1016/ S0003-3472(05)80179-4)
39. Le Comber, S. C., Faulkes, C. G., Formosinho, J. & Smith, C. 2003 Response of territorial males to the threat of sneaking in the three-spined stickleback (Gasterosteus aculeatus): a field study. J. Zool. 261, 15-20. (doi:10. 1017/S0952836903003911)
40. Lindström, K. & Sargent, R. C. 1997 Food access, brood size and filial cannibalism in the fantail darter, Etheostoma flabellare. Behav. Ecol. Sociobiol. 40, 107-110. (doi:10. 1007/s002650050322)
41. Lissa°ker, M. & Svensson, O. 2008 Cannibalize or care? The role of perceived paternity in the sand goby, Pomatoschistus minutus. Behav. Ecol. Sociobiol. 62, 1467-1475. (doi:10. 1007/s00265-008-0576-6)
42. Manica, A. 2002 Filial cannibalism in teleost fish. Biol. Rev. 77, 261-277. (doi:10.1017/S1464793101005905)
43. Manica, A. 2004 Parental fish change their cannibalistic behaviour in response to the cost-to-benefit ratio of parental care. Anim. Behav. 67, 1015-1021. (doi:10.1016/j.anbe-hav.2003.09.011)
44. Marconato, A., Bisazza, A. & Fabris, M. 1993 The cost of parental care and egg cannibalism in the river bullhead Cottus gobio L. (Pisces, Cottidae). Behav. Ecol. Sociobiol. 32, 229-237. (doi:10.1007/BF00166512)
45. Mehlis, M., Bakker, T. C. M. & Frommen, J. G. 2008 Smells like sib spirit: kin recognition in three-spined sticklebacks (Gasterosteus aculeatus) is mediated by olfactory cues. Anim. Cogn. 11, 643-650. (doi:10.1007/s10071-008- 0154-3)
46. Mehlis, M., Bakker, T. C. M. & Frommen, J. G. 2009 Nutritional benefits of filial cannibalism in three-spined sticklebacks (Gasterosteus aculeatus). Naturwissenschaften 96, 399-403. (doi:10.1007/s00114-008-0485-6)
47. Neff, B. D. 2003 Decisions about parental care in response to perceived paternity. Nature 422, 716-719. (doi:10.1038/ nature01528)
48. Ochi, H. 1985 Termination of parental care due to small clutch size in the temperate damselfish, Chromis notata. Environ. Biol. Fishes 12, 155-160. (doi:10.1007/ BF00002768)
49. Okuda, N. & Yanagisawa, Y. 1996 Filial cannibalism in a paternal mouthbrooding fish in relation to mate availability. Anim. Behav. 52, 307-314. (doi:10.1006/anbe. 1996.0176)
50. Petersen, C. W. & Hess, H. C. 1991 The adaptive significance of spawning synchronization in the Caribbean damselfish Stegastes dorsopunicans (Poey). J. Exp. Mar. Biol. Ecol. 151, 155-167. (doi:10.1016/0022-0981(91) 90122-D)
51. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & The R Core Team. 2009 nlme: linear and nonlinear mixed effects models, R package version 3.1-92.
52. Polis, G. A. 1981 The evolution and dynamics of intraspeci-fic predation. Annu. Rev. Ecol. Syst. 12, 225-251. (doi:10. 1146/annurev.es.12.110181.001301)
53. Reebs, S. G., Whoriskey, F. G. & FitzGerald, G. J. 1984 Diel patterns of fanning activity, egg respiration, and the nocturnal behavior of male threespined sticklebacks, Gasterosteus aculeatus L. Can. J. Zool. 62, 329-334. (doi:10.1139/z84-051)
54. Rios-Cardenas, O. & Webster, M. S. 2005 Paternity and paternal effort in the pumpkin seed sunfish. Behav. Ecol. 16, 914-921. (doi:10.1093/beheco/ ari076) (Pubitemid 41191531)
55. Rohwer, S. 1978 Parent cannibalism of offspring and egg raiding as a courtship strategy. Am. Nat. 112, 429-439. (doi:10.1086/283284)
56. Sargent, R. C. 1985 Territoriality and reproductive tradeoffs in the threespine stickleback, Gasterosteus aculeatus. Behaviour 93, 217-226. (doi:10.1163/156853986X00892)
57. Sargent, R. C. 1989 Allopaternal care in the fathead minnow, Pimephales promelas: stepfathers discriminate against their adopted eggs. Behav. Ecol. Sociobiol. 25, 379-385. (doi:10.1007/BF00300183)
58. Sargent, R. C. 1992 Ecology of filial cannibalism in fish: theoretical perspective. In Cannibalism: ecology and evolution among diverse taxa (eds M. A. Elgar & B. J. Crespi), pp. 38-62. Oxford, UK: Oxford University Press.
59. Sargent, R. C. & Gebler, J. B. 1980 Effects of nest site concealment on hatching success, reproductive success, and paternal behavior of the threespine stickleback, Gasteros-teus aculeatus. Behav. Ecol. Sociobiol. 7, 137-142. (doi:10.1007/BF00299519)
60. Schwank, E. J. 1986 Filial cannibalism in Tilapia mariae. J. Appl. Ichthyol. 2, 56-74. (doi:10.1111/j.1439-0426.1986.tb00431.x)
61. Smith, C. & Reay, P. 1991 Cannibalism in teleost fish. Rev. Fish Biol. Fish. 1, 41-64. (doi:10.1007/BF00042661)
62. Smith, C. & Wootton, R. J. 1999 Parental energy expenditure of the male three-spined stickleback. J. Fish Biol. 54, 1132-1136. (doi:10.1111/j.1095- 8649.1999.tb00866.x)
63. Svensson, O. & Kvarnemo, C. 2007 Parasitic spawning in sand gobies: an experimental assessment of nest-opening size, sneaker male cues, paternity, and filial cannibalism. Behav. Ecol. 18, 410-419. (doi:10.1093/beheco/arl098) (Pubitemid 46363265)
64. Taborsky, M. 1994 Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Adv. Study Behav. 23, 1-100. (doi:10.1016/S0065-3454(08) 60351-4)
65. Thomas, L. K. & Manica, A. 2003 Filial cannibalism in an assassin bug. Anim. Behav. 66, 205-210. (doi:10.1006/anbe.2003.2202) (Pubitemid 36990303)
66. Trivers, R. L. 1972 Parental investment and sexual selection. In Sexual selection and the descent of man, 1871-1971 (ed. B. Campbell), pp. 136-179. Chicago, IL: Aldine.
67. Van den Assem, J. 1967 Territory in the three-spined stickleback Gasterosteus aculeatus L. An experimental study in intra-specific competition. Behaviour Suppl. 16, 1-164.
68. Van Iersel, J. J. A. 1953 An analysis of the parental behaviour of the male three-spined stickleback (Gasterosteus aculeatus L.). Behaviour Suppl. 3, 1-159.
69. Wootton, R. J. 1976 The biology of the sticklebacks. London, UK: Academic Press.
70. Xia, X. H. 1992 Uncertainty of paternity can select against paternal care. Am. Nat. 139, 1126-1129. (doi:10.1086/285377)