Spatial variation in egg size and egg number reflects trade-offs and bet-hedging in a freshwater fish

Journal of Animal Ecology

Volumn 81, Issue 4, 2012, Pages 806-817

  Morrongiello, John R ^a,b,c   Bond, Nicholas R ^a,b,d   Crook, David A ^b,e,f   Wong, Bob B M ^a  

^a MONASH UNIVERSITY   (Australia)

^b EWATER COOPERATIVE RESEARCH CENTRE   (Australia)

^c CSIRO   (Australia)

^d GRIFFITH UNIVERSITY   (Australia)

^e ARTHUR RYLAH INSTITUTE FOR ENVIRONMENTAL RESEARCH   (Australia)

^f CHARLES DARWIN UNIVERSITY   (Australia)

Author keywords

Adaptive phenotypic plasticity; Environmental quality; Freshwater fish; Maternal effect; Optimal offspring size; Reproductive life history; Spatial bet hedging; Unpredictable environment

Indexed keywords

ADAPTATION; ANTHROPOGENIC EFFECT; BET-HEDGING; EGG PRODUCTION; EGG SIZE; ENVIRONMENTAL GRADIENT; ENVIRONMENTAL QUALITY; FECUNDITY; FRESHWATER ENVIRONMENT; LIFE HISTORY TRAIT; MATERNAL EFFECT; PARENTAL INVESTMENT; PERCIFORM; PHENOTYPIC PLASTICITY; SPATIAL VARIATION; TRADE-OFF;

ANIMAL; ARTICLE; AUSTRALIA; BIOLOGICAL MODEL; ENVIRONMENT; FEMALE; FERTILITY; GENETICS; OOCYTE; PERCIFORMES; PHYSIOLOGY; REPRODUCTION; REPRODUCTIVE FITNESS;

ANIMALS; ENVIRONMENT; FEMALE; FERTILITY; GENETIC FITNESS; MODELS, BIOLOGICAL; OVUM; PERCIFORMES; REPRODUCTION; VICTORIA;

ANIMALIA; NANNOPERCA AUSTRALIS;

EID: 84862704242     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/j.1365-2656.2012.01961.x     Document Type: Article

References (93)

1. Allen, R.M., Buckley, Y.M. & Marshall, D.J. (2008) Offspring size plasticity in response to intraspecific competition: an adaptive maternal effect across life-history stages. American Naturalist, 171, 225-237.
2. Arendt, J.D. & Reznick, D.N. (2005) Evolution of juvenile growth rates in female guppies (Poecilia reticulata): predator regime or resource level? Proceedings of the Royal Society B-Biological Sciences, 272, 333-337.
3. Bashey, F. (2008) Competition as a selective mechanism for larger offspring size in guppies. Oikos, 117, 104-113.
4. Beacham, T.D. & Murray, C.B. (1993) Fecundity and egg size variation in North American Pacific salmon (Oncorhynchus). Journal of Fish Biology, 42, 485-508.
5. van den Berghe, E.P. & Gross, M.R. (1989) Natural selection resulting from female breeding competition in a Pacific salmon (Coho: Oncorhynchus kisutch). Evolution, 43, 125-140.
6. Bernardo, J. (1996) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. American Zoologist, 36, 216-236.
7. Bond, N.R. & Lake, P.S. (2003) Characterizing fish-habitat associations in streams as the first step in ecological restoration. Austral Ecology, 28, 611-621.
8. Bond, N.R. & Lake, P.S. (2005) Ecological restoration and large-scale ecological disturbance: the effects of drought on the response by fish to a habitat restoration experiment. Restoration Ecology, 13, 39-48.
9. Bond, N.R., Lake, P.S. & Arthington, A.H. (2008) The impacts of drought on freshwater ecosystems: an Australian perspective. Hydrobiologia, 600, 3-16.
10. Bond, N., Thomson, J., Reich, P. & Stein, J.L. (2011) Using species distribution models to infer potential climate change-induced range shifts of freshwater fish in south-eastern Australia. Marine and Freshwater Research, 62, 1043-1061.
11. Boulton, A.J. & Lake, P.S. (1992) The ecology of 2 intermittent streams in Victoria, Australia 2. Comparisons of faunal composition between habitats, rivers and years. Freshwater Biology, 27, 99-121.
12. Brockelman, W.Y. (1975) Competition, fitness of offspring, and optimal clutch size. American Naturalist, 109, 677-699.
13. Burnham, K.P. & Anderson, D.R. (2002) Model Selection and Inference: a Practical Information-Theoretic Approach, 2nd edn. Springer-Verlag, New York, New York, USA.
14. Charnov, E.L. & Downhower, J.F. (1995) A trade-off-invariant life-history rule for optimal offspring size. Nature, 376, 418-419.
15. Childs, D.Z., Metcalf, C.J.E. & Rees, M. (2010) Evolutionary bet-hedging in the real world: empirical evidence and challenges revealed by plants. Proceedings of the Royal Society B-Biological Sciences, 277, 3055-3064.
16. Clarke, A., Mac Nally, R., Bond, N. & Lake, P.S. (2010) Flow permanence affects aquatic macroinvertebrate diversity and community structure in three headwater streams in a forested catchment. Canadian Journal of Fisheries and Aquatic Sciences, 67, 1649-1657.
17. Cohen, D. (1966) Optimizing reproduction in a randomly varying environment. Journal of Theoretical Biology, 12, 119-129.
18. Colwell, R.K. (1974) Predictability, constancy and contingency of periodic phenomena. Ecology, 55, 1148-1153.
19. Cook, B.D., Bunn, S.E. & Hughes, J.M. (2007) Molecular genetic and stable isotope signatures reveal complementary patterns of population connectivity in the regionally vulnerable southern pygmy perch (Nannoperca australis). Biological Conservation, 138, 60-72.
20. Crawley, M.J. (2007) The R Book, Wiley, Chichester, England.
21. Crean, A.J. & Marshall, D.J. (2009) Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Philosophical Transactions of the Royal Society B-Biological Sciences, 364, 1087-1096.
22. Dibattista, J.D., Feldheim, K.A., Gruber, S.H. & Hendry, A.P. (2007) When bigger is not better: selection against large size, high condition and fast growth in juvenile lemon sharks. Journal of Evolutionary Biology, 20, 201-212.
23. Dziminski, M.A., Vercoe, P.E. & Roberts, J.D. (2009) Variable offspring provisioning and fitness: a direct test in the field. Functional Ecology, 23, 164-171.
24. Ebert, D. (1994) Fractional resource allocation into few eggs: Daphnia as an example. Ecology, 75, 568-571.
25. Einum, S. & Fleming, I.A. (1999) Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality. Proceedings of the Royal Society B-Biological Sciences, 266, 2095-2100.
26. Einum, S. & Fleming, I.A. (2000) Highly fecund mothers sacrifice offspring survival to maximise fitness. Nature, 405, 565-567.
27. Einum, S. & Fleming, I.A. (2002) Does within-population variation in fish egg size reflect maternal influences on optimal values? American Naturalist, 160, 756-765.
28. Einum, S. & Fleming, I.A. (2004) Environmental unpredictability and offspring size: conservative versus diversified bet-hedging. Evolutionary Ecology Research, 6, 443-455.
29. Fischer, B., Taborsky, B. & Kokko, H. (2011) How to balance the offspring quality-quantity tradeoff when environmental cues are unreliable. Oikos, 120, 258-270.
30. Fleming, I.A. & Gross, M.R. (1990) Latitudinal clines- a trade-off between egg number and size in Pacific salmon. Ecology, 71, 1-11.
31. Forbes, L.S. (1991) Optimal size and number of offspring in a variable environment. Journal of Theoretical Biology, 150, 299-304.
32. Fox, C.W. & Czesak, M.E. (2000) Evolutionary ecology of progeny size in arthropods. Annual Review of Entomology, 45, 341-369.
33. Fox, C.W., Thakar, M.S. & Mousseau, T.A. (1997) Egg size plasticity in a seed beetle: an adaptive maternal effect. American Naturalist, 149, 149-163.
34. Guinnee, M.A., West, S.A. & Little, T.J. (2004) Testing small clutch size models with Daphnia. American Naturalist, 163, 880-887.
35. Hendry, A.P., Day, T. & Cooper, A.B. (2001) Optimal size and number of propagules: allowance for discrete stages and effects of maternal size on reproductive output and offspring fitness. American Naturalist, 157, 387-407.
36. Humphries, P. (1995) Life history, food and habitat of southern pygmy perch, Nannoperca australis, in the Macquarie River, Tasmania. Marine and Freshwater Research, 46, 1159-1169.
37. Jackson, D.A., Peres-Neto, P.R. & Olden, J.D. (2001) What controls who is where in freshwater fish communities - the roles of biotic, abiotic, and spatial factors. Canadian Journal of Fisheries and Aquatic Sciences, 58, 157-170.
38. Johnston, T.A. & Leggett, W.C. (2002) Maternal and environmental gradients in the egg size of an iteroparous fish. Ecology, 83, 1777-1791.
39. Kamel, S.J., Grosberg, R.K. & Marshall, D.J. (2010) Family conflicts in the sea. Trends in Ecology & Evolution, 25, 442-449.
40. Kaplan, R.H. (1992) Greater maternal investment can decrease offspring survival in the frog Bombina orientalis. Ecology, 73, 280-288.
41. Kaplan, R.H. & Cooper, W.S. (1984) The evolution of developmental plasticity in reproductive characteristics: an application of the "adaptive coin-flipping" principle. American Naturalist, 123, 393-410.
42. Kaplan, R.H. & King, E.G. (1997) Egg size is a developmentally plastic trait: evidence from long term studies in the frog Bombina orientalis. Herpetologica, 53, 149-165.
43. Kennard, M.J., Pusey, B.J., Olden, J.D., MacKay, S.J., Stein, J.L. & Marsh, N. (2010) Classification of natural flow regimes in Australia to support environmental flow management. Freshwater Biology, 55, 171-193.
44. Knight, J.T., Butler, G.L., Smith, P.S. & Wager, R.N.E. (2007) Reproductive biology of the endangered Oxleyan pygmy perch Nannoperca oxleyana Whitley. Journal of Fish Biology, 71, 1494-1511.
45. Koops, M.A., Hutchings, J.A. & Adams, B.K. (2003) Environmental predictability and the cost of imperfect information: influences on offspring size variability. Evolutionary Ecology Research, 5, 29-42.
46. Krug, P.J. (2009) Not my "type": larval dispersal dimorphisms and bet-hedging in opisthobranch life histories. Biological Bulletin, 216, 355-372.
47. Kudo, S.I. (2001) Intraclutch egg-size variation in acanthosomatid bugs: adaptive allocation of maternal investment? Oikos, 92, 208-214.
48. Lake, P.S. (1982) The relationships between freshwater fish distribution, stream drainage area and stream length in some streams of south-eastern Australia. Bulletin of the Australian Society for Limnology, 8, 31-37.
49. Lake, P.S. (2000) Disturbance, patchiness, and diversity in streams. Journal of the North American Benthological Society, 19, 573-592.
50. Lake, P.S. (2003) Ecological effects of perturbation by drought in flowing waters. Freshwater Biology, 48, 1161-1172.
51. Lalonde, R.G. (1991) Optimal offspring provisioning when resources are not predictable. American Naturalist, 138, 680-686.
52. Lips, K.R. (2001) Reproductive trade-offs and bet-hedging in Hyla calypsa, a neotropical treefrog. Oecologia, 128, 509-518.
53. Llewellyn, L.C. (1974) Spawning, development and distribution of the southern pigmy perch Nannoperca australis australis Günther from inland waters in eastern Australia. Australian Journal of Marine and Freshwater Research, 25, 121-149.
54. Lytle, D.A. & Poff, N.L. (2004) Adaptation to natural flow regimes. Trends in Ecology & Evolution, 19, 94-100.
55. Magoulick, D.D. & Kobza, R.M. (2003) The role of refugia for fishes during drought: a review and synthesis. Freshwater Biology, 48, 1186-1198.
56. Marsh, N.A., Stewardson, M.J. & Kennard, M.J. (2003) River Analysis Package. Cooperative Research Centre for Catchment Hydrology, Monash University, Melbourne.
57. Marshall, D.J., Bonduriansky, R. & Bussiere, L.F. (2008) Offspring size variation within broods as a bet-hedging strategy in unpredictable environments. Ecology, 89, 2506-2517.
58. Marshall, D.J. & Keough, M.J. (2008) The relationship between offspring size and performance in the sea. American Naturalist, 171, 214-224.
59. Marshall, D.J., Heppell, S.S., Munch, S.B. & Warner, R.R. (2010) The relationship between maternal phenotype and offspring quality: do older mothers really produce the best offspring? Ecology, 91, 2862-2873.
60. McGinley, M.A., Temme, D.H. & Geber, M.A. (1987) Parental investment in offspring in variable environments: theoretical and empirical considerations. American Naturalist, 130, 370-398.
61. McMaster, D. & Bond, N.R. (2008) A field and experimental study on the tolerances of fish to Eucalyptus camaldulensis leachate and low dissolved oxygen concentrations. Marine and Freshwater Research, 59, 177-185.
62. Mitchell, P.A. (1976) A Study of the Behaviour and Breeding Biology of the Southern Pigmy Perch Nannoperca Australis Australis (Günther) (Teleostei, Nannopercidae). B. Sc. (hons) Honours, University of Melbourne, Melbourne, Australia.
63. Moran, A.L. & Emlet, R.B. (2001) Offspring size and performance in variable environments: field studies on a marine snail. Ecology, 82, 1597-1612.
64. Morrongiello, J.R. (2011) Life History Variation along Environmental Gradients in a Freshwater Fish, the Southern Pygmy Perch Nannoperca australis. PhD thesis, Monash University, Melbourne.
65. Morrongiello, J.R., Bond, N.R., Crook, D.A. & Wong, B.B.M. (2011) Eucalyptus leachate inhibits reproduction in a freshwater fish. Freshwater Biology, 56, 1736-1745.
66. Naiman, R.J., Latterell, J.J., Pettit, N.E. & Olden, J.D. (2008) Flow variability and the biophysical vitality of river systems. Comptes Rendus Geoscience, 340, 629-643.
67. van Overveld, T. & Matthysen, E. (2010) Personality predicts spatial responses to food manipulations in free-ranging great tits (Parus major). Biology Letters, 6, 187-190.
68. Parker, G.A. & Begon, M. (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. American Naturalist, 128, 573-592.
69. Perry, G.L.W. & Bond, N.R. (2009) Spatially explicit modelling of habitat dynamics and fish population persistence in an intermittent lowland stream. Ecological Applications, 19, 731-746.
70. Poff, N.L. & Ward, J.V. (1989) Implications of streamflow variability and predictability for lotic community structure: a regional analysis of streamflow patterns. Canadian Journal of Fisheries and Aquatic Sciences, 46, 1805-1818.
71. Poff, N.L., Allan, J.D., Bain, M.B., Karr, J.R., Prestegaard, K.L., Richter, B.D., Sparks, R.E. & Stromberg, J.C. (1997) The natural flow regime. BioScience, 47, 769-784.
72. R Development Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
73. Rasanen, K., Soderman, F., Laurila, A. & Merila, J. (2008) Geographic variation in maternal investment: acidity affects egg size and fecundity in Rana arvalis. Ecology, 89, 2553-2562.
74. Reist, J.D. (1986) An empirical evaluation of coefficients used in residual and allometric adjustment of size covariation. Canadian Journal of Zoology-Revue Canadienne De Zoologie, 64, 1363-1368.
75. Reznick, D., Butler, M.J. & Rodd, H. (2001) Life-history evolution in guppies. VII. The comparative ecology of high- and low-predation environments. American Naturalist, 157, 126-140.
76. Reznick, D.N., Rodd, F.H. & Cardenas, M. (1996) Life-history evolution in guppies (Poecilia reticulata: Poeciliidae). IV. Parallelism in life-history phenotypes. American Naturalist, 147, 319-338.
77. Schlosser, I.J. (1987) A conceptual framework for fish communities in small warmwater streams. Community and Evolutionary Ecology of North American Stream Fishes (eds W.J. Matthews & D.C. Heins). pp. 17-24, University of Oklahoma Press, Norman, USA.
78. Schlosser, I.J. (1990) Environmental variation, life-history attributes, and community structure in stream fishes: implications for environmental management and assessment. Environmental Management, 14, 621-628.
79. Seger, J. & Brockmann, H.J. (1987) What is bet-hedging? Oxford Surveys in Evolutionary Biology, 4, 182-211.
80. Semmens, D. (2008) Maternal Effects on Offspring Fitness in an Australian Native Fish, Galaxias maculatus. PhD thesis, University of Melbourne, Melbourne, Australia.
81. Simons, A.M. (2011) Modes of response to environmental change and the elusive empirical evidence for bet hedging. Proceedings of the Royal Society B-Biological Sciences, 278, 1601-1609.
82. Smith, C.C. & Fretwell, S.D. (1974) The optimal balance between size and number of offspring. American Naturalist, 108, 499-506.
83. Stearns, S.C. (1992) The Evolution of Life Histories. Oxford University Press, London.
84. Tamate, T. & Maekawa, K. (2000) Interpopulation variation in reproductive traits of female masu salmon, Oncorhynchus masou. Oikos, 90, 209-218.
85. Teder, T., Tammaru, T. & Esperk, T. (2008) Dependence of phenotypic variance in body size on environmental quality. American Naturalist, 172, 223-232.
86. Tonkin, Z., King, A.J. & Mahoney, J. (2008) Effects of flooding on recruitment and dispersal of the southern pygmy perch (Nannoperca australis) at a Murray River floodplain wetland. Ecological Management & Restoration, 9, 196-201.
87. Tremblay, I., Thomas, D.W., Lambrechts, M.M., Blondel, J. & Perret, P. (2003) Variation in Blue Tit breeding performance across gradients in habitat richness. Ecology, 84, 3033-3043.
88. Vaughton, G. & Ramsey, M. (1998) Sources and consequences of seed mass variation in Banksia marginata (Proteaceae). Journal of Ecology, 86, 563-573.
89. Wellborn, G.A., Skelly, D.K. & Werner, E.E. (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annual Review of Ecology and Systematics, 27, 337-363.
90. Woodward, G.M.A. (2005) Factors Influencing the Distribution and Abundance of Nannoperca obscura (Yarra pygmy perch) and Nannoperca australis (Southern pygmy perch). PhD thesis, LaTrobe University, Melbourne.
91. Wootton, R.J. (1998) Ecology of Teleost Fishes. Kluwer Academic Publishers, London, UK.
92. Zovi, D., Stastny, M., Battisti, A. & Larsson, S. (2008) Ecological costs on local adaptation of an insect herbivore imposed by host plants and enemies. Ecology, 89, 1388-1398.
93. Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A. & Smith, G.M. (2009) Mixed Effects Models and Extensions in Ecology with R. Springer, New York, USA.