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Operational sex ratio and alternative reproductive behaviours in the European bitterling, Rhodeus sericeus

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Abstract

We investigated the effects of male population density and male-biased operational sex ratio (OSR) with constant and limited resource density on male mating tactics shown by a freshwater fish, the European bitterling, Rhodeus sericeus. This species spawns inside living unionid mussels. Large males defended territories and were aggressive towards conspecifics under equal sex ratios. They also monopolised pair spawnings with females, releasing 98% of all sperm clouds during mating. However, the mating tactic changed at high male density where large males ceased to be territorial and instead competed with groups of smaller males to release sperm when females spawned. Large, medium and small males now obtained 61%, 33%, and 6% of sperm releases respectively, thereby reducing the opportunity for sexual selection by half. Females spawned at equal rates in the two densities of males, despite lower courtship at high density. These results run counter to the usual expectation that an increasingly male-biased OSR should lead to higher variance in male mating success. Instead, the use of alternative reproductive behaviours by males can lead to lower resource competition and mating variance at high male densities.

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References

  • Aldridge DC (1999) Development of European bitterling in the gills of freshwater mussels. J Fish Biol 54:138–151

    Article  Google Scholar 

  • Ahnesjö I, Kvarnemo C, Merilaita S (2001) Using potential reproductive rates to predict mating competition among individuals qualified to mate. Behav Ecol 12:397–401

    Article  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, New Jersey

  • Arnold SJ, Wade MJ (1984) On measurement of natural and sexual selection: theory. Evolution 38:709–719

    Google Scholar 

  • Balshine-Earn S (1996) Reproductive rates, operational sex ratios and mate choice in St Peter's fish. Behav Ecol Sociobiol 39:107–116

    Article  Google Scholar 

  • Brown JL (1964) The evolution of diversity in avian territorial systems. Wilson Bull 76:160–169

    Google Scholar 

  • Cade WH, Cade ES (1992) Male mating success, calling and searching behaviour at high and low densities in the field cricket, Gryllus integer. Anim Behav 43:49–56

    Google Scholar 

  • Candolin U, Reynolds JD (2001) Sexual signaling in the European bitterling: females learn the truth by inspecting the resource. Behav Ecol 12:407–411

    Article  Google Scholar 

  • Candolin U, Reynolds JD (2002a) Adjustments of ejaculation rates in response to risk of sperm competition in a fish, the bitterling (Rhodeus sericeus). Proc R Soc Lond B 269:1459–1553

    Google Scholar 

  • Candolin U, Reynolds JD (2002b) Why do males tolerate sneakers? Tests with the European bitterling, Rhodeus sericeus. Behav Ecol 51:146–152

    Article  Google Scholar 

  • Chapman MR, Kramer DL (1996) Guarded resources: the effect of intruder number on the tactics and success of defenders and intruders. Anim Behav 52:83–94

    Article  Google Scholar 

  • Clutton-Brock TH, Parker GA (1992) Potential reproductive rates and the operation of sexual selection. Q Rev Biol 67:437–456

    Google Scholar 

  • Clutton-Brock TH, Vincent ACJ (1991) Sexual selection and the potential reproductive rates of males and females. Nature 351:58–60

    CAS  PubMed  Google Scholar 

  • Debuse VJ, Addison JT, Reynolds JD (1999) The effects of sex ratio on sexual competition in the European lobster. Anim Behav 58:973–981

    Article  PubMed  Google Scholar 

  • Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    CAS  PubMed  Google Scholar 

  • Evans JP, Magurran AE (2000) Multiple benefits of multiple mating in guppies. Proc Natl Acad Sci USA 97:10074–10076

    Google Scholar 

  • French BW, Cade WH (1989) Sexual selection at varying population densities in male field crickets Gryllus velevtus and G. pennsylvanicus. J Insect Behav 2:105–121

    Google Scholar 

  • Grant JWA (1993) Whether or not to defend? The influence of resource distribution. Mar Behav Physiol 23:137–153

    Google Scholar 

  • Grant JWA, Bryant MJ, Soos CE (1995) Operational sex-ratio, mediated by synchrony of female arrival, alters the variance of male mating success in Japanese medaka. Anim Behav 49:367–375

    Google Scholar 

  • Grant JWA, Gaboury CL, Levitt HL (2000) Competitor-to-resource ratio, a general formulation of operational sex ratio, as a predictor of competitive aggression in Japanese medaka (Pisces: Oryziidae). Behav Ecol 11:670–675

    Article  Google Scholar 

  • Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:A92-A98

    Google Scholar 

  • Jirotkul M (1999a) Operational sex ratio influences female preference and male-male competition in guppies. Anim Behav 58:287–294

    Article  PubMed  Google Scholar 

  • Jirotkul M (1999b) Population density influences male-male competition in guppies. Anim Behav 58:1169–1175

    PubMed  Google Scholar 

  • Kanoh Y (1996) Pre-oviposition ejaculation in externally fertilizing fish: how sneaker male rose bitterlings contrive to mate. Ethology 102:883–899

    Google Scholar 

  • Kanoh Y (2000) Reproductive success associated with territoriality, sneaking, and grouping in male rose bitterlings, Rhodeus ocellatus (Pisces : Cyprinidae). Environ Biol Fishes 57:143–154

    Article  Google Scholar 

  • Kokko H, Johnstone RA (2002) Why is mutual mate choice not the norm? Operational sex ratios, sex roles and the evolution of sexually dimorphic and monomorphic signalling. Philos Trans R Soc Lond B Biol Sci 357:319–330

    Article  PubMed  Google Scholar 

  • Kokko H, Monaghan P (2001) Predicting the direction of sexual selection. Ecol Lett 4:159–165

    Article  Google Scholar 

  • Kvarnemo C (1994) Temperature differentially affects male and female reproductive rates in the sand goby—consequences for operational sex-ratio. Proc R Soc Lond B Biol Sci 256:151–156

    Google Scholar 

  • Kvarnemo C (1996) Temperature affects operational sex ratio and intensity of male–male competition: experimental study of sand gobies, Pomatoschistus minutus. Behav Ecol 7:208–212

    Google Scholar 

  • Kvarnemo C, Ahnesjö I (1996) The dynamics of operational sex ratios and competition for mates. Trends Ecol Evol 11:404–408

    Article  Google Scholar 

  • Kvarnemo C, Forsgren E, Magnhagen C (1995) Effects of sex ratio on intra- and inter-sexual behaviour in sand gobies. Anim Behav 50:1455–1461

    Google Scholar 

  • Madsen T, Shine R (1993) Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes. Am Nat 141:167–171

    Article  Google Scholar 

  • McLain DK, Boromisa RD (1987) Male choice, fighting ability, assortative mating and the intensity of sexual selection in the milkweed longhorn beetle, Tetropes tertraphtalmus (Coleoptera, Cerambycidae). Behav Ecol Sociobiol 20:239–246

    Google Scholar 

  • Mills SC, Reynolds JD (2002a) Host species preferences by bitterling, Rhodeus sericeus, spawning in freshwater mussels and consequences for offspring survival. Anim Behav 63:1029–1036

    Article  Google Scholar 

  • Mills SC, Reynolds JD (2002b) Mussel ventilation rates as a proximate cue for host selection by bitterling, Rhodeus sericeus. Oecologia 131:473–478

    Article  Google Scholar 

  • Myers JP, Connors PG, Pitelka FA (1979) Territory size in wintering sanderlings: the effects of prey abundance and intruder density. Auk 96:551–561

    Google Scholar 

  • O'Donald P (1978) Theoretical aspects of sexual selection: a generalized model of mating behaviour. Theor Popul Biol 13:226–243

    PubMed  Google Scholar 

  • Oliveira RF, Almada VC, Forsgren E, Gonçalves EJ (1999) Temporal variation in male traits, nesting aggregations and mating success in the peacock blenny. J Fish Biol 54:499–512

    Article  Google Scholar 

  • Otronen M (1996) Effects of seasonal variation in operational sex ratio and population density on the mating success of different sized and aged males in the yellow dung fly, Scathophaga stercoraria. Ethol Ecol Evol 8:399–411

    Google Scholar 

  • Parker GA, Simmons LW (1996) Parental investment and the control of sexual selection: predicting the direction of sexual competition. Proc R Soc Lond B Biol Sci 263:315–321

    Google Scholar 

  • Reynolds JD (1996) Animal breeding systems. Trends Ecol Evol 11:A68-A72

    Google Scholar 

  • Reynolds JD, Guillaume HP (1998) Effects of phosphate on the reproductive symbiosis between bitterling and freshwater mussels: implications for conservation. J Appl Ecol 35:575–581

    CAS  Google Scholar 

  • Reynolds JD, Colwell MA, Cooke F (1986) Sexual selection and spring arrival times of red-necked and Wilson Phalaropes. Behav Ecol Sociobiol 18:303–310

    Google Scholar 

  • Reynolds JD, Debuse VJ, Aldridge DC (1997) Host specialisation in an unusual symbiosis: European bitterlings spawning in freshwater mussels. Oikos 78:539–545

    Google Scholar 

  • Smith C, Reynolds JD, Sutherland WJ (2000a) Population consequences of reproductive decisions. Proc R Soc Lond B Biol Sci 267:1327–1334

    Article  PubMed  Google Scholar 

  • Smith C, Reynolds JD, Sutherland WJ (2000b) Adaptive host choice and avoidance of superparasitism in the spawning decisions of bitterling (Rhodeus sericeus). Behav Ecol Sociobiol 48:29–3

    Article  Google Scholar 

  • Taborsky M (1998) Sperm competition in fish: 'bourgeois' males and parasitic spawning. Trends Ecol Evol 13:222–227

    Article  Google Scholar 

  • Venkataraman AB (1998) Male-biased adult sex ratios and their significance for cooperative breeding in dhole, Cuon alpinus, packs. Ethology 104:671–684

    Google Scholar 

  • Warner RR, Hoffman SG (1980) Population density and the economics of territorial defense in a coral reef fish. Ecology 61:772–780

    Google Scholar 

  • Wiepkema PR (1961) An ethological analysis of the reproductive behaviour of the bitterling (Rhodeus amarus Bloch). Arch Neerl Zool 14:103–199

    Google Scholar 

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Acknowledgements

We thank Chris Wiskin and Thierry Fredou for their invaluable help with fieldwork and data collection; Mark Abrahams, Ulrika Candolin, Steve Emlen, Matt Gage, Jim Grant, Jo Ridley and two anonymous referees for useful comments on the manuscript; Martin Perrow and Mark Tomlinson for help with the fieldwork; and Geoff Eagles and Paul Cooke for laboratory support. We also thank the John and Pamela Salter Charitable Trust for help with funding. This research was supported by a studentship from the Natural Environment Research Council to S.C. Mills. The experiments comply with the current laws of the country in which they were performed.

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  1. Suzanne C. Mills

    Present address: Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35 YAC, 40041, Jyväskylä, Finland

Authors and Affiliations

  1. Centre for Ecology, Evolution and Conservation, School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK

    Suzanne C. Mills & John D. Reynolds

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  1. Suzanne C. Mills
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  2. John D. Reynolds
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Correspondence to Suzanne C. Mills.

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Communicated by M. Abrahams

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Mills, S.C., Reynolds, J.D. Operational sex ratio and alternative reproductive behaviours in the European bitterling, Rhodeus sericeus . Behav Ecol Sociobiol 54, 98–104 (2003). https://doi.org/10.1007/s00265-003-0616-1

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  • DOI: https://doi.org/10.1007/s00265-003-0616-1

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