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Determinate growth in a paternal mouthbrooding fish whose reproductive success is limited by buccal capacity

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Abstract

The life history of the paternal mouthbrooding cardinal fish Apogon doederleini was investigated in the temperate waters of Japan, with particular reference to its growth and reproductive rate. Both males and females almost ceased to grow at age 3 years, although living to 7 years of age. Their growth pattern, represented by the relative size at sexual maturity to the asymptotic size and the von Bertalanffy growth coefficient, was among the most determinate in ectothermic vertebrates. Brood size just before hatching increased in proportion to the second power of the body size of the brooding male, and correlated more positively with the male's than the female's body size, suggesting that it was limited by the male's buccal capacity. The estimated total number of broods hatched in a breeding season showed a weak or no correlation with the body size or age in either sex. Using life-history parameters based on data of A. doederleini, a simulation model of energy allocation without considering sexual interaction revealed that the optimal growth pattern shows an indeterminate growth that differs greatly from the actual growth pattern of A. doederleini. This suggests that there are some brooding constraints to size-advantage of reproductive success in this species. The possible mechanism of such reproductive constraint is discussed.

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References

  • Ahnesjö, I. (1992) Consequences of male brood care: Weight and number of newborn in a sex-role reversed pipefish. Funct. Ecol. 6, 274–281.

    Google Scholar 

  • Barger, L.E. (1985) Age and growth of Atlantic croakers in the northern Gulf of Mexico, based on otolith sections. Trans. Am. Fish. Soc. 114, 847–850.

    Google Scholar 

  • Berglund, A., Rosenqvist, G. and Svensson, I. (1989) Reproductive success of females limited by males in two pipefish species. Am. Nat. 133, 506–516.

    Google Scholar 

  • Beverton, R.J.H. and Holt, S.J. (1959) A review of the lifespans and mortality rates of fish in nature and the relation to growth and other physiological characteristics. In CIBA Foundation Colloquia on Aging: The Lifespan of Animals, pp. 142–177. Churchill, London.

  • Blueweiss, L., Fox, H., Kudzma, V., Nakashima, D., Peters, R. and Sams, S. (1978) Relationships between body size and some life history parameters. Oecologia 37, 257–272.

    Google Scholar 

  • Blumer, L.S. (1979) Male parental care in the bony fishes. Quart. Rev. Biol. 54, 149–161.

    Article  Google Scholar 

  • Blumer, L.S. (1982) A bibliography and categorization of bony fishes exhibiting parental care. Zool. J. Linn. Soc. 76, 1–22.

    Google Scholar 

  • Branstetter, S. (1987a) Age and growth validation of newborn sharks held in laboratory aquaria, with comments on the life history of the Atlantic sharpnose shark, Rhizoprionodon terraenovae. Copeia 2, 291–300.

    Google Scholar 

  • Branstetter, S. (1987b) Age, growth and reproductive biology of the silky shark, Carcharhinus falciformis, and the scalloped hammerhead, Sphyrna lewini, from the northwestern Gulf of Mexico. Env. Biol. Fish. 19, 161–173.

    Google Scholar 

  • Casey, J.G., Pratt, H.L., Jr. and Stillwell, C.E. (1985) Age and growth of the sandbar shark (Carcharhinus plumbeus) from the western North Atlantic. Can. J. Fish. Aquat. Sci. 42, 963–975.

    Google Scholar 

  • Chisnall, B.L. (1989) Age, growth, and condition of freshwater eels (Anguilla sp.) in backwaters of the lower Waikato River, New Zealand. N.Z. J. Mar. Freshwat. Res. 23, 459–465.

    Google Scholar 

  • Clutton-Brock, T.H. (1991) The Evolution of Parental Care. Princeton University Press, Oxford.

    Google Scholar 

  • Clutton-Brock, T.H. and Vincent, A.C.J. (1991) Sexual selection and the potential reproductive rates of males and females. Nature 351, 58–60.

    PubMed  Google Scholar 

  • Daniels, R.A. (1987) Comparative life histories and microhabitat use in three sympatric sculpins (Cottidae: Cottus) in northeastern California. Env. Biol. Fish. 19, 93–110.

    Google Scholar 

  • Dee, A.J. and Radtke, R.L. (1989) Age and growth of the brick soldierfish, Myripristis amaena. Coral Reefs 8, 79–85.

    Google Scholar 

  • DeMartini, E.E. and Anderson, M.E. (1980) Comparative survivorship and life history of painted greenling (Oxylebius pictus) in Puget Sound, Washington and Monterey Bay, California. Env. Biol. Fish. 5, 33–47.

    Google Scholar 

  • Demestre, M., Molí, B., Recasens, L. and Sánchez, P. (1993) Life history and fishery of Lepidopus caudatus (Pisces: Trichiuridae) in the Catalan Sea (northwestern Mediterranean). Mar. Biol. 115, 23–32.

    Google Scholar 

  • Dijkstra, C., Bult, A., Bijlsma, S., Daan, S., Meijer, T. and Zijlstra, M. (1990) Brood size manipulations in the kestrel (Falco tinnunculus): Effects on o.spring and parent survival. J. Anim. Ecol. 59, 269–285.

    Google Scholar 

  • Dygert, P.H. (1990) Seasonal changes in energy content and proximate composition associated with somatic growth and reproduction in a representative age-class of female English sole. Trans. Am. Fish. Soc. 119, 791–801.

    Google Scholar 

  • Ferreira, B.P. and Russ, G.R. (1992) Age, growth and mortality of the inshore coral trout Plectropomus maculatus (Pisces: Serranidae) from the central Great Barrier Reef, Australia. Aust. J. Mar. Freshwat. Res. 43, 429–440.

    Google Scholar 

  • Ford, N.B. and Seigel, R.A. (1989) Relationships among body size, clutch size, and egg size in three species of oviparous snakes. Herpetologica 45, 75–83.

    Google Scholar 

  • Fowler, A.J. (1991) Reproductive biology of bisexual and all-female populations of chaetodontid fishes from the southern Great Barrier Reef. Env. Biol. Fish. 31, 261–274.

    Google Scholar 

  • Fowler, A.J. and Doherty, P.J. (1992) Validation of annual growth increments in the otoliths of two species of damselfish from the southern Great Barrier Reef. Aust. J. Mar. Freshwat. Res. 43, 185–196.

    Google Scholar 

  • Gibbons, J.W., Greene, J.L. and Patterson, K.K. (1982) Variation in reproductive characteristics of aquatic turtles. Copeia 4, 776–784.

    Google Scholar 

  • Gross, M.R. and Sargent, R.C. (1985) The evolution of male and female parental care in fishes. Am. Zool. 25, 807–822.

    Google Scholar 

  • Gross, M.R. and Shine, R. (1981) Parental care and mode of fertilization in ectothermic vertebrates. Evolution 35, 775–793.

    Google Scholar 

  • Haldorson, L. and Craig, P. (1984) Life history and ecology of a Pacific-Arctic population of rainbow smelt in coastal waters of the Beaufort Sea. Trans. Am. Fish. Soc. 113, 33–38.

    Google Scholar 

  • Hill, K.T. and Radtke, R.L. (1988) Gerontological studies of the damselfish, Dascyllus albisella. Bull. Mar. Sci. 42, 424–434.

    Google Scholar 

  • Johnson, A.G. (1983) Age and growth of yellowtail snapper from south Florida. Trans. Am. Fish. Soc. 112, 173–177.

    Google Scholar 

  • Ketchen, K.S. (1975) Age and growth of dogfish Squalus acanthias in British Columbia waters. J. Fish. Res. Board Can. 32, 43–59.

    Google Scholar 

  • Kozlowski, J. and Uchmanski, J. (1987) Optimal individual growth and reproduction in perennial species with indeterminate growth. Evol. Ecol. 1, 214–230.

    Google Scholar 

  • Kusher, D.I., Smith, S.E. and Cailliet, G.M. (1992) Validated age and growth of the leopard shark, Triakis semifasciata, with comments on reproduction. Env. Biol. Fish. 35, 187–203.

    Google Scholar 

  • Kuwamura, T. (1983) Change of habitat and spacing pattern in the life histories of the cardinalfishes Apogon spp. at Shirahama, Japan. Nankiseibutsu 25, 13–18 (in Japanese).

    Google Scholar 

  • Kuwamura, T. (1985) Social and reproductive behavior of three mouthbrooding cardinalfishes, Apogon doederleini, A. niger and A. notatus. Env. Biol. Fish. 13, 17–24.

    Google Scholar 

  • Lack, D. (1954) The Natural Regulation of Animal Numbers. Clarendon Press, Oxford.

    Google Scholar 

  • Lemen, C.A. and Voris, H.K. (1981) A comparison of reproductive strategies among marine snakes. J. Anim. Ecol. 50, 89–101.

    Google Scholar 

  • Mann, R.H.K. (1973) Observations on the age, growth, reproduction and food of the roach Rutilus rutilus (L.) in two rivers in southern England. J. Fish Biol. 5, 707–736.

    Google Scholar 

  • Mann, R.H.K. (1974) Observations on the age, growth, reproduction and food of the dace, Leuciscus leuciscus (L.), in two rivers in southern England. J. Fish Biol. 6, 237–253.

    Google Scholar 

  • Mann, R.H.K. (1976) Observations on the age, growth, reproduction and food of the pike Esox lucius (L.) in two rivers in southern England. J. Fish Biol. 8, 179–197.

    Google Scholar 

  • Morales-Nin, B. and Ralston, S. (1990) Age and growth of Lutjanus kasmira (Forskål) in Hawaiian waters. J. Fish Biol. 36, 191–203.

    Google Scholar 

  • Nakashima, B.S. and Leggett, W.C. (1975) Yellow perch (Perca flavescens) biomass responses to different levels of phytoplankton and benthic biomass in Lake Memphremagog, Quebec-Vermont. J. Fish. Res. Board Can. 32, 1785–1797.

    Google Scholar 

  • Noltie, D.B. (1988) Comparative growth and condition of northern stream-dwelling rock bass, Ambloplites rupestris (Rafinesque). Hydrobiologia 160, 199–206.

    Google Scholar 

  • Okuda, N. and Yanagisawa, Y. (1996a) Filial cannibalism in a paternal mouthbrooding fish in relation to mate availability. Anim. Behav. 52, 307–314.

    Google Scholar 

  • Okuda, N. and Yanagisawa, Y. (1996b) Filial cannibalism by mouthbrooding males of the cardinal fish, Apogon doederleini, in relation to their physical condition. Env. Biol. Fish. 45, 397–404.

    Google Scholar 

  • Petersen, C.W. and Marchetti, K. (1989) Filial cannibalism in the cortez damselfish Stegastes rectifraenum. Evolution 43, 158–168.

    Google Scholar 

  • Pratt, H.L., Jr. and Casey, J.G. (1983) Age and growth of the shortfin mako, Isurus oxyrinchus, using four methods. Can. J. Fish. Aquat. Sci. 40, 1944–1957.

    Google Scholar 

  • Radtke, R.L., Fine, M.L. and Bell, J. (1985) Somatic and otolith growth in the oyster toadfish (Opsanus tau L.). J. Exp. Mar. Biol. Ecol. 90, 259–275.

    Google Scholar 

  • Ricker, W.E. (1979) Growth rates and models. In Fish Physiology (W.S. Hoar, D.J. Randall and J.R. Brett, eds), pp. 677–743. Academic Press, London.

    Google Scholar 

  • Ricklefs, R.E. (1968) Patterns of growth in birds. Ibis 110, 419–451.

    Google Scholar 

  • Rincon, P.A. and Lobon-Cervia, J. (1989) Reproductive and growth strategies of the red roach, Rutilus arcasii (Steindachner, 1866), in two contrasting tributaries of the River Duero, Spain. J. Fish Biol. 34, 687–705.

    Google Scholar 

  • Roff, D.A. (1984) The evolution of life history parameters in teleosts. Can. J. Fish. Aquat. Sci. 41, 989–1000.

    Google Scholar 

  • Roff, D.A. (1992) The Evolution of Life Histories. Chapman & Hall, New York.

    Google Scholar 

  • Satoh, K., Yamaoka, K. and Taniguchi, N. (1993) Distribution pattern and sampling efficiency of Gammaridea in Murote Bay. Bull. Mar. Sci. Fish., Kochi Univ. 13, 1–10 (in Japanese).

    Google Scholar 

  • Schmitt, D.N. and Hubert, W.A. (1983) Growth and condition factors of yellow perch in the Okoboji Lakes, Iowa. Iowa State J. Res. 57, 233–243.

    Google Scholar 

  • Shine, R. (1988) Parental care in reptiles. In Biology of the Reptilia (C. Gans, ed.), pp. 276–329. Alan R. Liss, New York.

    Google Scholar 

  • Shine, R. and Charnov, E.L. (1992) Patterns of survival, growth, and maturation in snakes and lizards. Am. Nat. 139, 1257–1269.

    Google Scholar 

  • Suzuki, K. and Ueno, S. (1983) Life history of the cardinalfish, Apogon cyanosoma, in Suruga Bay, central Japan. Bull. Inst. Ocean. Res. Develop., Tokai Univ. 5, 49–55 (in Japanese).

    Google Scholar 

  • Suzuki, K. and Ueno, S. (1987) Life history of the cardinalfish, Apogon semilineatus, in Suruga Bay, central Japan. J. Fac. Mar. Sci. Technol., Tokai Univ. 24, 121–131 (in Japanese).

    Google Scholar 

  • Suzuki, T., Ouchi, K. and Ikehara, K. (1978) On the determination of the age and growth of Sebastes thompsoni (Jordan et Hubbs). Bull. Japan Sea Reg. Fish. Res. Lab., Fish. Agency 29, 111–119 (in Japanese).

    Google Scholar 

  • Tilley, S.G. (1968) Size-fecundity relationships and their evolutionary implications in five desmognathine salamanders. Evolution 22, 806–816.

    Google Scholar 

  • Ueno, S., Suzuki, K. and Funao, T. (1987) Life history of the cardinalfish, Apogon notatus, in Suruga Bay, central Japan. J. Fac. Mar. Sci. Technol., Tokai Univ. 24, 111–119 (in Japanese).

    Google Scholar 

  • Wassef, E.A. (1991) Comparative growth studies on Lethrinus lentjan, Lacépède 1802 and Lethrinus mahsena, Forsskål 1775 (Pisces, Lethrinidae) in the Red Sea. Fish. Res. 11, 75–92.

    Google Scholar 

  • Wilson, C.A., Dean, J.M. and Radtke, R. (1982) Age, growth rate and feeding habits of the oyster toadfish, Opsanus tau (Linnaeus) in South Carolina. J. Exp. Mar. Biol. Ecol. 62, 251–259.

    Google Scholar 

  • Wootton, R.J. (1979) Energy costs of egg production and environmental determinants of fecundity in teleost fishes. Symp. Zool. Soc. Lond. 44, 133–159.

    Google Scholar 

  • Wootton, R.J. (1991) Ecology of Teleost Fishes. Chapman & Hall, London.

    Google Scholar 

  • Yokogawa, K. and Iguchi, M. (1992) Food habit and maturation of marbled rockfish, Sebastiscus marmoratus in southern coastal waters of the Harima Sea. Suisanzoshoku 40, 131–137 (in Japanese).

    Google Scholar 

  • Yokogawa, K., Iguchi, M. and Yamaga, K. (1992) Age, growth and condition factor of marbled rockfish, Sebastiscus marmoratus in southern coastal waters of the Harima Sea. Suisanzoshoku 40, 227–234 (in Japanese).

    Google Scholar 

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Authors and Affiliations

  1. Center for Ecological Research, Kyoto University, Otsu, 520-0105, Japan

    Noboru Okuda & Ichiro Tayasu

  2. Department of Biology, Ehime University, 2-5 Bunkyo-cho, Matsuyama, Ehime, 790-8577, Japan

    Yasunobu Yanagisawa

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  1. Noboru Okuda
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  2. Ichiro Tayasu
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Okuda, N., Tayasu, I. & Yanagisawa, Y. Determinate growth in a paternal mouthbrooding fish whose reproductive success is limited by buccal capacity. Evolutionary Ecology 12, 681–699 (1998). https://doi.org/10.1023/A:1006533531952

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