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Additions and amendments to the classification of reproductive styles in fishes

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The guild concept is explained to represent peaks in the landscape of reproductive styles, which respond to the ‘altricial ⇄ precocial principle’ caused by the processes of heterochrony and saltation. Guilds represent evolutionary trends but not units. New evidence for a specialization within the mouthbrooding external bearers is reviewed, e.g. the unique specialization of juvenile feeding inside the female's buccal cavity. Ability to withstand extreme environments is revealed in some water-edge spawners and a new guild of nonguarding aerophils is distinguished. The walleye is placed into another guild and the significance of spawning inside of sponges discussed. Due to a better understanding of reproductive styles used by some external bearers, termed earlier as forehead, skin and possibly armpit and backpack brooders, a single guild of auxiliary brooders is named. The classification of internal bearers is revised into four redefined and renamed guilds — facultative internal bearers, obligate lecithotrophic livebearers, matrotrophous oophages and adephophages, and viviparous trophoderms.

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References cited

  • Adams, P.B. 1980. Life history patterns in marine fishes and their consequences for fisheries management. U.S. Fish. Bull. 78: 1–12.

    Google Scholar 

  • Allen, G.R. 1975. The anemonefishes, their classification and biology. T.F.H. Publ., Neptune City. 352 pp.

    Google Scholar 

  • Amoroso, E.C. 1960. Viviparity in fishes. pp. 153–181. In: L.C. Jones (ed.) Hormones in Fish, Symp. Zool. Soc. London.

    Google Scholar 

  • Assheton, R. 1896. Notes on the ciliation of the ectoderm of the amphibian embryo. Quarterly J. Microscop. Sci. 38: 465–484.

    Google Scholar 

  • Atz, J.W. 1958. A mouthful of babies. Anim. Kingdom 6: 182–186.

    Google Scholar 

  • Balon, E.K. 1975a. Reproductive guilds of fishes: a proposal and definition. J. Fish. Res. Board Can. 32: 821–864.

    Google Scholar 

  • Balon, E.K. 1975b. Terminology of intervals in fish development. J. Fish. Res. Board Can. 32: 1663–1670.

    Google Scholar 

  • Balon, E.K. 1977. Early ontogeny ofLabeotropheus Ahl, 1927 (Mbuna, Cichlidae, Lake Malawi), with a discussion on advanced protective styles in fish reproduction and development. Env. Biol. Fish. 2: 147–176.

    Google Scholar 

  • Balon, E.K. 1978. Reproductive guilds and the ultimate structure of fish taxocenes: amended contribution to the discussion presented at the mini-symposium. Env. Biol. Fish. 3: 149–152.

    Google Scholar 

  • Balon, E.K. 1979a. The role of carotenoids in endogenous respiration of fish embryos. Abstracts of 59th Annual Meeting of American Society of Ichthyologists and Herpetologists, Orono.

  • Balon, E.K. 1979b. The theory of saltation and its application in the ontogeny of fishes: steps and thresholds. Env. Biol. Fish. 4: 97–101.

    Google Scholar 

  • Balon, E.K. 1979c. The juvenilization process in phylogeny and the altricial to precocial forms in the ontogeny of fishes. Env. Biol. Fish. 4: 193–198.

    Google Scholar 

  • Balon, E.K. (ed.) 1980. Charrs: salmonid fishes of the genusSalvelinus. Perspectives in Vertebrate Science 1, Dr. W. Junk Publishers. The Hague. 928 pp.

  • Balon, E. K. 1981a. About processes which cause the evolution of guilds and species. Env. Biol. Fish. 6: 129–138.

    Google Scholar 

  • Balon, E. K. 1981b. Saltatory processes and altricial to precocial forms in the ontogeny of fishes. Amer. Zool. 21: 573–596.

    Google Scholar 

  • Balon. E.K. 1981c. Life histories of arctic charts: epigenetic explanations of their invading ability and evolution. International Symposium on Arctic Chart, Winnipeg (in print).

  • Barlow, G.W. 1981. Patterns of parental investment, dispersal and size among coral-reef fishes. Env. Biol. Fish. 6: 65–85.

    Google Scholar 

  • Baylis, J.R. 1981. The evolution of parental care in fishes, with reference to Darwin's rule of male sexual selection. Env. Biol. Fish. 6: 223–251.

    Google Scholar 

  • Beamish, F.W.H. 1979. Migration and spawning energetics of the anadromous sea lamprey,Petromyzon murinus. Env. Biol. Fish. 4: 3–7.

    Google Scholar 

  • Bell, G. 1980. The cost of reproduction and their consequences. Amer. Natur. 116: 45–76.

    Google Scholar 

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

    Google Scholar 

  • Böhlke, J.E. & C.C.G. Chaplin. 1968. Fishes of the Bahamas and adjacent tropical waters. Livingston Publishing Co., Wynnewood. 771 pp.

    Google Scholar 

  • Breder, C.M. Jr. 1933. On the genesis of oral incubation in fishes. Anat. Rec. 57: 62–63.

    Google Scholar 

  • Breder, C.M. Jr. 1939. On the life history and development of the sponge blenny.Paraclinus marmoratus (Steindachner). Zoologica 24: 487–496.

    Google Scholar 

  • Breder, C.M. Jr. 1941. On the reproductive behavior of the sponge blenny,Paraclinus marmoratus (Steindachner). Zoologica 26: 233–235.

    Google Scholar 

  • Budgett, J.S. 1901. On the breeding habits of some West African fishes, with an account of the external features in the development ofProtopterus annectens, and a description of the larva ofPolypterus lapradei. Trans. Zool. Soc. London 16: 115–136.

    Google Scholar 

  • Constantz, G.D. 1979. Life history patterns of a lifebearing fish in contrasting environments. Oecologia (Berlin) 40: 189–201.

    Google Scholar 

  • Daniels, R.A. 1978. Nesting behaviour ofHarpagifer bispinis in Arthur Harbour, Antarctic Peninsula, J. Fish Biol. 12: 465–474.

    Google Scholar 

  • Denizot, J.-P., F. Kirschbaum, G.W.M. Westby & S. Tsuji. 1978. The larval electric organ of the weakly electric fishPollimyrus (Marcusenius) isidori (Mormyridae, Teleostei). J. Neurocytology 7: 165–181.

    Google Scholar 

  • Dépèche, J. 1976. Acquisition et limites de l'autonomie trophique embryonnaire au cours du développement du poisson téléostéen viviparePoecilia reticulata. Bulletin Biologique de la France et de la Belgique 110: 45–97.

    Google Scholar 

  • Eldon, G.A. 1971. Suspected terrestrial deposition of eggs byNeochana apoda Günther (Pisces: Salmoniformes: Galaxiidae). J. Fish Biol. 3: 247–249.

    Google Scholar 

  • Fishelson, L. 1966. Cichlidae of the genusTilapia in Israel. Israel Bull. Fish. Cult. 18: 67–80.

    Google Scholar 

  • Garnaud, J. 1950. La reproduction et l'incubation branchiale chezApogon imberbis G. et L. Bull. Inst. Oceanogr. (Monaco) 977: 1–10.

    Google Scholar 

  • Garnaud, J. 1963. Éthologie d'un poisson extraordinaire:Apogon imberbis. Musée Oceanographique (Monaco) Comm. ID: 51–60.

    Google Scholar 

  • Gerbilsky, N. L. 1956. The role of nervous system in determining the process of change in fish organism into spawning condition. Trudy Karelskogo fit. AN SSSR 5: 6–12. (In Russian).

    Google Scholar 

  • Greenbank, J. & P.R. Nelson. 1959. Life history of the three-spine sticklebackGasterosteus aculeatus Linnaeus in Karluk Lake and Bare Lake. Kodiak Island, Alaska. U.S. Fish. Bull. 153: 537–559.

    Google Scholar 

  • Gross, M.R. 1979. Cuckoldry in sunfishes (Lepomis: Centrarchidae). Can. J. Zool. 57: 1507–1509.

    Google Scholar 

  • Gross. M.R. & E.L. Charnov. 1980. Alternative male life histories in bluegill sunfish. Proc. Natl. Acad. Sci. USA 77: 6937–6940.

    Google Scholar 

  • Gunter, G. 1947. Observations on breeding of the marine catfish.Galeichtys felis (Linnacus). Copeia 1947: 217–223.

    Google Scholar 

  • Hale, H.M. 1947. Evidence of the habit of oral gestation in a south Australian marine fish (Apogon conspersus Klunzinger). The South Austr. Nat. 24: 1–3.

    Google Scholar 

  • Gudger, E.W. 1927. The nest and the nesting habits of the butterfish or gunnel,Pholis gunnellus. Nat. Hist. 27: 65–71.

    Google Scholar 

  • Hamlett, W.C. & J.P. Wourms. 1979. Morphogenesis of the yolk sac placenta in the blue shark,P. glauca. Amer. Zool. 19: 947.

    Google Scholar 

  • Hamlett, W.C., J.P. Wourms & J.W. Smith. 1979. Maternal-fetal relationship in the viviparous cownose-ray,Rhinoptera bonasus. Amer. Zool. 19: 976.

    Google Scholar 

  • Harrington, R.W. 1959. Delayed hatching in stranded eggs of marsh killifish,Fundulus confluentus. Ecology 40: 430–437.

    Google Scholar 

  • Hefford, A.E. 1931. Whitebait. Rep. Fish. N.Z. 1930: 21–23 and 1931: 14, 16–17.

    Google Scholar 

  • Hefford, A.E. 1932. Whitebait investigation. Rep. Fish. N.Z. 1932: 14–15.

    Google Scholar 

  • Hoar, W.S. 1969. Reproduction. pp. 1–72. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, Vol. 3, Academic Press, New York.

    Google Scholar 

  • Karnaukhov, V.N. 1979. The role of filtrator molluscs rich in carotenoid in the self-cleaning of fresh waters. Symp. Biol. Hung. 19: 151–167.

    Google Scholar 

  • Keenleyside, M.H.A. 1979. Diversity and adaptation in fish behaviour. Springer-Verlag, Berlin. 208 pp.

    Google Scholar 

  • Kirschbaum, F. 1977. Electric-organ ontogeny: distinctlarval organ precedes theadult organ in weakly electric fish. Naturwissenschaften 64: 387–388.

    Google Scholar 

  • Kramer, D.L. 1978. Terrestrial group spawning ofBrycon petrosus (Pisces: Characidae) in Panama. Copeia 1978: 536–537.

  • Liem, K.F. 1980. Larvae of air-breathing fishes as counter-current flow devices in hypoxic environments. Amer. Zool. 20: 758.

    Google Scholar 

  • Liem, K.F. 1981. Larvae of air-breathing fishes as counter-current flow devices in hypoxic environments. Science 211: 1177–1179.

    Google Scholar 

  • Lund, R. 1980. Viviparity and intrauterine feeding in a new holocephalan fish from the Lower Carboniferous of Montana. Science 209: 697–699.

    Google Scholar 

  • McDowall, R.M. 1968.Galaxias maculatus, the New Zealand whitebait. N.Z. Fish. Res. Bull. 2: 1–84.

    Google Scholar 

  • McDowall, R.M. 1978. New Zealand freshwater fishes: a guide and natural history. Heinemann Educational Books, Auckland. 230 pp.

    Google Scholar 

  • McElman, J.F. & E.K. Balon. 1979. Early ontogeny of walleye,Stizostedion vitreum, with steps of saltatory development. Env. Biol. Fish. 4: 309–348.

    Google Scholar 

  • McElman, J.F. & E.K. Balon. 1980. Early ontogeny of white sucker,Catostomus commersoni, with steps of saltatory development. Env. Biol. Fish. 5: 191–224.

    Google Scholar 

  • McKaye, K.R. 1977. Defense of a predator's young by a herbivorous fish: an unusual strategy. Amer. Natur. 111: 301–315.

    Google Scholar 

  • McKaye, K.R. 1979. Defense of a predator's young revisited. Amer. Natur. 113: 595–601.

    Google Scholar 

  • McKaye, K.R. & M.K. Oliver, 1980. Geometry of a selfish school: defence of cichlid young by bagrid catfish in Lake Malawi, Africa. Anim. Behaviour 28: 1287.

    Google Scholar 

  • Middaugh, D.P. 1980. Reproductive behavior of the atlantic silverside,Menidia menidia. Abstracts of 60th Annual Meeting of American Society of Ichthyologists and Herpetologists, Fort Worth.

  • Middaugh, D.P., G.I. Scott & J.M. Dean. 1981. Reproductive behavior of the atlantic silverside,Menidia menidia (Pisces: Atherinidae). Env. Biol. Fish. 6: 269–276.

    Google Scholar 

  • Miller, P.J. 1979. A concept of fish phenology. Symp. zool. Soc. Lond. 44: 1–28.

    Google Scholar 

  • Moore, C.J. 1980. Spawning ofMenidia menidia (Piscesa: Atherinidae). Copeia 1980: 886–887.

  • Moreno, C.A. 1980. Observations on food and reproduction inTrematonsus bernacchii (Pisces: Notothemiidae) from the Palmer Archipelago, Antarctica. Copeia 1980: 171–173.

  • Oppenheimer, J.R. & G.W. Barlow. 1968. Dynamics of parental behavior in the black-chinned mouthbreeder,Tilapia melanotheron (Pisces: Cichlidae). Z. Tierpsychol. 25: 889–914.

    Google Scholar 

  • Pietsch, T.W. & D.B. Grobecker. 1980. Parental care as an alternative reproductive mode in an antennariid anglerfish. Copeia 1980: 551–553.

  • Portmann, A. 1945. Die Ontogenese des Menschen als Problem der Evolutionsforschung. Verh. Schweiz. Naturf. Ges. 125: 44–53.

    Google Scholar 

  • Qasim, S.Z. 1957. The biology ofCentronotus gunnellus (L.) (Teleostei). J. Anim. Ecol. 26: 388–401.

    Google Scholar 

  • Reznitchenko, P.N. & Y.G. Yurovitsky. 1959. Ectodermal cilia of embryos, larvae and juveniles of the Kura River sturgeon and their physiological significance. Doklady Akad. nauk SSSR 125: 949–952. (In Russian).

    Google Scholar 

  • Ribbink, A.J., A.C. Marsh & B.A. Marsh. 1981. Nest-building and communal care of young byTilapia rendalli Dumeril (Pisces, Cichlidae) in Lake Malawi. Env. Biol. Fish. 6: 219–222.

    Google Scholar 

  • Ricklefs, R.E. 1979. Adaptation, constraint, and compromise in avian postnatal development. Biol. Rev. 54: 269–290.

    Google Scholar 

  • Rosen, D.E. 1962. Egg retention: pattern in evolution. Natural History 71: 46–53.

    Google Scholar 

  • Rowland, W.J. 1974. Reproductive behavior of the fourspine stickleback,Apeltes quadratus. Copeia 1974: 183–194.

  • Sale, P.F. 1978. Coexistence of coral reef fishes — a lottery for living space. Env. Biol. Fish. 3: 85–102.

    Google Scholar 

  • Shaw, E.S. & L.R. Aronson. 1954. Oral incubation inTilapia macrocephala. Bull. Amer. Mus. Nat. His. 103: 375–416.

    Google Scholar 

  • Soin, S.G. 1951. Data on the development of sturgeons of the Amur River. Trudy Amurskoy ichtiologitcheskoy ekspeditsii 2: 223–232. (In Russian).

    Google Scholar 

  • Soin, S.G. 1968. Adaptive principles of fish development. Moscow Univ. Press, Moscow. 90 pp. (In Russian).

    Google Scholar 

  • Stribling, M.D., W.C. Hamlett & J.P. Wourms. 1980 Developmental efficiency of oophagy, a method of viviparous embryonic nutrition displayed by the sand tiger shark (Eugomphodus taurus). Bull. South Carolina Acad. Sci. 42: 111.

    Google Scholar 

  • Taylor, M.H., L. DiMichele & G.J. Leach. 1977. Egg stranding in the life cycle of the mummichog,Fundulus heteroclitus. Copeia 1977: 397–399.

  • Thibault, R.E. & R.J. Schultz. 1978. Reproductive adaptations among viviparous fishes (Cyprinodontiformes: Poeciliidae). Evolution 32: 320–333.

    Google Scholar 

  • Waddington, C.H. 1975. The evolution of an evolutionist. Edinburgh University Press, Edinburgh. 328 pp.

    Google Scholar 

  • Wallace, R.A. & K. Selman. 1981. The reproductive activity ofFundulus heteroclitus females from Woods Hole, Massachusetts, as compared with more southern locations. Copeia 1981: 212–215.

  • Ward, J.A. & R.L. Wyman. 1977. Ethology and ecology of cichlid fishes of the genusEtroplus in Sri Lanka: preliminary findings. Env. Biol. Fish. 2: 137–145.

    Google Scholar 

  • Werren, J.H., M.R. Cross & R. Shine. 1980. Paternity and the evolution of male parental care. J. theor. biol. 82: 619–631.

    Google Scholar 

  • Westby, G.W.M. & F. Kirschbaum. 1977. Emergence and development of the electric organ discharge in the mormyrid fish,Pollimyrus isidori. I. The larval discharge. J. comp. Physiol. 122: 251–271.

    Google Scholar 

  • Westby, G.W.M. & F. Kirschbaum. 1978. Emergence and development of the electric organ discharge in the mormyrid fish,Pollimyrus isidori. II. Replacement of the larval by the adult discharge. J. Comp. Physiol. 127: 45–49.

    Google Scholar 

  • Whiting, H.P. & Q. Bone. 1980. Ciliary cells in the epidermis of the larval Australian dipnoan,Neoceratodus. Zool. J. Linn. Soc. 68: 125–137.

    Google Scholar 

  • Wourms, J.P. 1971. The developmental basis for the survival of annual fish populations. Symposium on the Biology of Cyprinodontoid Fishes, Annual Meeting of the American Society of Ichthyologists and Herpetologists, Los Angeles.

  • Wourms, J.P. 1977. Reproduction and development in chondrichthyan fishes. Amer. Zool. 17: 379–410.

    Google Scholar 

  • Wourms, J.P. & W.C. Hamlett. 1978. Cell surfaces during development of shark yolk sac plancentae. Amer. Zool. 18:642.

    Google Scholar 

  • Wourms, J.P. & J. Lombardi. 1979. Convergent evolution of trophotaeniae and other gut-derived embryonic adaptations in viviparous teleosts. Abstracts of 59th Ann. Meet. Amer. Soc. Ichthyol. Herpet., Orono.

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Balon, E.K. Additions and amendments to the classification of reproductive styles in fishes. Environ Biol Fish 6, 377–389 (1981). https://doi.org/10.1007/BF00005769

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