A reconceptualization of the interactions between spawning and growth in bony fish

Authors

  • Daniel Pauly Sea Around Us, Institute for the Ocean and Fisheries, University of British Columbia https://orcid.org/0000-0003-3756-4793
  • Cui Liang CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences - Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology https://orcid.org/0000-0001-6099-4965

DOI:

https://doi.org/10.3989/scimar.05280.044

Keywords:

Von Bertalanffy, reproductive drain, maturation, gill-oxygen limitation theory (GOLT)

Abstract


Among fishery biologists and even ichthyologists, maturation and spawning of fish are viewed as processes that use “energy” that would otherwise be applied to somatic growth, which is supposed to explain why post-maturity growth in length tends to decline. This widespread conceptualization may be called the “reproductive drain hypothesis” (RDH). However, when growth is correctly viewed as involving body mass, and is thus expressed in weight, post-maturity turns out (in iteroparous bony fish whose maximum length exceeds 10 cm) to accelerate after first maturity, despite its energy cost. This, and other common observations flatly contradict the RDH, and the time has come to withdraw this hypothesis. As a contribution towards this task, we propose an alternative reconceptualization of fish spawning consistent with what is known about fish biology. 

Downloads

Download data is not yet available.

References

Amarasinghe U.S., Pauly D. 2021. The relationship between size at maturity and maximum size in cichlid populations corroborates the Gill- Oxygen Limitation Theory (GOLT). Asian Fish. Sci. 34: 14-22. https://doi.org/10.33997/j.afs.2021.34.1.002

Beverton R.J.H., Holt S.J. 1959. A Review of the Lifespans and Mortality Rates of Fish in Nature, and Their Relation to Growth and Other Physiological Characteristics. In: Wolstenhome G.E.W., Maeve O'Oconner B.A. (eds), Ciba Foundation Symposium - The Lifespan of Animals (Colloquia on Ageing). John Wiley & Sons Ltd, pp. 142-180. https://doi.org/10.1002/9780470715253.ch10

Budaev S., Jørgensen C., Mangel M., et al. 2019. Decision-making from the animal perspective: bridging ecology and subjective cognition. Front. Ecol. Evol. 7: 164. https://doi.org/10.3389/fevo.2019.00164

Charnov E. 2008. Fish growth: Bertalanffy k is proportional to reproductive effort. Environ. Biol. Fishes. 83: 185-187. https://doi.org/10.1007/s10641-007-9315-5

Chen Z., Bigman J., Xian W., et al. 2022. The ratio of length at first maturity to maximum length in marine and freshwater fish. J. Fish Biol. https://doi.org/10.1111/jfb.14970 PMid:34874555

Cushing D.H. 1981. Fisheries Biology: as Study in Population Dynamics, 2nd edition. University of Wisconsin Press, Madison, 295 pp.

De Jager S., Dekkers W.J. 1974. Relations Between Gill Structure and Activity in Fish. Neth. J. Zool. 25: 276-308. https://doi.org/10.1163/002829675X00290

Froese R. 2006. Cube law, condition factor and weight-length relationships: history, meta-analysis and recommendations. J. Appl. Ichthyol. 22: 241-253. https://doi.org/10.1111/j.1439-0426.2006.00805.x

Froese R., Binohlan C. 2000. Empirical relationships to estimate asymptotic length, length at first maturity and length at maximum yield per recruit in fishes, with a simple method to evaluate length frequency data. J. Fish Biol. 56: 758-773. https://doi.org/10.1111/j.1095-8649.2000.tb00870.x

Hay A., Xian W., BaillyN., Liang C. and Pauly D. 2020. The why and how of determining length-weight relationships of fish from preserved museum specimens. J. Appl. Ichthyol. 36: 373-379. https://doi.org/10.1111/jai.14014

Hubbs C.L. 1926. The structural consequence and modifications of the development rate in fishes, considered in reference to certain problems of evolution. Am. Nat. 60: 57-81. https://doi.org/10.1086/280071

Iles T.D. 1974. The tactics and strategy of growth in fishes. In: Harden Jones E.R. (ed), Sea Fisheries Research. Elek Science, London, pp. 331-345.

Jørgensen C., Ernande B., Fiksen Ø., Dieckman U. 2006. The logic of skipped spawning in fish. Can. J. Fish. Aquat. Sci. 63: 200-211. https://doi.org/10.1139/f05-210

Le Franc G. 1970. Biologie de la morue du Sud de la mer du Nord et de la Manche Orientale. Rev. Trav. Inst. Pêches Marit. 34: 277-296.

Lester N.P., Shuter B.J., Abrams P.A. 2004. Interpreting the von Bertalanffy model of somatic growth in fishes: the cost of reproduction. Proc. R. Soc. B: Biol. Sci. 271: 1625-1631. https://doi.org/10.1098/rspb.2004.2778 PMid:15306310 PMCid:PMC1691769

Li Z.-L., Lu H.-S., Gan X,-P., Jing X. 2009. Growth and mortality of bottom threadfin bream Nemipterus bathybius in the mouth of Beibu Gulf, South China Sea. Fish. Sci. 28: 556-562. [In Chinese with English abstract]

Longhurst A., Pauly D. 1987. Ecology of Tropical Oceans. Academic Press, San Diego, 407 pp. https://doi.org/10.1016/B978-0-12-455562-4.50010-0

Meyer K.A., Schill D.J. 2021. The Gill-Oxygen Limitation Theory and size at maturity/maximum size relationships for salmonid populations occupying flowing waters. J. Fish Biol. 98: 44-49. https://doi.org/10.1111/jfb.14555 PMid:32964452

Morbey Y.E. and D. Pauly. 2022. Juvenile-to-adult transition invariances in fishes: perspectives on proximate and ultimate causation. J. Fish Biol. 1-11. https://doi.org/10.1111/jfb.15146 PMid:35762307

Muir B.S., Hughes G.M. 1969. Gill Dimensions for Three Species of Tunny. J. Exp. Biol. 51: 271-285. https://doi.org/10.1242/jeb.51.2.271b

Pankhurst N.W. 2016. Reproduction and development. In: Schreck C.B., Tort L., Farrell A.P., Brauner C.J. (eds), Fish Physiology Vol. 35. Elsevier, Amsterdam, pp. 295-331. https://doi.org/10.1016/B978-0-12-802728-8.00008-4

Pauly D. 1981. The relationships between gill surface area and growth performance in fish: a generalization of von Bertalanffy's theory of growth. Berichte der Deutschen wissenschaftlichen Kommission für Meeresforschung 28: 251-282.

Pauly D. 1984. A mechanism for the juvenile-to-adult transition in fishes. J. Cons. Int. Explor. Mer 41: 280-284. https://doi.org/10.1093/icesjms/41.3.280

Pauly D. 2019. Gasping Fish and Panting Squids: Oxygen, Temperature and the Growth of Water-Breathing Animals - 2nd Edition. International Ecology Institute, Oldendorf/Luhe, Germany, 279 pp.

Pauly D. 2021a. The Gill-Oxygen Limitation Theory (GOLT) and its critics. Sci. Adv. 7: 2. https://doi.org/10.1126/sciadv.abc6050 PMid:33523964 PMCid:PMC7787657

Pauly D. 2021b. Why do fish reach first maturity when they do? J. Fish Biol. https://doi.org/10.1111/jfb.14902 PMid:34487555

Pauly D., Liang C. 2022. Temperature and the early maturation of fish: a simple sine-wave model for predicting spring spawning. Environ. Biol. Fish. https://doi.org/10.1007/s10641-022-01212-0

Pütter A. 1920. Studien über physiologische Ähnlichkeit VI. Wachstumsähnlichkeiten. Pflüger's Archiv für die gesamte Physiologie des Menschen und der Tiere 180: 298-340. https://doi.org/10.1007/BF01755094

Quince C., Abrams P.A., Shuter B.J., Lester N.P. 2008. Biphasic growth in fish I: Theoretical foundations. J. Theor. Biol. 254: 197-206. https://doi.org/10.1016/j.jtbi.2008.05.029 PMid:18606423

Rideout R.M., Rose G.A., Burton M. 2005. Skipped spawning in female iteroparous fish. Fish Fish. 6: 50-62. https://doi.org/10.1111/j.1467-2679.2005.00174.x

Rijnsdorp A.D. 1989. Maturation of male and female North Sea plaice (Pleuronectes platessa L.). ICES J. Mar. Sci. 46: 35-51. https://doi.org/10.1093/icesjms/46.1.35

Shi D.F., Zhang K., Cai Y.C., Geng P., Xu Y.W., Sun M.S., Chen Z.Z. 2020. Population structure of Trichiurus japonicus in northern South China Sea and parameters of its growth, mortality and maturity. South China Fisheries Science 16: 51-59.

Thom R. 1975. Structural stability and morphogenesis: an outline of a general theory of models. Translated by D.H. Fowler. Benjamin-Cummings, Reading, MA, 348 pp.

Trippel E.A., Kjesbu O.S., Solemdial P. 1997. Effects of adult age and size structure on reproductive output in marine fishes. In: Chambers R.C., Trippel E.A. (eds), Early life history in fish populations. Chapman & Hall-Kluwer, Dordrecht, pp. 31-61. https://doi.org/10.1007/978-94-009-1439-1_2

Wang T., Gao X., Wang J., Jakovlić I., Dan S.G., Liu H.Z. 2015. Life history traits and implications for conservation of rock carp Procypris rabaudi Tchang, an endemic fish in the upper Yangtze River, China. Fish. Sci. 81: 515-523. https://doi.org/10.1007/s12562-015-0872-9

Woodcock A., Davis M. 1980. Catastrophe theory: a new way of understanding how things change. Penguin Books, Harmondworth, 152 pp.

Warlen S.M., Burke J.S. 1990. Immigration of larvae of fall/winter spawning marine fishes into a North Carolina estuary. Estuaries 13: 453-461. https://doi.org/10.2307/1351789

Published

2022-12-14

How to Cite

1.
Pauly D, Liang C. A reconceptualization of the interactions between spawning and growth in bony fish. scimar [Internet]. 2022Dec.14 [cited 2023Jan.28];86(4):e044. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1933

Issue

Section

Articles