Abstract
This work aimed to study the reproductive traits of the southernmost landlocked population of Galaxias maculatus living under extreme environmental conditions (54.5° S). Individuals were measured, weighed, sexed, and dissected. The reproductive cycle was analyzed based on the monthly variation of the gonadosomatic indices (GSIs) and the monthly proportion of gonadal stages (established through histology). Fecundity was evaluated by counting macroscopically hydrated oocytes. The reproductive season of G. maculatus in the population assessed extended from March through November (the more protracted for the species described so far). The GSI was higher in males than females, with maximum individual values occurring at the final maturation stage. The simultaneous presence of postovulatory follicles and developing oocytes indicates iteroparity. Our results suggest lower instantaneous investment in reproduction at the individual level but a more prolonged throughout the year than other populations of the species, even under more extreme winter conditions. Considering the increased reproduction costs under extreme habitats and based on our findings, we suggest how populations from the same geographic area can deploy different strategies to cope with energy trade-offs. These results highlight the importance of integrated physiological and ecological approaches to elucidate the basis for variation in life-history traits.
Similar content being viewed by others
Data availability
Data are available from the authors upon reasonable request.
References
Barbee, N. C., R. Hale, J. Morrongiello, A. Hicks, D. Semmens, B. J. Downes & S. E. Swearer, 2011. Large-scale variation in life history traits of the widespread diadromous fish, Galaxias maculatus, reflects geographic differences in local environmental conditions. Marine and Freshwater Research 62: 790–800. https://doi.org/10.1071/MF10284.
Barriga, J. P., M. A. Battini, P. J. Macchi, D. Milano & V. E. Cussac, 2002. Spatial and temporal distribution of landlocked Galaxias maculatus and Galaxias platei (Pisces: Galaxiidae) in a lake in the South American Andes. New Zealand Journal of Marine and Freshwater Research 36: 345–359. https://doi.org/10.1080/00288330.2002.9517092.
Barriga, J. P., M. A. Battini & V. E. Cussac, 2007. Annual dynamics variation of a landlocked Galaxias maculatus (Jenyns 1842) population in a Northern Patagonian river: occurrence of juvenile upstream migration. Journal of Applied Ichthyology 23: 128–135. https://doi.org/10.1111/j.1439-0426.2006.00820.x.
Boy, C. C., E. Morriconi & J. Calvo, 2007. Reproduction in puyen, Galaxias maculatus (Pisces: Galaxiidae), in the southernmost extreme of distribution. Journal of Applied Ichthyology 23: 547–554. https://doi.org/10.1111/j.1439-0426.2006.00842.x.
Boy, C. C., A. F. Pérez, D. A. Fernández, J. Calvo & E. R. Morriconi, 2008. Energy allocation in relation to spawning and overwintering of a diadromous Puyen (Galaxias maculatus) population in the southernmost limit of the species distribution. Polar Biology 32: 9–14. https://doi.org/10.1007/s00300-008-0495-z.
Boy, C. C., A. F. Pérez, M. E. Lattuca, J. Calvo & E. Morriconi, 2009a. Reproductive biology of Galaxias maculatus (Jenyns 1842) in Río Ovando estuary, a high-latitude environment in southernmost Patagonia. Journal of Applied Ichthyology 25: 661–668. https://doi.org/10.1111/j.1439-0426.2009.01309.x.
Boy, C. C., A. F. Pérez, D. A. Fernández, J. Calvo & E. R. Morriconi, 2009b. Energy allocation in relation to spawning and overwintering of a diadromous Puyen (Galaxias maculatus) population in the southernmost limit of the species distribution. Polar Biology 32: 9–14. https://doi.org/10.1007/s00300-008-0495-z.
Campos, H., 1970. Galaxias maculatus (Jenyns) en Chile, con especial referencia a su reproducción. Boletín Del Museo De Historia Natural, Santiago De Chile 31: 5–20.
Campos, H., 1973. Migration of Galaxias maculatus (Jenyns) (Galaxiidae, Pisces) in Valdivia Estuary, Chile. Hydrobiologia 43: 301–312.
Carrea, C., V. E. Cussac & D. E. Ruzzante, 2013. Genetic and phenotypic variation among Galaxias maculatus populations reflects contrasting landscape effects between northern and southern Patagonia. Freshwater Biology 58: 36–49. https://doi.org/10.1111/fwb.12036.
Chapman, A., D. L. Morgan, S. J. Beatty & H. S. Gill, 2006. Variation in life history of land-locked lacustrine and riverine populations of Galaxias maculatus (Jenyns 1842) in Western Australia. Environmental Biology of Fishes 77: 21–37. https://doi.org/10.1007/s10641-006-9051-2.
Closs, G. P., A. S. Hicks & P. G. Jellyman, 2013. Life histories of closely related amphidromous and non-migratory fish species: a trade-off between egg size and fecundity. Freshwater Biology 58: 1162–1177. https://doi.org/10.1111/fwb.12116.
Cussac, V. E., P. M. Cervellini & M. A. Battini, 1992. Intralacustrine movements of Galaxias maculatus (Galaxiidae) and Odontesthes microlepidotus (Atherinidae) during their early life history. Environmental Biology of Fishes 35: 141–148. https://doi.org/10.1007/BF00002189.
Cussac, V. E., M. E. Barrantes, C. C. Boy, K. Górski, E. Habit, M. E. Lattuca & J. H. Rojo, 2020. New insights into the distribution, physiology and life histories of South American Galaxiid fishes, and potential threats to this unique fauna. Diversity 12: 178–193. https://doi.org/10.3390/d12050178.
Drent, R. H. & S. Daan, 1980. The prudent parent: energetic adjustments in avian breeding. Ardea 68: 225–252. https://doi.org/10.5253/arde.v68.p225.
Ferriz, R. A., 1987. Biología del Puyen “Galaxias maculatus” (Jenyns) (Teleostomi, Galaxiidae) en un embalse norpatagónico. Ciclo de vida, ciclo gonadal y fecundidad. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” e Instituto Nacional de Investigación de las Ciencias Naturales 6: 29–38.
Humphries, P., 1989. Variation in the life history of diadromous and landlocked populations of the spotted Galaxias, Galaxias truttaceus Valenciennes, in Tasmania. Australian Journal of Marine and Freshwater Research 40: 501–518. https://doi.org/10.1071/MF9890501.
Jenyns, L., 1842. Part IV, Fish In Darwin, C. (ed), The zoology of the voyage of H.M.S. Beagle, under the command of Captain Fitzroy, R.N. during the years 1832 to 1836. Smith, Elder & Co., London
Laurenson, L. J. B., R. P. French, P. Jones, D. Ierodiaconou, S. Gray, V. L. Versace, A. Rattray, S. Brown & J. Monk, 2012. Aspects of the biology of Galaxias maculatus. Journal of Fish Biology 81: 1085–1100. https://doi.org/10.1111/j.1095-8649.2012.03383.x.
McDowall, R. M., 1968. Galaxias maculatus (Jenyns), the New Zealand whitebait. Fisheries Research Division, Marine Dept., Wellington.
McDowall, R. M., 1990. New Zealand freshwater fishes: a natural history and guide. Heinemann Reed, Auckland, Australia.
Peredo, S. & C. Sobarzo, 1994. Actividad gonádica estacional de Galaxias maculatus (Jenyns, 1842) en el río Cautín. Boletin Sociedad De Biologia Concepción 65: 65–70.
Pollard, D. A., 1971. The biology of a landlocked form of the normally catadromous salmoniform fish Galaxias maculatus (Jenyns). I. Life cycle and origin. Australian Journal of Marine and Freshwater Research 22: 91–123. https://doi.org/10.1071/MF9710091.
R Core Team, 2022. R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna:
Rodríguez, P., González Garraza, G., López, R., Coronato, A., Mataloni, G., Granitto, M., Malits, A., & F. Veira, 2023. Caracterización limnológica, fitoplanctónica y batimétrica de un lago coloreado (Laguna Negra, Parque Nacional Tierra del Fuego, Argentina). Ecología Austral 33: 285–299. https://doi.org/10.25260/EA.23.33.1.0.2014.
Roff, D. A., 1983. An allocation model of growth and reproduction in fish. Canadian Journal of Fisheries and Aquatic Sciences 40: 1395–1404. https://doi.org/10.1139/f83-161.
Roff, D. A., 1992. The Evolution of Life Histories; Theory and Analysis, Chapman & Hall, New York:
Rojo, J. H. & C. C. Boy, 2022. Life-history traits in the southernmost landlocked population of the fish Galaxias maculatus. Polar Biology 45: 1093–1103. https://doi.org/10.1007/s00300-022-03064-x.
Rojo, J. H., D. E. Figueroa & C. C. Boy, 2018. Age and growth of diadromous Galaxias maculatus (Jenyns 1842) in southernmost South America (54° S) including contribution of age classes to reproduction. Environmental Biology of Fishes 101: 1149–1160. https://doi.org/10.1007/s10641-018-0765-8.
Rojo, J. H., D. A. Fernández, D. E. Figueroa & C. C. Boy, 2020a. Phenotypic and genetic differentiation between diadromous and landlocked puyen Galaxias maculatus. Journal of Fish Biology 96: 956–967. https://doi.org/10.1111/jfb.14285.
Rojo, J. H., P. Rodríguez & C. C. Boy, 2020b. Morphological differentiation in the widespread fish Galaxias maculatus: do darker environments imply bigger eyes? Hydrobiologia 847: 2863–2872. https://doi.org/10.1007/s10750-020-04278-y.
Salas-Singh, C., E. Morales-Bojórquez & H. Aguirre-Villaseñor, 2022. Reproductive biology of the bullseye puffer Sphoeroides annulatus: Gonadosomatic index and its suitability for estimating length at maturity. Journal of Fish Biology 101: 1119–1133. https://doi.org/10.1111/jfb.15174.
Sokal, R. R. & F. J. Rohlf, 1995. Biometry, W. H Freeman and Company, New York:
Souto, M., D. Castro, V. Pancotto & M. I. Fraga, 2015. Liverworts of Sphagnum magellanicum Brid. raised bogs from Tierra del Fuego National Park, Ushuaia Argentina. Journal of Bryology 37: 104–111. https://doi.org/10.1179/1743282014Y.0000000131.
Stearns, S. C., 1989. Trade-offs in life-history evolution. Functional Ecology 3: 259–268. https://doi.org/10.2307/2389364.
Stearns, S. C., 1992. The Evolution of Life Histories, Oxford University Press, Oxford:
Stearns, S. C., 2000. Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87: 476–486. https://doi.org/10.1007/s001140050763.
Stevens, J. C. B., M. J. H. Hickford & D. R. Schiel, 2016. Evidence of iteroparity in the widely distributed diadromous fish inanga Galaxias maculatus and potential implications for reproductive output. Journal of Fish Biology 89: 1931–1946. https://doi.org/10.1111/jfb.13083.
Ware, D. M., 1975. Relation between egg size, growth, and natural mortality of larval fish. Journal of the Fisheries Research Board of Canada 32: 2503–2512. https://doi.org/10.1139/f75-288.
Watson, A. S., M. J. H. Hickford & D. R. Schiel, 2023. Closing the life-history loop: density effects on fecundity and egg size of an exploited, amphidromous fish (Galaxias maculatus) in freshwater protected areas. Freshwater Biology. https://doi.org/10.1111/fwb.14091.
West, G., 1990. Methods of assessing ovarian development in fishes: A review. Australian Journal of Marine and Freshwater Research 41: 199–222. https://doi.org/10.1071/MF9900199.
Wickham, H., 2011. The split-apply-combine strategy for data analysis. Journal of Statistical Software 40: 1–29. https://doi.org/10.18637/jss.v040.i01.
Wickham, H., 2016. Elegant Graphics for Data Analysis, Springer-Verlag, New York:
Wickham, H., R. François, L. Henry & K. Müller, 2021. dplyr: a grammar of data manipulation. R Package Version 1: 3.
Wilke, C. O., 2021. ggridges: Ridgeline plots in “ggplot2”. R package version 0.5.3.
Wootton, R. J., 1984. Tactics and strategies in fish reproduction. In Potts, G. W. & R. J. Wootton (eds), Fish Reproduction: Strategies and Tactics Academic Press, New York, United States: 1–12.
Yoneda, M., H. Kitano, S. Selvaraj, M. Matsuyama & A. Shimizu, 2013. Dynamics of gonadosomatic index of fish with indeterminate fecundity between subsequent egg batches: application to Japanese anchovy Engraulis japonicus under captive conditions. Marine Biology 160: 2733–2741. https://doi.org/10.1007/s00227-013-2266-9.
Zar, J. H., 1996. Biostatistical Analysis, Prentice Hall International Ed., Upper Saddle River:
Acknowledgements
The authors thank Sonia Rimbau, Mariela Victorio, Maximiliano Rubel, Katie Johnson, Eugenia Barrantes, and María Florencia Ferreira for their invaluable collaboration with field and laboratory work; and Dra. Myriam Zawoznik for the revision of the language. We thank the associate editor and two anonymous reviewers whose suggestions and comments helped to improve the quality and clarity of the manuscript. This research was supported by Consejo Nacional de Investigaciones Científicas y Técnicas (PIP2021-2023 Nº2934, P-UE 2016), Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación (PICT2017 Nº3845, PICT2021 Nº211), Administración de Parques Nacionales (032CPA), and Fundación Científica Felipe Fiorellino.
Funding
This research was supported by Consejo Nacional de Investigaciones Científicas y Técnicas (PIP2021-2023 Nº2934, P-UE 2016), Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación (PICT2017 Nº3845, PICT2021 Nº211), Administración de Parques Nacionales (032CPA), and Fundación Científica Felipe Fiorellino.
Author information
Authors and Affiliations
Contributions
CCB, JHR, and AFP contributed to conceptualization; CCB, JHR, CPF, DRA, and AFP contributed to developing methods; CCB, JHR, CPF, AO, DRA, and AFP contributed to conducting the research; CCB, JHR, CPF, and AFP contributed to data analysis and interpretation; CCB, JHR, and CPF contributed to preparation of figures and tables; and CCB, JHR, CPF, and AFP contributed to writing.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no competing interests to declare that are relevant to the content of this article.
Ethical approval
Specimens were collected following international and local guidelines of the Comité Institucional de Bioética, Centro Austral de Investigaciones Científicas (CIB-CADIC).
Additional information
Handling editor: Fernando M. Pelicice
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Boy, C.C., Rojo, J.H., Fraysse, C.P. et al. Reproductive traits in the southernmost landlocked population of the fish Galaxias maculatus. Hydrobiologia 851, 573–584 (2024). https://doi.org/10.1007/s10750-023-05345-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-023-05345-w