Reproductive aspects of Galaxias platei (Pisces, Galaxiidae) in a deep lake in North Patagonia
Daniela Milano A B and Juan P. Barriga AA Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Universidad Nacional del Comahue, Quintral 1250, San Carlos de Bariloche 8400, Río Negro, Argentina.
B Corresponding author. Email: danielamilano@comahue-conicet.gob.ar
Marine and Freshwater Research 69(9) 1379-1388 https://doi.org/10.1071/MF17304
Submitted: 12 October 2017 Accepted: 1 February 2018 Published: 22 May 2018
Abstract
Reproductive characteristics of the native fish Galaxias platei were studied in Lake Moreno, an ultra-oligotrophic deep lake in North Patagonia. According to histological analysis of ovaries, G. platei presents synchronous oocyte development typical of a group-synchronous spawner. Mature oocyte diameter ranged from 1031 to 1419 μm. Based on the gonadosomatic index, annual spawning occurs between April and June (austral autumn) and is directly related to the water temperature of deeper strata (below 30 m) where this species lives, but not with photoperiod. Female G. platei acquire sexual maturity at a length of 105 mm, whereas males acquire sexual maturity at a length of 177 mm. Delaying maturity to obtain higher fecundity, as well as maximum body size and longevity, indicates that G. platei is more specialised than the other South American Galaxias, G. maculatus, in terms of lifestyle. These specialised features are related to the stable environment G. platei lives in and indicate that it could eventually become a vulnerable species in unstable environments, such as the Patagonian lakes dominated by salmonids.
Additional keywords: Andean lakes, oocyte, ovary, reproductive strategy, spawning season.
References
Acharjee, A., Chaube, R., and Joy, K. P. (2017). Effects of altered photoperiod and temperature on expression levels of gonadotrophin subunit mRNAs in the female stinging catfish Heteropneustes fossilis. Journal of Fish Biology 90, 2289–2311.| Effects of altered photoperiod and temperature on expression levels of gonadotrophin subunit mRNAs in the female stinging catfish Heteropneustes fossilis.Crossref | GoogleScholarGoogle Scholar |
Ali, M. A., Sakurai, S., and Collin, S. P. (1990). Adaptive radiation of the retina in Galaxiidae (Salmoniformes). Australian Journal of Zoology 38, 173–186.
| Adaptive radiation of the retina in Galaxiidae (Salmoniformes).Crossref | GoogleScholarGoogle Scholar |
Alonso, C., Rocco, V., Barriga, J. P., Battini, M. A., and Zagarese, H. (2004). Surface avoidance by freshwater zooplankton: field evidence on the role of ultraviolet radiation. Limnology and Oceanography 49, 225–232.
| Surface avoidance by freshwater zooplankton: field evidence on the role of ultraviolet radiation.Crossref | GoogleScholarGoogle Scholar |
Balon, E. K. (1981). Additions and amendments to the classification of reproductive styles in fishes. Environmental Biology of Fishes 6, 377–389.
| Additions and amendments to the classification of reproductive styles in fishes.Crossref | GoogleScholarGoogle Scholar |
Balseiro, E. G., Modenutti, B. E., and Queimaliños, C. (2001). Feeding of Boeckella gracilipes (Copepoda, Calanoida) on ciliates and phytoflagellates in an ultraoligotrophic Andean lake. Journal of Plankton Research 23, 849–857.
| Feeding of Boeckella gracilipes (Copepoda, Calanoida) on ciliates and phytoflagellates in an ultraoligotrophic Andean lake.Crossref | GoogleScholarGoogle Scholar |
Barrantes, M. E., Lattuca, M. E., Vanella, F. A., and Fernández, D. A. (2017). Thermal ecology of Galaxias platei (Pisces, Galaxiidae) in South Patagonia: perspectives under a climate change scenario. Hydrobiologia 802, 255–267.
| Thermal ecology of Galaxias platei (Pisces, Galaxiidae) in South Patagonia: perspectives under a climate change scenario.Crossref | GoogleScholarGoogle Scholar |
Barriga, J. P., Battini, M. A., Macchi, P. J., Milano, D., and Cussac, V. E. (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.
| Spatial and temporal distribution of landlocked Galaxias maculatus and Galaxias platei (Pisces, Galaxiidae) in a lake in the South American Andes.Crossref | GoogleScholarGoogle Scholar |
Barriga, J. P., Battini, M. A., and Cussac, V. E. (2007). Annual dynamic 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.
| Annual dynamic variation of a landlocked Galaxias maculatus (Jenyns 1842) population in a Northern Patagonian river: occurrence of juvenile upstream migration.Crossref | GoogleScholarGoogle Scholar |
Barriga, J. P., Milano, D., and Cussac, V. E. (2013). Variation in vertebral number and its morphological implication in the South American galaxiid, Galaxias platei. Journal of Fish Biology 83, 1321–1333.
| Variation in vertebral number and its morphological implication in the South American galaxiid, Galaxias platei.Crossref | GoogleScholarGoogle Scholar |
Belk, M. C., Habit, E., Ortiz-Sandoval, J. J., Sobenes, C., and Combs, E. A. (2014). Ecology of Galaxias platei in a depauperate lake. Ecology Freshwater Fish 23, 615–621.
| Ecology of Galaxias platei in a depauperate lake.Crossref | GoogleScholarGoogle Scholar |
Boy, C. C., Morriconi, E., and Calvo, J. (2007). Reproduccion in puyen, Galaxias maculatus (Pisces: Galaxiidae), in the southermost extreme of distribution. Journal of Applied Ichthyology 23, 547–554.
| Reproduccion in puyen, Galaxias maculatus (Pisces: Galaxiidae), in the southermost extreme of distribution.Crossref | GoogleScholarGoogle Scholar |
Boy, C. C., Pérez, A. F., Lattuca, M. E., Calvo, J., and Morriconi, E. (2009). Reproductive biology of Galaxias maculatus (Jenyns 1842) in the Río Ovando, a high-latitude environment in southernmost Patagonia, Argentina. Journal of Applied Ichthyology 25, 661–668.
| Reproductive biology of Galaxias maculatus (Jenyns 1842) in the Río Ovando, a high-latitude environment in southernmost Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |
Buria, L., Walde, S. J., Battini, M., Macchi, P. J., Alonso, M., Ruzzante, D. E., and Cussac, V. E. (2007). Movement of a South American perch Percichthys trucha in a mountain Patagonian lake during spawning and pre-spawning periods. Journal of Fish Biology 70, 215–230.
| Movement of a South American perch Percichthys trucha in a mountain Patagonian lake during spawning and pre-spawning periods.Crossref | GoogleScholarGoogle Scholar |
Campos, H. (1969). Reproducción del Aplochiton taeniatus Jenyns. Boletín del Museo Nacional de Historia Natural 29, 207–222.
Campos, H. (1970). Galaxias maculatus (Jenyns) en Chile, con especial referencia a su reproducción. Boletín del Museo Nacional de Historia Natural 31, 5–20.
Campos, H. (1984). Gondwana and neotropical galaxioid fish biogeography. In ‘Evolutionary Ecology of Neotropical Freshwater Fishes’. (Ed. T. M. Zaret.) pp. 113–125. (Dr Junk Publishers: The Hague, Netherlands.)
Carrea, C., Cussac, V. E., and Ruzzante, D. E. (2013). Genetic and phenotypic variation among Galaxias maculatus populations reflects contrasting landscape effects between northern and southern Patagonia. Freshwater Biology 58, 36–49.
| Genetic and phenotypic variation among Galaxias maculatus populations reflects contrasting landscape effects between northern and southern Patagonia.Crossref | GoogleScholarGoogle Scholar |
Chiarello-Sosa, J. M., Battini, M. A., and Barriga, J. P. (2016). Reproductive strategy of the Patagonian catfish Hatcheria macraei. Journal of Fish Biology 89, 1810–1827.
| Reproductive strategy of the Patagonian catfish Hatcheria macraei.Crossref | GoogleScholarGoogle Scholar |
Correa, C., and Hendry, A. P. (2012). Invasive salmonids and lake order interact in the decline of puye grande Galaxias platei in western Patagonia lakes. Ecological Applications 22, 828–842.
| Invasive salmonids and lake order interact in the decline of puye grande Galaxias platei in western Patagonia lakes.Crossref | GoogleScholarGoogle Scholar |
Correa, C., Bravo, A. P., and Hendry, A. P. (2012). Reciprocal trophic niche shifts in native and invasive fish: salmonids and galaxiids in Patagonian lakes. Freshwater Biology 57, 1769–1781.
| Reciprocal trophic niche shifts in native and invasive fish: salmonids and galaxiids in Patagonian lakes.Crossref | GoogleScholarGoogle Scholar |
Cussac, V. E., Cervellini, P. M., and Battini, M. A. (1992). Intralacustrine movements of Galaxias maculatus (Galaxiidae) and Odontesthes microlepidotus (Atherinidae) during their early life history. Environmental Biology of Fishes 35, 141–148.
| Intralacustrine movements of Galaxias maculatus (Galaxiidae) and Odontesthes microlepidotus (Atherinidae) during their early life history.Crossref | GoogleScholarGoogle Scholar |
Cussac, V. E., Ortubay, S., Iglesias, G., Milano, D., Lattuca, M., Barriga, J. P., Battini, M. A., and Gross, M. (2004). The distribution of South American galaxiid fishes: the role of biological traits and post glacial history. Journal of Biogeography 31, 103–121.
| The distribution of South American galaxiid fishes: the role of biological traits and post glacial history.Crossref | GoogleScholarGoogle Scholar |
Dománico, A. A., and Lauce Freyre, R. (2008). Reproductive aspects of the Patagonian silverside (Odontesthes hatcheri Eigenmann, 1909) from the Ezequiel Ramos Mexía reservoir (Argentina). Revista Mvz Cordoba 13, 1446–1455.
| Reproductive aspects of the Patagonian silverside (Odontesthes hatcheri Eigenmann, 1909) from the Ezequiel Ramos Mexía reservoir (Argentina).Crossref | GoogleScholarGoogle Scholar |
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 – B. Rivadavia 6, 29–38.
Habit, E., Piedra, P., Ruzzante, D. E., Walde, S. J., Belk, M. C., Cussac, V. E., Gonzalez, J., and Colin, N. (2010). Changes in the distribution of native fishes in response to introduced species and other anthropogenic effects. Global Ecology and Biogeography 19, 697–710.
| Changes in the distribution of native fishes in response to introduced species and other anthropogenic effects.Crossref | GoogleScholarGoogle Scholar |
Habit, E., Gonzalez, J., Ruzzante, D. E., and Walde, S. J. (2012). Native and introduced fish species richness in Chilean Patagonian lakes: inferences on invasion mechanisms using salmonid-free lakes. Diversity & Distributions 18, 1153–1165.
| Native and introduced fish species richness in Chilean Patagonian lakes: inferences on invasion mechanisms using salmonid-free lakes.Crossref | GoogleScholarGoogle Scholar |
Hutchings, J. A. (2008). Life histories of fish. In ‘Handbook of Fish Biology and Fisheries’. (Eds P. J. B. Hart and J. D. Reynolds.) pp. 149–174. (Blackwell Science: Oxford, UK.)
Jobling, M. (1995). ‘Environmental Biology of Fishes’, 1st edn. (Chapman and Hall: London, UK).
Johnson, D. L. (2000). Preliminary examination of the match–mismatch hypothesis and recruitment variability of yellowtail flounder, Limanda ferruginea. Fish Bulletin 98, 854–863.
Kokita, T., and Nakazono, A. (1998). Plasticity in the mating system of the longnose filefish, Oxymonacanthus longirostris, in relation to mate availability. Journal of Ethology 16, 81–89.
| Plasticity in the mating system of the longnose filefish, Oxymonacanthus longirostris, in relation to mate availability.Crossref | GoogleScholarGoogle Scholar |
Lattuca, M. E., Brown, D., Castineira, L., Renzi, M., Luizon, C., Urbanski, J., and Cussac, V. (2008). Reproduction of landlocked Aplochiton zebra Jenyns (Pisces, Galaxiidae). Ecology Freshwater Fish 17, 394–405.
| Reproduction of landlocked Aplochiton zebra Jenyns (Pisces, Galaxiidae).Crossref | GoogleScholarGoogle Scholar |
Martoja, R., and Martoja Pierson, M. (1970). ‘Técnicas de histología animal’, 1st edn. (Editorial Toray-Mason: Barcelona, Spain.)
Matthews, W. J. (1998). ‘Patterns in Freshwater Fish Ecology’, 2nd edn. (Chapman and Hall: New York, NY, USA.)
McDowall, R. M. (1971). The galaxiid fishes of South America. Zoological Journal of the Linnean Society 50, 33–73.
| The galaxiid fishes of South America.Crossref | GoogleScholarGoogle Scholar |
McDowall, R. M. (1998). Phylogenetic relationships and ecomorphological divergence in sympatric and allopatric species of Paragalaxias (Teleostei: Galaxiidae) in high elevation Tasmanian lakes. Environmental Biology of Fishes 53, 235–257.
| Phylogenetic relationships and ecomorphological divergence in sympatric and allopatric species of Paragalaxias (Teleostei: Galaxiidae) in high elevation Tasmanian lakes.Crossref | GoogleScholarGoogle Scholar |
McDowall, R. M. (2006). Crying wolf, crying foul, or crying shame: alien salmonids and a biodiversity crisis in the southern cool-temperate galaxioid fishes? Reviews in Fish Biology and Fisheries 16, 233–422.
| Crying wolf, crying foul, or crying shame: alien salmonids and a biodiversity crisis in the southern cool-temperate galaxioid fishes?Crossref | GoogleScholarGoogle Scholar |
McDowall, R. M. (2008). Diadromy, history and ecology: a question of scale. Hydrobiologia 602, 5–14.
| Diadromy, history and ecology: a question of scale.Crossref | GoogleScholarGoogle Scholar |
Milano, D. (2003). Biología de Galaxias platei (Pisces, Galaxiidae): especializaciones relativas a su distribución [Biology of Galaxias platei (Pisces, Galaxiidae): Specializations relating to their distribution]. Ph.D. Thesis, Universidad Nacional del Comahue, Bariloche, Argentina.
Milano, D., and Vigliano, P. H. (1997). Nuevos registros de Galaxias platei Steindachner, 1898 en lagos andinos-patagónicos (Teleostei: Osmeriformes: Galaxiidae). Neotrópica 43, 109–111.
Milano, D., Cussac, V. E., Macchi, P. J., Ruzzante, D. E., Alonso, M. F., Vigliano, P. H., and Denegri, M. A. (2002). Predator associated morphology in Galaxias platei in Patagonian lakes. Journal of Fish Biology 61, 138–156.
| Predator associated morphology in Galaxias platei in Patagonian lakes.Crossref | GoogleScholarGoogle Scholar |
Milano, D., Ruzzante, D. E., Cussac, V. E., Macchi, P. J., Ferriz, R. A., Barriga, J. P., Aigo, J. C., Lattuca, M. E., and Walde, S. (2006). Latitudinal and ecological correlates of morphological variation in Galaxias platei (Pisces, Galaxiidae) in Patagonia. Biological Journal of the Linnean Society. Linnean Society of London 87, 69–82.
| Latitudinal and ecological correlates of morphological variation in Galaxias platei (Pisces, Galaxiidae) in Patagonia.Crossref | GoogleScholarGoogle Scholar |
Modenutti, B. E., Balseiro, E. G., and Queimaliños, C. P. (2000). Ciliate community structure in two South Andean lakes: the effect of lake water on Ophrydium naumanni distribution. Aquatic Microbial Ecology 21, 299–307.
| Ciliate community structure in two South Andean lakes: the effect of lake water on Ophrydium naumanni distribution.Crossref | GoogleScholarGoogle Scholar |
Morris, D. P., Zagarese, H. E., Williamson, C. E., Balseiro, E. G., Hargreaves, B. R., Modenutti, B., Moeller, R., and Queimaliños, C. (1995). The attenuation of UV radiation in lakes and the role of dissolved organic carbon. Limnology and Oceanography 40, 1381–1391.
| The attenuation of UV radiation in lakes and the role of dissolved organic carbon.Crossref | GoogleScholarGoogle Scholar |
Murua, H., and Saborido-Rey, F. (2003). Female reproductive strategies of marine fish species of the North Atlantic. Journal of Northwest Atlantic Fishery Science 33, 23–31.
| Female reproductive strategies of marine fish species of the North Atlantic.Crossref | GoogleScholarGoogle Scholar |
Nagahama, Y. (1983). The functional morphology of teleost gonads. In ‘Fish Physiology: Reproduction. Endocrine Tissues and Hormones’. (Eds W. S. Hoar, D. J. Randall, and E. M. Donaldson.) pp. 223–275. (Academic Press: New York, NY, USA.)
Norusis, M. J. (1986). ‘SPSS/PC+ Advanced Statistics' (SPSS Inc.: Chicago, IL, USA.)
Olden, J. D., Poff, N. L., and Bestgen, K. R. (2008). Traits synergisms and the rarity, extirpation, and extinction risk of desert fishes. Ecology 89, 847–856.
| Traits synergisms and the rarity, extirpation, and extinction risk of desert fishes.Crossref | GoogleScholarGoogle Scholar |
Ortubay, S., and Wegrzyn, D. (1991). Fecundación artificial y desarrollo embrionario de Galaxias platei Steindachner (Salmoniformes, Galaxiidae). Medio Ambiente 11, 84–89.
Pankhurst, N. W., and Porter, M. J. R. (2003). Cold and dark or warm and light: variations on the theme of environmental control of reproduction. Fish Physiology and Biochemistry 28, 385–389.
| Cold and dark or warm and light: variations on the theme of environmental control of reproduction.Crossref | GoogleScholarGoogle Scholar |
Pérez, G. L., Queimaliños, C. P., and Modenutti, B. E. (2002). Light climate and plankton in the deep chlorophylly maxima in North Patagonian Andean lakes. Journal of Plankton Research 24, 591–599.
| Light climate and plankton in the deep chlorophylly maxima in North Patagonian Andean lakes.Crossref | GoogleScholarGoogle Scholar |
Pitcher, T. J. (1993). ‘Behaviour of Teleost Fishes’, 2nd edn. (Chapman and Hall: London, UK.)
Ringuelet, R. A. (1975). Zoogeografia y ecología de los peces de aguas continentales de la Argentina y consideraciones sobre las áreas ictiológicas de América del Sur. Ecosur 2, 1–122.
Roff, D. A. (1984). The evolution of life history parameters in teleosts. Canadian Journal of Fisheries and Aquatic Sciences 41, 989–1000.
| The evolution of life history parameters in teleosts.Crossref | GoogleScholarGoogle Scholar |
Ruzzante, D. E., Walde, S. J., Gosse, J. C., Cussac, V. E., Habit, E. M., Zemlak, T. S., and Adams, E. D. M. (2008). Climate control on ancestral population dynamics: insight from Patagonian fish phylogeography. Molecular Ecology 17, 2234–2244.
| Climate control on ancestral population dynamics: insight from Patagonian fish phylogeography.Crossref | GoogleScholarGoogle Scholar |
Schoebitz, K., Rodríguez Echandia, E. L., and Campos, H. (1973). Complex mitochondria in the retinal cones of the teleost Galaxias platei. Journal de Microscopie 18, 109–114.
Shuter, B. J., and Post, J. R. (1990). Climate, population viability, and the zoogeography of temperate fishes. Transactions of the American Fisheries Society 119, 314–336.
| Climate, population viability, and the zoogeography of temperate fishes.Crossref | GoogleScholarGoogle Scholar |
Shuter, B. J., Finstad, A. G., Helland, I. P., Zweimüller, I., and Hölker, F. (2012). The role of winter phenology in shaping the ecology of freshwater fish and their sensitivities to climate change. Aquatic Sciences 74, 637–657.
| The role of winter phenology in shaping the ecology of freshwater fish and their sensitivities to climate change.Crossref | GoogleScholarGoogle Scholar |
Sobenes, C., Link, O., and Habit, E. (2013). Density-dependent microhabitat selection in Galaxias platei: an experimental study. Gayana (Concepción) 77, 35–42.
| Density-dependent microhabitat selection in Galaxias platei: an experimental study.Crossref | GoogleScholarGoogle Scholar |
Stearns, C. S. (2000). Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87, 476–486.
| Life history evolution: successes, limitations, and prospects.Crossref | GoogleScholarGoogle Scholar |
Vigliano, P., Macchi, P., Alonso, M., Denegri, A., Milano, D., Lippolt, G., and Padilla, G. (1999). Un diseño modificado y procedimiento de calado de redes agalleras para estudios cualicuantitativos de peces por estratos de profundidad en lagos araucanos. Natura Neotropicalis 30, 1–11.
Vigliano, P. H., Beauchamp, D. A., Milano, D., Macchi, P. J., Alonso, M. F., Garcia Asorey, M., Denegri, M. A., Ciancio, J. E., Lippolt, G., Rechencq, M., and Barriga, J. P. (2009). Quantifying predation on galaxiids and other native organisms by introduced rainbow trout in an ultraoligotrophic Lake in Northern Patagonia, Argentina: a bioenergetics modeling approach. Transactions of the American Fisheries Society 138, 1405–1419.
| Quantifying predation on galaxiids and other native organisms by introduced rainbow trout in an ultraoligotrophic Lake in Northern Patagonia, Argentina: a bioenergetics modeling approach.Crossref | GoogleScholarGoogle Scholar |
Wetzel, R. G. (2001). ‘Limmnology. Lake and River Ecosystems’, 3rd edn. (Academic Press: San Diego, CA, USA.)
Winemiller, K. O. (2005). Life history strategies, population regulation, and implications for fisheries management. Canadian Journal of Fisheries and Aquatic Sciences 62, 872–885.
| Life history strategies, population regulation, and implications for fisheries management.Crossref | GoogleScholarGoogle Scholar |
Winemiller, K. O., and Rose, K. A. (1992). Patterns of life-history diversification in North American fishes: implications for population regulation. Canadian Journal of Fisheries and Aquatic Sciences 49, 2196–2218.
| Patterns of life-history diversification in North American fishes: implications for population regulation.Crossref | GoogleScholarGoogle Scholar |
Wootton, R. J. (1990). ‘Ecology of Teleost Fishes’, 2nd edn. (Kluwer Academic Publications: London, UK.)
Wootton, R. J., and Smith, C. (2002) ‘Reproductive Biology of Teleost Fishes’, 1st edn. (Wiley: Oxford, UK.)
Zama, A. (1986). Some biological observations on the galaxiid fish, Galaxias platei, collected in Southern Chile. Japanese Journal of Ichthyology 32, 450–453.
| Some biological observations on the galaxiid fish, Galaxias platei, collected in Southern Chile.Crossref | GoogleScholarGoogle Scholar |
Zemlak, T. S., Habit, E. M., Walde, S. J., Battini, M. A., Adams, E. D. M., and Ruzzante, D. E. (2008). Across the southern Andes on fin: glacial refugia, drainage reversals and a secondary contact zone revealed by the phylogeographical signal of Galaxias platei in Patagonia. Molecular Ecology 17, 5049–5061.
| Across the southern Andes on fin: glacial refugia, drainage reversals and a secondary contact zone revealed by the phylogeographical signal of Galaxias platei in Patagonia.Crossref | GoogleScholarGoogle Scholar |