Abstract
Studying life-history traits is critical to understanding the intraspecific variation among fish populations. In this research, we investigated the age, growth, and sexual maturity of Galaxias maculatus population from Laguna Negra (LN), the southernmost landlocked population of the species, and compared the results obtained with those obtained before for the diadromous population from Arroyo Negro (AN), 1.8 km away from LN. We read otolith growth bands to estimate age structure and calculated the gonadosomatic index to estimate sexual maturity. We found five age classes (0 + to 4 +) in LN; the maximum age was 4.5 years, the maximum documented age for the species, exceeding in 1 year the maximum age found previously for the AN population. Age class 2 + was the most represented throughout the year, and the greater age and length-at-age ratio observed in this landlocked population suggest a slower growth rate than that of AN. We hypothesize that landlocked individuals reach their first sexual maturity 1 year later than their diadromous counterparts. The protracted reproductive season detected in this landlocked population (9 months) may be related to the high size variability within age classes, where some individuals might maximize growth while others might maximize first sexual maturity. Our results suggest higher energetic costs for these basic biological activities in landlocked than diadromous populations from Tierra del Fuego, Argentina. Further studies are necessary to understand the trade-off between growth and sexual maturation in sub-Antarctic G. maculatus populations.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article.
References
Allen RL (1976) Method for comparing fish growth curves. N Z J Mar Freshw Res 10:687–692. https://doi.org/10.1080/00288330.1976.9515649
Barbee NC, Hale R, Morrongiello J, Hicks A, Semmens D, Downes BJ, Swearer SE (2011) Large-scale variation in life history traits of the widespread diadromous fish, Galaxias maculatus, reflects geographic differences in local environmental conditions. Mar Freshw Res 62:790–800. https://doi.org/10.1071/MF10284
Barriga JP, Battini MA, Macchi PJ, Milano D, Cussac VE (2002) Spatial and temporal distribution of landlocked Galaxias maculatus and Galaxias platei (Pisces: Galaxiidae) in a lake in the South American Andes. N Z J Mar Freshw Res 36:345–359. https://doi.org/10.1080/00288330.2002.9517092
Barriga JP, Battini MA, Cussac VE (2007) Annual dynamics variation of a landlocked Galaxias maculatus (Jenyns 1842) population in a Northern Patagonian river: occurrence of juvenile upstream migration. J Appl Ichthyol 23:128–135. https://doi.org/10.1111/j.1439-0426.2006.00820.x
Baty F, Ritz C, Charles S, Brutsche M, Flandrois JP, Delignette-Muller ML (2015) A toolbox for nonlinear regression in R: The package nlstools. J Stat Softw 66:1–21. https://doi.org/10.18637/jss.v066.i05
Beamish RJ, Fournier DA (1981) A method for comparing the precision of a set of age determinations. Can J Fish Aquat Sci 38:982–983. https://doi.org/10.1139/f81-132
Beverton RJH, Holt SJ (1961) A review of the lifespans and mortality rates of fish in nature, and their relation to growth and other physiological characteristics. CIBA Found Colloquia Ageing 5:142–180. https://doi.org/10.1002/9780470715253.ch10
Billerbeck JM, Lankford TE Jr, Conover DO (2001) Evolution of intrinsic growth and energy acquisition rates. I. Trade-offs with swimming performance in Menidia menidia. Evolution 55:1863–1872. https://doi.org/10.1111/j.0014-3820.2001.tb00835.x
Blanck A, Lamouroux N (2007) Large-scale intraspecific variation in life-history traits of European freshwater fish. J Biogeogr 34:862–875. https://doi.org/10.1111/j.1365-2699.2006.01654.x
Bloch ME, Schneider JG (1801) M.E. Blochii, Systema Ichthyologiae iconibus cx illustratum. Post obitum auctoris opus inchoatum absolvit, correxit, interpolavit Jo. Gottlob Schneider, Saxo. Berolini. Sumtibus Austoris Impressum et Bibliopolio Sanderiano Commissum
Boltovskoy D, Gibbons MJ, Hutchings L, Binet D (1999) General biological features of the South Atlantic. In: Boltovskoy D (ed) South Atlantic zooplankton. Backhuys Publishers, Leiden, pp 1–42
Boy CC, Morriconi E, Calvo J (2007) Reproduction in puyen, Galaxias maculatus (Pisces: Galaxiidae), in the southernmost extreme of distribution. J Appl Ichthyol 23:547–554. https://doi.org/10.1111/j.1439-0426.2006.00842.x
Boy CC, Pérez AF, Fernández DA, Calvo J, Morriconi ER (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 Biol 32:9–14. https://doi.org/10.1007/s00300-008-0495-z
Boy CC, Pérez AF, Lattuca ME, Calvo J, Morriconi E (2009) Reproductive biology of Galaxias maculatus (Jenyns 1842) in RÃo Ovando estuary, a high-latitude environment in southernmost Patagonia. J Appl Ichthyol 25:661–668. https://doi.org/10.1111/j.1439-0426.2009.01309.x
Boy CC, Vanella FA, Lattuca ME, Ceballos SG, Aureliano DR, Rimbau S, Gutiérrez M, Fernández DA (2013) Effect of starvation on growth rate, muscle growth and energy density of puyen, Galaxias maculatus. J Appl Ichthyol 29:1001–1007. https://doi.org/10.1111/jai.12147
Brockington S, Peck LS (2001) Seasonality of respiration and ammonium excretion in the Antarctic echinoid Sterechinus neumayeri. Mar Ecol Prog Ser 219:159–168. https://doi.org/10.3354/meps219159
Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297. https://doi.org/10.3354/meps188263
Campana SE (2001) Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. J Fish Biol 59:197–242. https://doi.org/10.1111/j.1095-8649.2001.tb00127.x
Casselman JM (1987) Determination of age and growth. In: Weatherley AH, Gill HS (eds) The biology of fish growth. Academic Press, New York, pp 209–242
Chapman A, Morgan DL, Beatty SJ, Gill HS (2006) Variation in life history of land-locked lacustrine and riverine populations of Galaxias maculatus (Jenyns 1842) in Western Australia. Environ Biol Fishes 77:21–37. https://doi.org/10.1007/s10641-006-9051-2
Conover DO (1990) The relation between capacity for growth and length of growing season: evidence for and implications of countergradient variation. Trans Am Fish Soc 119:416–430. https://doi.org/10.1577/1548-8659(1990)119%3c0416:TRBCFG%3e2.3.CO;2
Conover DO, Brown JJ, Ehtisham A (1997) Countergradient variation in growth of young striped bass (Morone saxatilis) from different latitudes. Can J Fish Aquat Sci 54:2401–2409. https://doi.org/10.1139/f97-147
Cussac VE, Cervellini PM, Battini MA (1992) Intralacustrine movements of Galaxias maculatus (Galaxiidae) and Odontesthes microlepidotus (Atherinidae) during their early life history. Environ Biol Fishes 35:141–148. https://doi.org/10.1007/BF00002189
Cussac VE, Barrantes ME, Boy CC, Górski K, Habit E, Lattuca ME, Rojo JH (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
Depczynski M, Bellwood DR (2006) Extremes, plasticity, and invariance in vertebrate life history traits: insights from coral reef fishes. Ecology 87:3119–3127. https://doi.org/10.1890/0012-9658(2006)87[3119:EPAIIV]2.0.CO;2
Dinno A (2017) dunn.test: Dunn's test of multiple comparisons using rank sums. R package version 1.3.5 Available at https://CRAN.R-project.org/package=dunn.test. Accessed 15 Nov 2021
Egan EMC, Hickford MJH, Schiel DR (2019) Understanding the life histories of amphidromous fish by integrating otolith-derived growth reconstructions, post-larval migrations and reproductive traits. Aquat Conserv 29:1391–1402. https://doi.org/10.1002/aqc.3145
Erzini K (1994) An empirical study of variability in length-at-age of marine fishes. J Appl Ichthyol 10:17–41. https://doi.org/10.1111/j.1439-0426.1994.tb00140.x
Folkvord A, Jørgensen C, Korsbrekke K, Nash RDM, Nilsen T, Skjæraasen JE (2014) Trade-offs between growth and reproduction in wild Atlantic cod. Can J Fish Aquat Sci 71:1106–1112. https://doi.org/10.1139/cjfas-2013-0600
Gillanders BM, Izzo C, Doubleday ZA, Ye Q (2015) Partial migration: growth varies between resident and migratory fish. Biol Lett 11:20140850. https://doi.org/10.1098/rsbl.2014.0850
Humphries P (1989) Variation in the life history of diadromous and landlocked populations of the spotted Galaxias, Galaxias truttaceus Valenciennes, in Tasmania. Aust J Mar Freshw Res 40:501–518. https://doi.org/10.1071/MF9890501
Huss M, Lindmark M, Jacobson P, van Dorst RM, Gårdmark A (2019) Experimental evidence of gradual size-dependent shifts in body size and growth of fish in response to warming. Glob Change Biol 25:2285–2295. https://doi.org/10.1111/gcb.14637
Jenyns L (1842) Part IV, Fish. In Darwin C (ed) The zoology of the voyage of HMS Beagle, under the command of Captain Fitzroy, RN during the years 1832 to 1836. Smith, Elder & Co., London
Jennings S, Beverton RJH (1991) Intraspecific variation in the life history tactics of Atlantic herring (Clupea harengus L.) stocks. ICES J Mar Sci 48:117–125. https://doi.org/10.1093/icesjms/48.1.117
Jewett SL, Lachner EA (1983) Seven new species of the Indo-Pacific genus Eviota (Pisces: Gobiidae). Proc Biol Soc Wash 96:780–806
Laurenson LJB, French RP, Jones P, Ierodiaconou D, Gray S, Versace VL, Rattray A, Brown S, Monk J (2012) Aspects of the biology of Galaxias maculatus. J Fish Biol 81:1085–1100. https://doi.org/10.1111/j.1095-8649.2012.03383.x
Magnaye M, Rideout RM, Davoren G (2019) Irregular growth patterns in the otoliths of a short-lived forage fish do not reliably indicate reproductive history. Fish Res 218:120–126. https://doi.org/10.1016/j.fishres.2019.05.007
McDowall RM (1968) Galaxias maculatus (Jenyns), the New Zealand whitebait. Fisheries Research Division, Marine Dept., Wellington
McDowall RM (1971) The galaxiid fishes of South America. Zool J Linn Soc 50:33–73. https://doi.org/10.1111/j.1096-3642.1971.tb00751.x
McDowall RM, Mitchell CP, Brothers EB (1994) Age at migration from the sea of juvenile Galaxias in New Zealand (Pisces: Galaxiidae). Bull Mar Sci 54:385–402
Nielsen J, Hedeholm RB, Heinemeier J, Bushnell PG, Christiansen JS, Olsen J, Ramsey CB, Brill RW, Simon M, Steffensen KF, Steffensen JF (2016) Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus). Science 353:702–704. https://doi.org/10.1126/science.aaf1703
Ogle DH (2016) FSA: fisheries stock analysis. R package version 0.8.9. Available at https://cran.r-project.org/web/packages/FSA. Accessed 15 May 2021
Olsen Z, McDonald D, Bumguardner B (2018) Intraspecific variation in life history strategies and implications for management: a case study of black drum (Pogonias cromis) in the Upper Laguna Madre, Texas USA. Fish Res 207:55–62. https://doi.org/10.1016/j.fishres.2018.06.009
Parker Jr. RO, Dixon RL (1998) Changes in a North Carolina reef fish community after 15 years of intense fishing—Global warming implications. Trans Am Fish Soc 127:908–920. https://doi.org/10.1577/1548-8659(1998)127%3c0908:CIANCR%3e2.0.CO;2
Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25:459–467. https://doi.org/10.1016/j.tree.2010.05.006
Pollard DA (1971) The biology of a landlocked form of the normally catadromous salmoniform fish Galaxias maculatus (Jenyns). I. Life cycle and origin. Aust J Mar Freshw Res 22:91–123. https://doi.org/10.1071/MF9710091
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ricker WE (1969) Effects of size-selective mortality and sampling bias on estimates of growth, mortality, production and yield. J Fish Res Board Can 26:479–541. https://doi.org/10.1139/f69-051
Roff DA (1988) The evolution of migration and some life history parameters in marine fishes. Environ Biol Fishes 22:133–146. https://doi.org/10.1007/BF00001543
Rojo JH, Figueroa DE, Boy CC (2018) Age and growth of diadromous Galaxias maculatus (Jenyns 1842) in southernmost South America (54° S) including contribution of age classes to reproduction. Environ Biol Fishes 101:1149–1160. https://doi.org/10.1007/s10641-018-0765-8
Rojo JH, Fernández DA, Figueroa DE, Boy CC (2020a) Phenotypic and genetic differentiation between diadromous and landlocked puyen Galaxias maculatus. J Fish Biol 96:956–967. https://doi.org/10.1111/jfb.14285
Rojo JH, RodrÃguez P, Boy CC (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
Röpke C, Pires THS, Zuanon J, Freitas CEC, Hernandes MC, Souza F, Amadio S (2021) Growth–reproduction trade-off and fecundity regulate population stability in Amazon floodplain fishes. Freshw Biol 00:1–9. https://doi.org/10.1111/fwb.13702
Sainsbury KJ (1980) Effect of individual variability on the von Bertalanffy growth equation. Can J Fish Aquat Sci 37:241–247. https://doi.org/10.1139/f80-031
Snyder RJ (1991) Migration and life histories of the threespine stickleback: evidence for adaptive variation in growth rate between populations. Environ Biol Fishes 31:381–388. https://doi.org/10.1007/BF00002363
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Stevens WL (1951) Asymptotic regression. Biometrics 7:247–267. https://doi.org/10.2307/3001809
Stevens JCB, Hickford MJH, Schiel DR (2016) Evidence of iteroparity in the widely distributed diadromous fish inanga Galaxias maculatus and potential implications for reproductive output. J Fish Biol 89:1931–1946. https://doi.org/10.1111/jfb.13083
Urbatzka R, Beeck P, van der Velde G, Borcherding J (2008) Alternative use of food resources causes intra-cohort variation in the size distribution of young-of-the-year perch (Perca fluviatilis). Ecol Freshw Fish 17:475–480. https://doi.org/10.1111/j.1600-0633.2008.00300.x
van Rooij JM, Bruggemann JH, Videler JJ, Breeman AM (1995) Plastic growth of the herbivorous reef fish Sparisoma viride: field evidence for a trade-off between growth and reproduction. Mar Ecol Prog Ser 122:93–105. https://doi.org/10.3354/meps122093
Vega R, Dantagnan P, Mardones A, Valdebenito I, Zamorano J, Encina F (2013) Bases biológicas para el cultivo del puye Galaxias maculatus (Jenyns, 1842): una revisión. Lat Am J Aquat Res 41:369–386. https://doi.org/10.3856/vol41-issue3-fulltext-1
von Bertalanffy L (1938) A quantitative theory of organic growth (inquiries on growth laws, II). Hum Biol 10:181–213
von Bertalanffy L (1957) Quantitative laws in metabolism and growth. Q Rev Biol 32:217–231. https://doi.org/10.1086/401873
Wootton RJ (1990) Ecology of teleost fishes. Chapman and Hall, New York
Acknowledgements
The authors thank A. Odetto, S. Rimbau, and D. Aureliano for their collaboration. We also thank Dr. M. Zawoznik for the revision of the language. This research was supported by Consejo Nacional de Investigaciones CientÃficas y Técnicas (PIP 0440, P-UE 2016), Agencia Nacional de Promoción CientÃfica y Tecnológica (PICT 2014-1804, PICT 2017-3845), Administración de Parques Nacionales (032CPA).
Funding
This work was supported by CONICET (PIP 0440 and P-UE 2016); Agencia Nacional de Promoción CientÃfica y Tecnológica (PICT 2014-1804, PICT 2017-3845); Administración de Parques Nacionales (Project 032CPA).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception, design, sampling, and data analysis. All authors read and approved the final manuscript. Funding acquisition: CCB.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no competing financial or personal interests to declare that are relevant to the content of this article.
Ethical approval
The Administración de Parques Nacionales granted permission to capture and use the fish in this study (Project 032CPA). International guidelines on the care and use of laboratory animals were followed in this study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rojo, J.H., Boy, C.C. Life-history traits in the southernmost landlocked population of the fish Galaxias maculatus. Polar Biol 45, 1093–1103 (2022). https://doi.org/10.1007/s00300-022-03064-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-022-03064-x