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Histological analysis provides further insights into Harpagifer antarcticus reproductive biology at the western Antarctic Peninsula

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Abstract

Prior understanding of Harpagifer antarcticus reproductive biology was based exclusively on macroscopic observations of its gonadal maturation cycle. Our present study with H. antarcticus specimens collected in summer of 2019 at Paradise Bay (PB), Western Antarctic Peninsula (WAP), provides a) additional reproductive parameters, and b) for first time, a histological analysis of the gonads, clarifying understanding of the spawning period of the species in the area. In females the gonado-somatic index was 5.3–19.6%, leading clutch oocytes was 0.94–1.95 mm, and total fecundity ranged between 408 and 1723 oocytes/female (X ± SD = 794 ± 328, n = 22). The histology allowed the identification of gravid females with oocytes in late vitellogenesis with evidence of ongoing hydration processes and spent females with post-ovulatory follicles. The presence of spermatozoa in mature testes indicated that the males were in developing and ripe condition. Our reproductive data for H. antarcticus at PB, validated with histology, indicate that the species was in spawning during summer, in agreement with a previous report of a late spring–summer spawning for the species at the same site. Literature data indicate that at the South Orkney Islands, H. antarcticus spawns three months earlier (May–June), probably associated with differential environmental factors between this area and the WAP. Our findings support the hypothesis that the life cycle characteristics of H. antarcticus—e.g., low fecundity and short pelagic phase—promote the isolation of populations as reflected in differences in the reproductive timing.

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All data generated or analyzed during this study are included in this published article [and its supplementary information files].

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References

  • Agnew DJ, Heaps L, Jones C, Watson A, Berkieta K, Pearce J (1999) Depth distribution and spawning pattern of Dissostichus eleginoides at South Georgia. CCAMLR Science 6:19–36

    Google Scholar 

  • Barrera-Oro E (2002) Review: the role of fish in the Antarctic marine food web: differences between inshore and offshore waters in the southern Scotia Arc and west Antarctic Peninsula. Antarct Sci 14:293–309

    Article  Google Scholar 

  • Barrera-Oro E, La Mesa M, Moreira E (2014) Early life history timings in marbled rockcod (Notothenia rossii) fingerlings from the South Shetland Islands as revealed by otolith microincrement. Polar Biol 37:1099–1109

    Article  Google Scholar 

  • Brown-Peterson NJ, Wyanski DM, Saborido-Rey F, Macewicz BJ, Lowerre-Barbieri SK (2011) A standardized terminology for describing reproductive development in fishes. Mar Coast Fish 3:52–70

    Article  Google Scholar 

  • Burren PJ (1988) Reproductive biology of Harpagifer sp. at Signy Island, South Orkney Islands. MSc Thesis, University of North Wales, 52

  • Casaux RJ (1998) The contrasting diet of Harpagifer antarcticus (Notothenioidei, Harpagiferidae) at two localities of the South Shetland Islands, Antarctica. Polar Biol 19:283–285

    Article  Google Scholar 

  • Daniels RA (1978) Nesting behaviour of Harpagifer bispinis in Arthur Harbour, Antarctic Peninsula. J Fish Biol 12:465–474

    Article  Google Scholar 

  • Daniels RA (1979) Nest guard replacement in the Antarctic fish Harpagifer bispinis: possible altruistic behavior. Science 205:831–833

    Article  CAS  Google Scholar 

  • Daniels RA (1983) Demographic characteristics of an Antarctic plunderfish, Harpagifer bispinis antarcticus. Mar Ecol Progr Ser 13:181–187

    Article  Google Scholar 

  • Duhamel G, Hulley PA, Causse R, Koubbi P, Vacchi M, Pruvost P, Vigetta S, Irisson JO, Moreméde S, Belchier M, Dettai A, Detrich HW, Gutt J, Jones CD, Kock KH, Lopez Abellan LJ, Van de Putte AP, Biogeographic patterns of fish. En: De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz C. d’, Van de Putte AP, Danis B, David B, Grant S, Gutt J, Held C, Hosie G, Huettmann F, Post A, Ropert-Coudert Y (eds) (2014) Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, pp 328–362

    Google Scholar 

  • Eastman JT (2005) The nature of the diversity of Antarctic fishes. Polar Biol 28:93–107

    Article  Google Scholar 

  • Eastman JT (2017) Bathymetric distributions of notothenioid fishes. Polar Biol 40:2077–2095

    Article  Google Scholar 

  • Eastman JT (2019) An analysis of maximum body size and designation of size categories for notothenioid fishes. Polar Biol 42:1131–1145

    Article  Google Scholar 

  • Eastman JT, Eakin RR (2021) Checklist of the species of notothenioid fishes. Antarct Sci. https://doi.org/10.1017/S0954102020000632

    Article  Google Scholar 

  • Ghigliotti L, Ferrando S, Carlig E, Di Blasi D, Gallus L, Pisano E, Hancet S, Vacchi M (2017) Reproductive features of the Antarctic silverfish (Pleuragramma antarctica) from the western Ross Sea. Polar Biol 40:199–211

    Article  Google Scholar 

  • Gon O, Heemstra PC (eds) (1990) Fishes of the Southern Ocean. J. L. B. Smith Institute of Ichthyology, Grahamstown, 462 pp. 12 pls

  • Hourigan TF, Radtke RL (1989) Reproduction of the Antarctic fish Nototheniops nudifrons. Mar Biol 100:277–283

    Article  Google Scholar 

  • Hüne M, González-Wevar C, Poulin E, Mansilla A, Fernández DA, Barrera-Oro E (2015) Low level of genetic divergence between Harpagifer fish species (Perciformes: Notothenioidei) suggests a Quaternary colonization of Patagonia from the Antarctic Peninsula. Polar Biol 38:607–617

    Article  Google Scholar 

  • Hureau JC (1990) Harpagiferidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown, pp 357–363

  • Kjesbu O (2009) Applied fish reproductive biology: contribution of individual reproductive potential to recruitment and fisheries management. Wiley, Hoboken

    Google Scholar 

  • Kock KH, Kellermann A (1991) Reproduction in Antarctic notothenioids fish. Antarct Sci 3:125–150

    Article  Google Scholar 

  • La Mesa M, Caputo V, Rampa R, Vacchi M (2003) Macroscopic and histological analyses of gonads during the spawning season of Chionodraco hamatus (Pisces, Channichthyidae) of Terra Nova Bay, Ross Sea, Southern Ocean. Polar Biol 26:621–628

    Article  Google Scholar 

  • La Mesa M, Vera-Duarte J, Landaeta MF (2017) Early life history traits of Harpagifer antarcticus (Harpagiferidae, Notothenioidei) from the South Shetland Islands during austral summer. Polar Biol 40:1699–1705

    Article  Google Scholar 

  • La Mesa M, Llompart F, Riginella E, Eastman JT (2020) Parental care and reproductive strategies in notothenioid fishes. Fish Fish 22:356–376

    Article  Google Scholar 

  • Llompart F, Fernandez D, Aureliano D, La Mesa M (2020) Life-history traits of the Magellan plunderfish Harpagifer bispinis (Forster, 1801) in the Beagle Channel (Tierra del Fuego, South America). Polar Biol 43:1643–1654

    Article  Google Scholar 

  • Macchi G, Barrera-Oro E (1995) Histological study on the ovarian development of mackerel icefish (Champsocephalus gunnari) from the South Georgia Islands. CCAMLR Sci 2:35–49

    Google Scholar 

  • Meneghesso C, Riginella E, La Mesa M, Donato F, Mazzoldi C (2017) Age and reproduction in two Antarctic plunderfishes (Artedidraconidae) from the Weddell Sea. Polar Biol 40:13–24

    Article  Google Scholar 

  • Murua H, Motos L (1998) Reproductive modality and batch fecundity of the European hake (Merluccius merluccius L.) in the Bay of Biscay. Calif Coop Res Rep 39:196–203

    Google Scholar 

  • Murua H, Kraus G, Saborido-Rey F, Witthames PR, Thorsen A, Junquera S (2003) Procedures to estimate fecundity of marine fish species in relation to their reproductive strategy. J Northwest Atl Fish Sci 33:33–54

    Article  Google Scholar 

  • Novillo M, Moreira E, Macchi G, Barrera-Oro E (2019) Reproductive effort in Chaenocephalus aceratus validated by gonadal histology: inshore sites serve as spawning grounds for some notothenioids. Polar Biol 42:1959–1972

    Article  Google Scholar 

  • Piacentino G, Moreira E, Barrera Oro E (2018) Early stages of notothenioid fish from Potter Cove, South Shetland Islands. Polar Biol 41:2607–2613. https://doi.org/10.1007/s00300-018-2366-6

    Article  Google Scholar 

  • Rae GA, Calvo J (1995) Fecundity and reproductive habits in Patagonothen tessellata (Richardson, 1845) from the Beagle Channel, Argentina. Antarct Sci 7:235–240

    Article  Google Scholar 

  • Rae GA, Calvo J (1996) Histological analysis of gonadal development in Patagonotothen tessellata (Richardson 1845) (Nototheniidae: Pisces) from the Beagle Channel, Argentina. J Appl Ichthyol 12:31–38

    Article  Google Scholar 

  • Saborido-Rey F, Junquera S (1998) Histological assessment of variations in sexual maturity of cod (Gadus morhua) at the Flemish Cap (north-west Atlantic). ICES J Mar Sci 55:515–521

    Article  Google Scholar 

  • Tomo AP (1981) Contribución a1 conocimiento de la fauna ictiologica del sector Antártico Argentino. Contribución Científica, Instituto Antártico Argentino 14:1–242

    Google Scholar 

  • Van der Molen S, Matallanas J (2004) Reproductive biology of female Antarctic spiny plunderfish Harpagifer spinosus (Notothenioidei: Harpagiferidae), from Îles Crozet. Antarct Sci 16:99–105

    Article  Google Scholar 

  • Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleost. Am Zool 21:325–343

    Article  Google Scholar 

  • West G (1990) Methods of assessing ovarian development in fishes: a review. Aust J Mar Fresh Res 41:199–222

    Article  Google Scholar 

  • White MG, Burren PJ (1992) Reproduction and larval growth of Harpagifer antarcticus Nybelin (Pisces, Notothenioidei). Antarct Sci 4:421–430

    Article  Google Scholar 

  • Yates P, Ziegler P, Welsford D, McIvor J, Farmer B, Woodcook E (2018) Spatio-temporal dynamics in maturation and spawning of Patagonian toothfish Dissostichus eleginoides on the sub-Antarctic Kerguelen Plateau. J Fish Biol 92:34–54

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to Carlos Bellisio and Agustin Zarco for their help in field activities and laboratory tasks and to Marta Estrada and Hugo Brachetta for the histological sections preparation. Prof. Joseph Eastman provided useful advice on a previous version of this work. We thank Drs. Vladimir Laptikhovsky, Christopher D. Jones, and one anonymous reviewer whose comments improved the quality of our paper. INIDEP contribution N°2253.

Funding

This work was supported by grants from Dirección Nacional del Antártico, Instituto Antártico Argentino [Grant number PICTA 0100], Consejo Nacional de Investigaciones Científicas y Técnicas [Grant number PIP2017-2019: 11220170100219CO, Resolution 2018–8-APN-DIR#CONICET], and Fondo para la Investigación Científica y Tecnológica [Grant number PICT 2018:03310, Resolution 401/19].

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MN and EBO planned and designed the research. MN conducted fieldwork and carried out laboratory work. MN and EM performed statistical analyses. GM and MN analyzed the histological slides. MN and EBO led the writing of the manuscript with contributions from GM and EM.

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Correspondence to Manuel Novillo.

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Novillo, M., Moreira, E., Macchi, G. et al. Histological analysis provides further insights into Harpagifer antarcticus reproductive biology at the western Antarctic Peninsula. Polar Biol 44, 2165–2175 (2021). https://doi.org/10.1007/s00300-021-02953-x

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