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New insights into reproductive physiology in Antarctic fish: a trial in Lepidonotothen nudifrons

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Abstract

The spatio-temporal delimitation of fish reproduction is essential for the appropriate management and conservation strategies in populations. Assessing this feature in Antarctic Ichthyology is particularly difficult because harsh environmental conditions limit sample collection. This study shows how physiology can contribute compelling evidence to understand reproduction in Antarctic fish using the notothenioid Lepidonotothen nudifrons as a model species. Sampling included 121 specimens caught at Potter Cove (PC), South Shetland Islands (SSI), from November to late March of 2016–2018. Gonadal macroscopic and histologic features are reported. Oocyte growth and change in testosterone and estradiol plasma levels throughout the ovarian growth of L. nudifrons adult females is provided. In March, females (n = 17) attained gonado-somatic index of 13–20% (16.73 ± 4.20), total fecundity of 2196–4652 oocytes/female, the leading clutch oocytes measured 1.7–2.1 mm, and males (n = 5) showed spermatozoids in their testicles. The leading clutch growth was significantly associated with photoperiod, with no diameter variation until the summer solstice, when it began to grow linearly with an estimated rate of 0.01 mm/day. Testosterone and estradiol increased together with the oocyte growing throughout the analysed months, with a higher rate of increase during March. The reproductive effort data, and especially the significant plasma level increase in both sex steroids observed in March, suggest that (1) females were at a late vitellogenesis stage, just prior to the oocyte final maturation, and thus L. nudifrons spawning period might begin in March at SSI; (2) PC is likely a spawning site for L. nudifrons, which indicates that nearshore areas are spawning grounds for some notothenioids.

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Data availability

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

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 Sci 6:19–36

    Google Scholar 

  • Andersson E, Schulz RW, Male R, Bogerd J, Patiña D, Benedet S, Norberg B, Taranger GL (2013) Pituitary gonadotropin and ovarian gonadotropin receptor transcript levels: seasonal and photoperiod-induced changes in the reproductive physiology of female Atlantic salmon (Salmo salar). Gen Comp Endocrinol 191:247–258. https://doi.org/10.1016/j.ygcen.2013.07.001

    Article  CAS  PubMed  Google Scholar 

  • Babin PJ, Cerda J, Lubzens E (2007) The fish oocyte: from basic studies to biotechnological applications. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6235-3

    Book  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 ER, Lagger C (2010) Egg-guarding behaviour in the Antarctic bathydraconid dragonfish Parachaenichthys charcoti. Polar Biol 33:1585–1587

    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 

  • Barrera-Oro E, Moreira E, Seefeldt MA, Valli Francione M, Quartino ML (2019) The importance of macroalgae and associated amphipods in the selective benthic feeding of sister rockcod species Notothenia rossii and N. coriiceps (Nototheniidae) in West Antarctica. Polar Biol 42:317–334

    Article  Google Scholar 

  • Blasina G, Lopez Cazorla A, Deli Antoni M, Bruno D, Delpiani M, Diaz de Astarloa JM (2017) Ontogenetic changes in the feeding strategy of Lepidonotothen nudifrons (Pisces, Nototheniidae) off the South Shetland Islands and the Antarctic Peninsula. Polar Res 36:1331558

    Article  Google Scholar 

  • Bromage N, Porter M, Randall C (2001) The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture 197:63–98

    Article  CAS  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 

  • Cali F, Riginella E, La Mesa M, Mazzoldi C (2016) Life history traits of Notothenia rossii and N. coriiceps along the southern Scotia Arc. Polar Biol 40:1409–1423

    Article  Google Scholar 

  • Calvo J, Morriconi E, Rae GA (1999) Reproductive biology of the icefish Champsocephalus esox (Gunther, 1861) (Channichthyidae). Antarct Sci 11:140–149

    Article  Google Scholar 

  • Campana GL, Zacher K, Deregibus D, Momo FR, Wiencke C, Quartino M (2018) Succession of Antarctic benthic algae (Potter Cove, South Shetland Islands): structural patterns and glacial impact over a four-year period. Polar Biol 41:377–396

    Article  Google Scholar 

  • Casaux R, Barrera-Oro E, Baroni A, Ramon A (2003) Ecology of inshore notothenioid fish from the Danco Coast, Antarctic Peninsula. Polar Biol 26:157–165

    Article  Google Scholar 

  • Casaux R, Mazzotta A, Barrera-Oro E (1990) Seasonal aspects of the biology and diet of nearshore notothenioid fish at Potter Cove, South Shetland Islands, Antarctica. Polar Biol 11:63–72

    Article  Google Scholar 

  • Daniels RA (1982) Feeding ecology of some fishes of the Antarctic Peninsula. Fish Bull 80:575–588

    Google Scholar 

  • DeWitt HH, Heemstra PC, Gon O (1990) Nototheniidae. In: Gon O, Heemstra PC (eds) Fishes of the southern ocean. JLB Smith Institute of Ichthyology, Grahamstown, pp 279–331

    Google Scholar 

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

    Article  Google Scholar 

  • Elisio M, Chalde T, Miranda LA (2014) Seasonal changes and endocrine regulation of pejerrey (Odontesthes bonariensis) oogenesis in the wild. Comp Biochem Physiol A 75:102–109. https://doi.org/10.1016/j.cbpa.2014.05.020

    Article  CAS  Google Scholar 

  • Everson I (1970) Reproduction in Notothenia neglecta Nybelin. Br Antarct Surv Bull 23(81):92

    Google Scholar 

  • Everson I, Kock KH, Campbell S, Parkes G, Cielniaszek Z, Szlakowski, (1991) Reproduction in the mackerel icefish, Champsocephalus gunnari, at South Georgia. Document WG-FSA-91/7. CCAMLR, Hobart, Australia, p 12

    Google Scholar 

  • Ferreira MF, Lo Nostro F, Honji R, Ansaldo M, Genovese G (2019) Endocrine and reproductive endpoints of Notothenia rossii and N. coriiceps: A baseline study for ecotoxicological monitoring in Antarctic waters. Mar Pollut Bull 145:418–428

    Article  CAS  PubMed  Google Scholar 

  • Ferreira MF, Varela ML, Lo Nostro F, Ansaldo M, Genovese G (2017) Reproductive aspects of Notothenia rossii and N. coriiceps (Perciformes, Nototheniidae) at Potter Cove, 25 de Mayo (King George) Island during austral summer. Polar Biol 40:1–11

    Article  Google Scholar 

  • Fores H, Kock KH, Wilhelms S, Jones CD (2004) Diet of two icefish species from the Southern Shetland Islands and Elephant Island, Champsocepalus gunnari and Chaenocephalus aceratus. Polar Biol 27:119–129

    Article  Google Scholar 

  • Ghigliotti L, Herasymchuk VV, Kock KH, Vacchi M (2017) Reproductive strategies of the Antarctic silverfish: known knowns, known unknowns and unknown unknowns. In: Ghigliotti L, Pisano E, Vacchi M (eds) The Antarctic silverfish a keystone species in a changing ecosystem. Springer, Cham, pp 173–192

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  • Hunter JR, Macewicz BJ, Lo NCH, Kimbrell CA (1992) Fecundity, spawning, and maturity of female dover sole, Microstomus pacificus, with an evaluation of assumptions and precision. Fish Bull US 90:101–120

    Google Scholar 

  • Keele L (2008) Semiparametric regression for the social sciences. Wiley, Chichester

    Google Scholar 

  • Kobayashi M, Aisa K, Hanyu I (1989) Involvement of steroid hormones in the preovulatory gonadotropin surge in female goldfish. Fish Physiol Biochem 7:141–146

    Article  CAS  PubMed  Google Scholar 

  • Kock KH (1989) Reproduction in fish around Elephant Island. Arch Fisch Wiss 39:171–210

    Google Scholar 

  • Kock KH (1992) Antarctic fish and fisheries. Cambridge University Press, Cambridge

    Google Scholar 

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

    Article  Google Scholar 

  • Kock KH, Stransky C (2000) The composition of the coastal fish fauna around Elephant Island (South Shetland Islands, Antarctica). Polar Biol 23:825–832

    Article  Google Scholar 

  • Kozlov AN, Pinskaya IA, Podrazhanskaya SG, Tarverdiyeva M (1988) Feeding of glassfishes in different regions of the Atlantic sector of Antarctica. J Ichthyol 28:137–145

    Google Scholar 

  • Kraus G, Muller A, Trella K, Koster FW (2000) Fecundity of the Baltic cod: temporal and spatial variation. J Fish Biol 56:1327–1341

    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, Caputo V, Eastman JT (2006) Gametogenesis and reproductive strategies in some species of the Antarctic fish genus Trematomus (Nototheniidae) from Terra Nova Bay, Ross Sea. Polar Biol 29:963–970

    Article  Google Scholar 

  • La Mesa M, Cali F, Riginella E, Mazzoldi C, Jones CD (2020) Biological parameters of the High-Antarctic icefish, Cryodraco antarcticus (Channichthyidae) from the South Shetland Islands. Polar Biol 43:143–155

    Article  Google Scholar 

  • La Mesa M, Riginella E, Catalano B, Jones CD, Mazzoldi C (2017) Maternal contribution to spawning and early life-history strategies of the genus Lepidonotothen (Nototheniidae, Perciformes) along the southern Scotia Arc. Polar Biol 40:1441–1450

    Article  Google Scholar 

  • Lisovenko LA, Silyanova ZS (1979) The fecundity of some species of the family Nototheniidae in the Atlantic sector of the Southern Ocean. J Ichthyol 19:79–85

    Google Scholar 

  • Llompart F, Delpiani M, Lattuca E, Delpiani G, Cruz-Jimenez A, Orlando P, Ceballos S, Diaz de Astarloa JM, Vanella F, Fernandez D (2015) Spatial patterns of summer demersal fish assemblages around the Antarctic Peninsula and South Shetland Islands. Antarct Sci 27:109–117

    Article  Google Scholar 

  • Lowere-Barbieri S, Ganias K, Saborido-Rey F, Murua H, Hunter J (2010) Reproductive timing in marine fishes: variability, temporal scales, and methods. Mar Coast Fish 3:71–91

    Article  Google Scholar 

  • Lubzens E, Young G, Bobe J, Cerdà J (2010) Oogenesis in teleosts: how fish eggs are formed. Gen Comp Endocrinol 165:367–389

    Article  CAS  PubMed  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 

  • May AW (1967) Fecundity of the Atlantic cod. J Fish Res Board Can 24:1531–1551

    Article  Google Scholar 

  • Muncaster S, Andersson E, Kjesbu OS, Taranger GL, Skiftesvik AB, Norberg B (2010) The reproductive cycle of female ballan wrasse Labrus bergylta in high latitude, temperate waters. J Fish Biol 77:494–511

    CAS  PubMed  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 

  • Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38:217–229

    CAS  PubMed  Google Scholar 

  • Newman DM, Jones PL, Ingram BA (2008) Age-related changes in ovarian characteristics, plasma sex steroids and fertility during pubertal development in captive female Murray cod Maccullochella peelii peelii. Comp Biochem Physiol A 150:444–451. https://doi.org/10.1016/j.cbpa.2008.05.005

    Article  CAS  Google Scholar 

  • Novillo M, Moreira E, Macchi G, Barrera-Oro E (2018) Reproductive biology in the Antarctic bathydraconid dragonfish Parachaenichthys charcoti. Polar Biol 41:2239–2248

    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 

  • Pankhurst NW, Porter MJR (2003) Cold and dark or warm and light: variations on the theme of environmental control of reproduction. Fish Physiol Biochem 28:385–389

    Article  CAS  Google Scholar 

  • Pham HQ, Nguyen AT, Kjørsvik E, Nguyen MD, Arukwe A (2011) Seasonal reproductive cycle of Waigieu seaperch (Psammoperca waigiensis). Aquac Res 43:815–830. https://doi.org/10.1111/j.1365-2109.2011.02894.x

    Article  Google Scholar 

  • Polzonetti-Magni AM, Mosconi G, Soverchia L, Kikuyama S, Carnevali O (2004) Multihormonal control of vitellogenesis in lower vertebrates. Int Rev Cytol 239:1–46. https://doi.org/10.1016/S0074-7696(04)39001-7

    Article  CAS  PubMed  Google Scholar 

  • Quartino ML, Deregibus D, Campana G, Latorre G, Momo F (2013) Evidence of macroalgal colonization on newly ice-free areas following glacial retreat in Potter Cove (South Shetland Islands) Antarctica. PLoS ONE 8:e58223. https://doi.org/10.1371/journal.pone.0058223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Rae GA, Calvo J (1996) Fecundity and reproductive habits in Patagonotothen tessellata (Richardson, 1845) from the Beagle Channel, Argentina. Antarct Sci 3:235–240

    Google Scholar 

  • Ruhl HA, Hastings P, Zarubick LA, Jensen RM, Zdzitowiecki K (2003) Fish populations of Port Foster, Deception Island, Antarctica and vicinity. Deep Sea Res Part 2 50:1843–1858

    Article  Google Scholar 

  • Skóra K, Neyelov AV (1992) Fish of Admiralty Bay (King George Island, South Shetland Islands, Antarctica). Polar Biol 12:469–476

    Article  Google Scholar 

  • Takahashi M, Iwami T (1997) The summer diet of demersal fish at the South Shetland Islands. Antarct Sci 9:407–413

    Article  Google Scholar 

  • Targett TE (1981) Trophic ecology and structure of coastal Antarctic fish community. Mar Ecol Prog Ser 4:243–263

    Article  Google Scholar 

  • Trudeau VL, Lin HR, Peter RE (1991a) Testosterone potentiates the serum gonadotropin response to gonadotropin-releasing hormone in the common carp (Cyprinus carpio) and Chinese loach (Paramisgurnus dabryanus). Can J Zool 69:2480–2484. https://doi.org/10.1139/z91-349

    Article  CAS  Google Scholar 

  • Trudeau VL, Peter RE, Sloley BD (1991b) Testosterone and estradiol potentiate the serum gonadotropin response to gonadotropin-releasing hormone in goldfish. Biol Reprod 44:951–960. https://doi.org/10.1095/biolreprod44.6.951

    Article  CAS  PubMed  Google Scholar 

  • Vacchi M, Williams R, La Mesa M (1996) Reproduction in three species of fish from the Ross Sea and Mawson Sea. Antarct Sci 8:185–192

    Article  Google Scholar 

  • Van Der Molen S, Matallanas J (2003) Oocyte development and maturity classification of Gerlachea australis from the Weddell Sea, Antarctica. Polar Biol 26:653–658

    Article  Google Scholar 

  • Vanella FA, Calvo J, Morriconi ER, Aureliano DR (2005) Somatic energy content and histological analysis of the gonads in Antarctic fish from the Scotia Arc. Sci Mar 69(S2):305–316

    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 

  • YuYe P, Silyanova ZS (1971) New data on the reproductive biology and fecundity of fishes of the genus Notothenia (Richardson) in the Scotia Sea (Antarctica). J Ichthyol 11:693–705

    Google Scholar 

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Acknowledgements

We are grateful to Carlos Bellisio, Rodrigo Varela and Facundo Robino for their help in field activities and laboratory tasks, to Marta Estrada and Hugo Brachetta for the histological section preparation, and to Patricia Estofan for her help in the sex steroid measurements. Prof. Joseph Eastman helped with the English edition of the manuscript. We thank three referees,Drs. Thomas Desvignes, Nathalie Le François, and Vladimir Laptikhovsky, whose comments improve the quality of this work. INIDEP contribution N° 2242.

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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Authors and Affiliations

  1. Consejo Nacional de Investigaciones Científicas Y Técnicas (CONICET), C1425FQB, Buenos Aires, Argentina

    Manuel Novillo, Mariano Elisio, Eugenia Moreira, Gustavo Macchi & Esteban Barrera-Oro

  2. Consejo Nacional de Investigaciones Científicas Y Técnicas (CONICET), Museo Argentino de Ciencias Naturales Bernardino Rivadavia, Av. Ángel Gallardo 470, CI405DJR, Buenos Aires, Argentina

    Manuel Novillo & Esteban Barrera-Oro

  3. Instituto Nacional de Investigación Y Desarrollo Pesquero (INIDEP), B7602HSA, Mar del Plata, Buenos Aires, Argentina

    Mariano Elisio & Gustavo Macchi

  4. Instituto de Investigaciones Marinas Y Costeras (IIMyC), B7602GSD, Mar del Plata, Buenos Aires, Argentina

    Mariano Elisio & Gustavo Macchi

  5. Instituto Antártico Argentino, B1650HMK, San Martín, Prov. de Buenos Aires, Argentina

    Eugenia Moreira & Esteban Barrera-Oro

  6. Laboratorio de Biología Funcional Y Biotecnología (BIOLAB), UNCPBA-CICBA—INBIOTEC-CONICET. Facultad de Agronomía, 7300, Azul, Buenos Aires, Argentina

    Eugenia Moreira

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  1. Manuel Novillo
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Contributions

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

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Correspondence to Manuel Novillo.

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All procedures involving Lepidonotothen nudifrons specimens have followed all applicable appropriate international, national and institutional guidelines for the collection, care, and ethical use of research organisms and material. All necessary approvals were obtained. Sampling was performed under the permit granted by the Dirección Nacional del Antártico (Environmental Management Office).

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Novillo, M., Elisio, M., Moreira, E. et al. New insights into reproductive physiology in Antarctic fish: a trial in Lepidonotothen nudifrons. Polar Biol 44, 1127–1139 (2021). https://doi.org/10.1007/s00300-021-02879-4

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