Abstract
The Antarctic silverfish Pleuragramma antarctica is the most abundant pelagic fish inhabiting the Ross Sea. Given its ecological relevance in the local food web, it is considered a keystone species in the Antarctic coastal ecosystems. Many aspects of its biology have been elucidated, but knowledge of important parts of its life cycle, including reproduction, is still poor. Here we use macroscopic and histological approaches to describe the reproductive features of the Antarctic silverfish based on fish sampled in late summer in the Ross Sea. Both males and females were at an early developmental stage, consistent with what has been reported for the same species from other Antarctic sectors and with spawning occurring in late winter. Widespread follicular atresia has been detected in the fish examined. The analysis of its intensity and prevalence suggests that skipped spawning (not all adults spawn every year) is likely to be a reproductive strategy of the Antarctic silverfish.
Similar content being viewed by others
References
Andriashev AP (1965) A general review of the Antarctic fish fauna. In: van Mieghem J, van Oye P (eds) Biogeography and ecology in Antarctica. Springer, Netherlands, pp 491–550. doi:10.1007/978-94-015-7204-0_15
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. doi:10.1080/19425120.2011.555724
Burton MPM (1999) Notes on potential errors in estimating spawning stock biomass: determining the effects of non- participatory adults for some groundfish species. J North-west Atl Fish Sci 25:1–9
Butskaya NA, Faleeva TI (1987) Seasonal changes in gonads and fecundity of Antarctic fishes Trematomus bernacchii Boulenger, Trematomus hansoni Boulenger and Pagothenia borchgrevinki (Boulenger). Voprosy Ikhtiologii 27:27–36
Calvo J, Morriconi E, Rae GA (1999) Reproductive biology of the icefish Champsocephalus esox (Günther, 1861) (Channichthyidae). Antarctic Sci 11:140–149. doi:10.1017/S0954102099000206
Chapman BB, Skov C, Hulthén K, Brodersen J, Nilsson PA, Hansson LA, Brönmark C (2012) Partial migration in fishes: definitions, methodologies and taxonomic distribution. J Fish Biol 81:479–499. doi:10.1111/j.1095-8649.2012.03349.x
Crim LW, Glebe BD (1990) Reproduction. In: Schreck CB, Moyle PB (eds) Methods for fish biology. American Fisheries Society, Bethesda, pp 529–553
Cury P (1994) Obstinate nature: an ecology of individuals. Thoughts on reproductive behaviour and biodiversity. Can J Fish Aquat Sci 51:1664–1673. doi:10.1139/f94-167
DeWitt HH (1970) The character of the midwater fish fauna of the Ross Sea, Antarctica. In: Holdgate MW (ed) Antarctic ecology. Academic Press, London, pp 305–314
DeWitt HH, Heemstra PC, Gon O (1990) Nototheniidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. Smith Institute of Ichthyology, Grahamstown, pp 279–331
Duhamel G, Kock KH, Balguerias E, Hureau JC (1993) Reproduction in fish of the Weddell Sea. Polar Biol 13:193–200. doi:10.1007/BF00238929
Eastman JT (1997) Phyletic divergence and specialization for pelagic life in the antarctic nothotenioid fish Pleuragramma antarcticum. Comp Biochem Physiol 118A:1095–1101
Everson I (1977) The living resources of the Southern Ocean. FAO Report, GLO/S0177/1, Rome, pp 1–156
Everson I, Kock KH, Campbell S, Parkes G, Cielniaszek Z, Szlakowski J (1991) Reproduction in the mackerel icefish, Champsocephalus gunnari, at South Georgia. Working Document CCAMLR WG-FSA 91/7, pp 1–12
Faleeva TI, Gerasimchuk VV (1990) Reproduction biology peculiarities of Antarctic silverfish, Pleuragramma antarcticum (Nototheniidae). Quest Ichthyol 30:67–79 (in Russian)
Gerasimchuk VV (1987) On the fecundity of Antarctic sidestripe, Pleuragramma antarcticum. J Ichthyol 28:98–100
Gerasimchuk VV (1992) A brief outline of the biology of the Antarctic silverfish, Pleuragramma antarcticum Boulenger, 1902 (Nototheniidae) from the Antarctic Indian Ocean. Working Document CCAMLR WG-FSA-92/11, 47
Giraldo C, Cherel Y, Vallet C, Mayzaud P, Tavernier E, Moteki M, Hosie G, Koubbi P (2011) Ontogenic changes in the feeding ecology of the early life stages of the Antarctic silverfish (Pleuragramma antarcticum) documented by stable isotopes and diet analysis in the Dumont d’Urville Sea (East Antarctica). Polar Sci 5:252–263. doi:10.1016/j.polar.2011.04.004
Granata A, Guglielmo L, Greco S, Vacchi M, Sidoti O, Zagami G, La Mesa M (2000) Spatial distribution and feeding habits of larval and juvenile Pleuragramma antarcticum in the western Ross Sea (Antarctica). In: Faranda F, Guglielmo L, Ianora A (eds) Ross Sea ecology. Springer, Berlin, pp 369–393
Granata A, Cubeta A, Gugliemo L, Sidoti O, Greco S, Vacchi M, La Mesa M (2002) Ichthyoplankton abundance and distribution in the Ross Sea during 1987–1996. Polar Biol 25:187–202. doi:10.1007/s00300-001-0326-y
Guglielmo L, Granata A, Greco S (1998) Distribution and abundance of postlarval and juvenile Pleuragramma antarcticum (Pisces, Nototheniidae) off Terra Nova Bay (Ross Sea, Antarctica). Polar Biol 19:37–51. doi:10.1007/s003000050214
Hanchet SM, Mitchell J, Bowden D, Clark M, Hall J, O’Driscoll R (2008) Ocean survey 20/20: New Zealand IPY-CAML Final Voyage Report. NIWA Client Report: WLG2008-74, October 2008. (Unpublished report held in NIWA library, Wellington)
Hubold G (1984) Spatial distribution of Pleuragramma antarcticum (Pisces: Nototheniidae) near the Filchner and Larsen Ice Shelves (Weddell Sea, Antarctica). Polar Biol 3:231–236. doi:10.1007/BF00292628
Hubold G (1985) The early life history of the high Antarctic Silverfish, Pleuragramma antarcticum. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Heidelberg, pp 445–451
Hunter JR, Macewicz BJ (1985) Rates of atresia in the ovary of captive and wild northern anchovy, Engraulis mordax. Fish Bull 83:119–136
Jørgensen C, Fiksen Ø (2006) State-dependent energy allocation in cod (Gadus morhua). Can J Fish Aquat Sci 63:186–199. doi:10.1139/f05-209
Kjesbu OS, Fonn M, Gonzáles BD, Nilsen T (2010) Stereological calibration of the profile method to quickly estimate atresia levels in fish. Fish Res 104:8–18. doi:10.1016/j.fishres.2010.03.013
Kock KH, Kellermann A (1991) Reproduction in Antarctic notothenioid fish—a review. Antarct Sci 3:125–150. doi:10.1017/S0954102091000172
Koubbi P, O’Brien C, Loots C, Giraldo C, Smith M, Tavernier E, Vacchi M, Vallet C, Chevallier J, Moteki M (2011) Spatial distribution and inter-annual variations in the size frequency distribution and abundances of Pleuragramma antarcticum larvae in the Dumont d’Urville Sea from 2004 to 2010. Polar Sci 5:225–238
La Mesa M, Eastman JT (2012) Antarctic silverfish: life strategies of a key species in the high-Antarctic ecosystem. Fish Fish 13:241–266. doi:10.1111/j.1467-2979.2011.00427.x
La Mesa M, Caputo V, Eastman JT (2008) The reproductive biology of two epibenthic species of Antarctic nototheniid fish of the genus Trematomus. Antarct Sci 20:355–364
La Mesa M, Riginella E, Mazzoldi C, Ashford J (2015) Reproductive resilience of ice-dependent Antarctic silverfish in a rapidly changing system along the Western Antarctic Peninsula. Mar Ecol 36:235–245. doi:10.1111/maec.12140
Loher T, Seitz AC (2008) Characterization of active spawning season and depth for eastern Pacific halibut (Hippoglossus stenolepis) and evidence of probable skipped spawning. J Northwest Atl Fish Sci 41:23–36
Mayzaud P, Chevalier J, Tavernier E, Moteki M, Koubbi P (2011) Lipid composition of the Antarctic fish Pleuragramma antarcticum influence of age class. Polar Sci 5:264–271. doi:10.1016/j.polar.2010.12.003
Miranda ACL, Bazzoli N, Rizzo E, Sato Y (1999) Ovarian follicular atresia in two teleost species: a histological and ultrastructural study. Tissue Cell 31:480–488
Molens S, Matallanas J (2004) Reproductive biology of female Antarctic spiny plunderfish Harpagifer spinosus (Notothenioidei: Harpagiferidae), from Îles Crozet. Antarct Sci 16:99–105. doi:10.1017/S0954102004001865
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
O’Driscoll RL, Macaulay GJ, Gauthier S, Pinkerton M, Hanchet S (2011) Distribution, abundance and acoustic properties of Antarctic silverfish (Pleuragramma antarcticum) in the Ross Sea. Deep Sea Res Part II: Top Stud Oceanogr 58:181–195. doi:10.1016/j.dsr2.2010.05.018
Papi F (1992) Animal homing. Chapman & Hall, London
Parker SJ, Grimes PJ (2010) Length and age at spawning of Antarctic toothfish (Dissostichus mawsoni) in the Ross Sea. CCAMLR Sci 17:53–73
Pinkerton MH, Forman J, Bury SJ, Brown J, Horn P, O’Driscoll RL (2013) Diet and trophic niche of Antarctic silverfish Pleuragramma antarcticum in the Ross Sea, Antarctica. J Fish Biol 82:141–164. doi:10.1111/j.1095-8649.2012.03476.x
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for statistical computing. Vienna, Austria. www.R-project.org
Rideout RM, Tomkiewicz J (2011) Skipped spawning in fishes: more common than you might think. Mar Coast Fish 3:176–189. doi:10.1080/19425120.2011.556943
Rideout RM, Rose GA, Burton MPM (2005) Skipped spawning in female iteroparous fishes. Fish Fish 6:50–72. doi:10.1111/j.1467-2679.2005.00174.x
Santos HB, Thome RG, Arantes FP, Sato Y, Bazzoli N, Rizzo E (2008) Ovarian follicular atresia is mediated by heterophagy, autophagy, and apoptosis in Prochilodus argenteus and Leporinus taeniatus (Teleostei: Characiformes). Theriogenology 70:1449–1460. doi:10.1016/j.theriogenology.2008.06.091
Shandikov GA, Faleeva TI (1992) Features of gametogenesis and sexual cycles of six notothenioid fishes from East Antarctica. Polar Biol 11:615–621. doi:10.1007/BF00237956
Shaw AK, Levin SA (2011) To breed or not to breed: a model of partial migration. Oikos 120:1871–1879. doi:10.1111/j.1600-0706.2011.19443.x
Skjæraasena JE, Nashb RDM, Korsbrekkeb K et al (2012) Frequent skipped spawning in the world’s largest cod population. Proc Natl Acad Sci USA 109:8995–8999. doi:10.1073/pnas.1200223109
Smith WO, Ainley DG, Cattaneo-Vietti R (2007) Trophic interactions within the Ross Sea continental shelf ecosystem. Philos Trans R Soc B 362:95–111. doi:10.1098/rstb.2006.1956
Üçüncü Sİ, Çakıcı Ö (2009) Atresia and apoptosis in preovulatory follicles in the ovary of Danio rerio (zebrafish). Turk J Fish Aquat Sci 9:215–221
Vacchi M, La Mesa M, Greco S (1999) Summer distribution and abundance of larval and juvenile fishes in the western Ross Sea. Antarct Sci 11:54–60. doi:10.1017/S0954102099000085
Vacchi M, DeVries AL, Evans CW, Bottaro M, Ghigliotti L, Cutroneo L, Pisano E (2012) A nursery area for the Antarctic silverfish Pleuragramma antarcticum at Terra Nova Bay (Ross Sea): first estimate of distribution and abundance of eggs and larvae under the seasonal sea-ice. Polar Biol 35:1573–1585. doi:10.1007/s00300-012-1199-y
Van Damme CJG, Dickey-Collas M, Rijnsdorp AD, Kjesbu OS (2009) Fecundity, atresia, and spawning strategies of Atlantic herring (Clupea harengus). Can J Fish Aquat Sci 66:2130–2141. doi:10.1139/F09-153
Vanella FA, Calvo J, Morriconi ER, Aureliano (2005) Somatic energy content and histological analysis of the gonads in Antarctic fish from the Scotia Arc. Sci Mar 69:305–316
Witthames PR, Greenwood L, Lyons B (1999) Ovarian atresia in Solea solea (L). In: Norberg OS, Kjesbu GL, Taranger GL, Andersson E, Stefansson SO (eds) Proceedings of the 6th international symposium on the reproductive physiology of fish, Bergen, Norway, July 4–9, 1999. Jon Greg AS, Bergen, p 106
Witthames PR, Thorsen A, Kjesbu OS (2010) The fate of vitellogenic follicles in experimentally monitored Atlantic cod Gadus morhua (L.): application to stock assessment. Fish Res 104:27–37. doi:10.1016/j.fishres.2009.11.008
Acknowledgments
This work was carried out within the project RAISE (PdR 2013/AZ1.18) supported by the Italian National Programme for Antarctic Research. We thank Michela Angiolillo for her contribution to part of the laboratory activity. The officers and crew of RV Tangaroa, and the scientific staff during the survey, are gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ghigliotti, L., Ferrando, S., Carlig, E. et al. Reproductive features of the Antarctic silverfish (Pleuragramma antarctica) from the western Ross Sea. Polar Biol 40, 199–211 (2017). https://doi.org/10.1007/s00300-016-1945-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-016-1945-7