Abstract
The limpet Nacella concinna is one of the most widely distributed gastropods along the Antarctic Peninsula. This species has been a useful tool in ecological and physiological studies for understanding Antarctic trophic interactions. Although the reproduction of limpets has been thoroughly studied, very little is known about gametogenesis in the genus Nacella. The purpose of this study is to describe the gonadal morphology and gametogenesis in N. concinna observed by light microscopy and to determine its chromosome complement. All the limpets were sexually mature at the time of sampling. Oocytes were separated by trabeculae with abundant glycogen reserves. There was a predominance of late vitellogenic oocytes. Many previtellogenic oocytes were pyriform in shape. Oogonia were clustered near the ovary wall or the trabeculae. Only two meiotic stages were found: metaphase I and anaphase I, both of which showed a regular arrangement of chromosomes. The oviduct contained mature oocytes surrounded by sperm. Testicular tubules were filled with spermatozoa. The elongated head of the spermatozoon resembles that of other Nacellidae members. One of the bivalents is heteropycnotic. The haploid complement is n = 4 and the sex determination system is XO/XX. Although N. concinna has been commonly characterized as a broadcast-spawner, its unique spawning behavior, the presence of oocytes at anaphase I and spermatozoa within the oviduct suggests internal fertilization.
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References
Ahn IY, Kim KW, Choi HJ (2002) A baseline study on metal concentrations in the Antarctic limpet Nacella concinna (Gastropoda: Patellidae) on King George island: variations with sex and body parts. Mar Pollut Bull 44:421–431. https://doi.org/10.1016/S0025-326X(01)00297-1
Amsler MO, Huang YM, Engl W, McClintock JB, Amsler CD (2015) Abundance and diversity of gastropods associated with dominant subtidal macroalgae from the western Antarctic Peninsula. Polar Biol 38:1171–1181. https://doi.org/10.1007/s00300-015-1681-4
Ansaldo M, Najle R, Luquet CM (2005) Oxidative stress generated by diesel seawater contamination in the digestive gland of the Antarctic limpet Nacella concinna. Mar Environ Res 59:381–390. https://doi.org/10.1016/j.marenvres.2004.06.003
Ansaldo M, Sacristán H, Wider E (2007) Does starvation influence the antioxidant status of the digestive gland of Nacella concinna in experimental conditions? Comp Biochem Physiol C 146:118–123. https://doi.org/10.1016/j.cbpc.2006.11.004
Barrera Oro ER, Casaux RJ (1990) Feeding selectivity in Notothenia neglecta, Nybelin, from Potter Cove, South Shetland Island, Antarctica. Antarct Sci 2:207–213. https://doi.org/10.1017/S0954102090000281
Benmeradi N (1992) La vitellogenese chez Patella coeruelae Lmk (Mollusca, Gasteropoda) Approche ultrastructurale. Société Française de Malacologie. Aspects Récents de la Biologie des Mollusques. Ifremer. Actes de Colloques, vol 13, pp. 39–46. https://archimer.ifremer.fr/doc/1991/acte-1720.pdf
Branch GM (1974) The Ecology of Patella Linnaeus from the Cape Peninsula, South Africa. 2. Reproductive cycles. Trans Roy Soc S Afr 41:111–160. https://doi.org/10.1080/00359197409520068
Brȇthes JC, Ferreyra G, de la Vega S (1994) Distribution, growth and reproduction of the limpet Nacella (Patinigera) concinna (Strebel 1908) in relation to potential food availability, in Esperanza Bay (Antarctic Peninsula). Polar Biol 14:161–170. https://doi.org/10.1007/BF00240521
Cadée GC (1999) Shell damage and shell repair in the Antarctic limpet Nacella concinna from King George Island. J Sea Res 41:149–161. https://doi.org/10.1016/S1385-1101(98)00042-2
Chen SH, Xia LP, Dahms HU, Peng X, Ying XP (2015) The ultrastructural characteristics of spermatogenesis in Onchidium struma (Pulmonata: Onchidiidae) and its functional adaptation. Ital J Zool 82:489–498. https://doi.org/10.1080/11250003.2015.1062149
Colas P, Dubé F (1998) Meiotic maturation in mollusc oocytes. Semin Cell Dev Biol 9:539–548. https://doi.org/10.1006/scdb.1998.0248
Collado GA, Brown DI (2006) Morphology of the spermatozoon in two sympatric species of Fissurella Bruguière, 1789 (Mollusca: Vetigastropoda) from Southern Chile. Invertebr Reprod Dev 49:79–84. https://doi.org/10.1080/07924259.2006.9652196
Dopchiz LP, Poggio L (1999) Meiosis and pollen grain development in Isolepis cernua f. cernua (Cyperaceae). Caryologia 52:197–201. https://doi.org/10.1080/00087114.1998.10589173
Dreon MS, Heras H, Pollero RJ (2006) Biochemical composition, tissue origin and functional properties of egg perivitellins from Pomacea canaliculata. Biocell 30:359–365
Favero M, Silva P, Ferreyra G (1997) Trophic relationships between the kelp gull and the Antarctic limpet at King George Island (South Shetland Islands, Antarctica) during the breeding season. Polar Biol 17:431–436. https://doi.org/10.1007/s003000050137
Harasewych MG, McArthur AG (2000) A molecular phylogeny of the Patellogastropoda (Mollusca: Gastropoda). Mar Biol 137:183–194. https://doi.org/10.1007/s002270000332
Hodgson AN (2009) Reproduction and sex in invertebrate. In: da Silva AP (ed) Reproduction and development biology. Encyclopedia of Life Support Systems. Developed under the auspices of the UNESCO, EOLSS Publishers, Paris, pp 1–27. http://www.eolss.net
Hodgson AN (2010) Prosobranchs with internal fertilization. In: Leonard JL, Córdoba-Aguilar A (eds) The evolution of primary sexual characters in animals. Oxford University Press, New York, pp 121–140
Hodgson AN, Bernard RTF (1988) A comparison of the structure of the spermatozoa and spermatogenesis of 16 species of patellid limpet (Mollusca: Gastropoda: Archaeogastropoda). J Morphol 195:205–223. https://doi.org/10.1002/jmor.1051950207
Hodgson AN, Bernard RTF (1989) Spermatozoon structure and the taxonomic affinity of the limpet Nacella delesserti (Gastropoda: Patellidae). J Mollus Stud 55:145–147. https://doi.org/10.1093/mollus/55.1.145
Hodgson AN, Eckelbarger KJ (2000) Ultrastructure of the ovary and oogenesis in six species of patellid limpets (Gastropoda: Patellogastropoda) from South Africa. Invertebr Biol 119:265–277. https://doi.org/10.1111/j.1744-7410.2000.tb00013.x
Hodgson AN, Ridgway S, Branch GM, Hawkins SJ (1996) Spermatozoan morphology of 19 species of prosobranch limpets (Patellogastropoda) with a discussion of patellid relationships. Phil Trans R Soc Lond B 351:339–347. https://doi.org/10.1098/rstb.1996.0027
Hodgson AN, Le Quesne WJF, Hawkins SJ, Bishop JDD (2007) Factors affecting fertilization success in two species of patellid limpet (Mollusca: Gastropoda) and development of fertilization kinetics models. Mar Biol 150:415–426. https://doi.org/10.1007/s00227-006-0354-9
Hodgson AN, Hodgson V, Eckelbarger KJ (2012) Structure and formation of the unusual sperm of Patelloida latistrigata (Mollusca: Patellogastropoda): implications for fertilization biology. Biol Bull 222:118–127. https://doi.org/10.1086/bblv222n2p118
Kessel RG (1982) Differentiation of Acmaea digitalis oocytes with special reference to lipid-endoplasmic reticulum-annulate lamellae-polyribosome relationships. J Morphol 171:225–243. https://doi.org/10.1002/jmor.1051710210
McCarthy M, Woosnam P, Culloty SC (2008) Histological investigation of the reproductive cycles of the limpets Patella vulgata and Patella ulyssiponensis. Mar Biol 153:871–877. https://doi.org/10.1007/s00227-007-0859-x
McNally KL, McNally FJ (2005) Fertilization initiates the transition from anaphase I to metaphase II during female meiosis in C. elegans. Dev Biol 282:218–230. https://doi.org/10.1016/j.ydbio.2005.03.009
Morriconi E (1999) Reproductive biology of the limpet Nacella (P.) deaurata (Gmelin, 1791) in Bahía Lapataia (Beagle Channel). Sci Mar 63:417–426. https://doi.org/10.3989/scimar.1999.63s1417
Najle R, Elissondo M, Gentile S, Gentile M, Vacarezza G, Solana H (2000) Histopathology of the digestive gland of an Antarctic limpet exposed to cadmium. Sci Total Environ 247:263–268. https://doi.org/10.1016/S0048-9697(99)00495-7
Najmudeen TM (2008) Ultrastructural studies of oogenesis in the variable abalone Haliotis varia (Vestigastropoda: Haliotidae). Aquat Biol 2:143–151. https://doi.org/10.3354/ab00046
Neuberger-Cywiak L, Rossini M, Najle R (2009) Monitoreo ambiental basado en estudios histológicos de hepatopáncreas y gónadas en Nacella concinna (Strebel, 1908) (Gastropoda: Patellidae) (Bahía Maxwell, Antártida). IX Congress of the Society of Environmental Toxicology and Chemistry in Latin America; II Peruvian Congress of Ecotoxicology and Environmental Chemistry, Santiago de Lima, Peru. https://doi.org/10.13140/2.1.4953.4723
Nishikawa S (1962) A comparative study of the chromosomes in marine gastropods, with some remarks on cytotaxonomy and phylogeny. J Shimonoseki Coll Fish 11:149–186
Niu C, Fuji A (1989) Gametogenesis and reproductive cycle of the limpet Collisella heroldi (Dunker, 1861). Bull Fac Fish Hokkaido Univ 40:214–227
Nuñez O (1968) An acetic-haematoxylin squash method for small chromosomes. Caryologia 21:115–119. https://doi.org/10.1080/00087114.1968.10796290
Picken GB (1980) The distribution, growth, and reproduction of the Antarctic limpet Nacella (Patinigera) concinna (Strebel, 1908). J Exp Mar Biol Ecol 42:71–85. https://doi.org/10.1016/0022-0981(80)90167-7
Picken GB, Allan D (1983) Unique spawning behaviour by the Antarctic limpet Nacella (Patinigera) concinna (Strebel, 1908). J Exp Mar Biol Ecol 71:283–287. https://doi.org/10.1016/0022-0981(83)90121-1
Powell DK, Tyler PA, Peck LS (2001) Effect of sperm concentration and sperm ageing on fertilization success in the Antarctic soft-shelled clam Laternula elliptica and the Antarctic limpet Nacella concinna. Mar Ecol Prog Ser 215:191–200. https://doi.org/10.3354/meps215191
Prusina I, Ezgeta-Balić D, Ljubimir S, Dobroslavić T, Glamuzina B (2014) On the reproduction of the Mediterranean keystone limpet Patella rustica: histological overview. J Mar Biol Assoc UK 94:1651–1660. https://doi.org/10.1017/S0025315414000976
Rasband WS (2017) ImageJ 1.51. U.S. National Institutes of Health, Bethesda, Maryland, USA. https://imagej.nih.gov/ij/
Reunov AA, Hodgson AN (1994) Ultrastructure of the spermatozoa of five species of South African bivalves (Mollusca), and an examination of early spermatogenesis. J Morphol 219:275–283. https://doi.org/10.1002/jmor.1052190307
Ridgway SA, Reid DG, Taylor JD, Branch GM, Hodgson AN (1998) A cladistic phylogeny of the family Patellidae (Mollusca: Gastropoda). Philos Trans R Soc Lond B 353:1645–1671. https://doi.org/10.1098/rstb.1998.0316
Rocha-Barreira CA (2002) Gonad characterization and reproductive cycle of Collisella subrugosa (Orbigny, 1846) (Gastropoda: Acmaeidae) in the Northeastern Brazil. Braz J Biol 62:885–895. https://doi.org/10.1590/S1519-69842002000500019
Southward AJ, Dodd JM (1956) Studies on the biology of limpets: I. The late J. H. Orton’s work on Patella. J Mar Biol Assoc UK 35:145–147. https://doi.org/10.1017/S0025315400009024
Stanwell-Smith D, Clarke A (1998) The timing of reproduction in the Antarctic limpet Nacella concinna (Strebel, 1908) (Patellidae) of Signy Island, in relation to environmental variables. J Mollus Stud 64:123–127. https://doi.org/10.1093/mollus/64.1.123
Suda CNK, Vani GS, de Oliveira MF, Rodrigues E Jr, Rodrigues E, Lavrado HP (2015) The biology and ecology of the Antarctic limpet Nacella concinna. Polar Biol 38:1949–1969. https://doi.org/10.1007/s00300-015-1789-6
Thiriot-Quiévreux C (2003) Advances in chromosomal studies of gastropod molluscs. J Mollus Stud 69:187–202. https://doi.org/10.1093/mollus/69.3.187
Valdovinos C, Rüth M (2005) Nacellidae limpets of the southern end of South America: taxonomy and distribution. Rev Chil Hist Nat 78:497–517. https://doi.org/10.4067/s0716-078x2005000300011
Vitturi R, Rasotto MB, Farinella-Ferruzza N (1982) The chromosomes of 16 molluscan species. Boll Zool 49:61–71. https://doi.org/10.1080/11250008209439373
Von Stetina JR, Orr-Weaver TL (2011) Developmental control of oocyte maturation and egg activation in metazoan models. CSH Perspect Biol 3:a005553. https://doi.org/10.1101/cshperspect.a005553
Acknowledgements
We thank the staff of the Instituto Antártico Argentino for sampling assistance. We acknowledge Dr. Silvia Pietrokovsky who helped in revising the language of the manuscript. Financial support by FONCyT/DNA-IAA under grant PICTO 0091 is gratefully acknowledged.
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Dopchiz, L.P., Ansaldo, M. & Genovese, G. Gonadal histology and gametogenesis of the Antarctic limpet Nacella concinna (Patellogastropoda, Nacellidae) collected at Potter Cove, 25 de Mayo (King George) Island, during austral summer. Polar Biol 41, 1751–1762 (2018). https://doi.org/10.1007/s00300-018-2314-5
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DOI: https://doi.org/10.1007/s00300-018-2314-5