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Reproduction and imposex in the edible snail Adelomelon ancilla from northern Patagonia, Argentina

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Abstract

The edible volutid snail Adelomelon ancilla occurs on the Argentine coast and may have the capacity to serve as source of support for local fisheries. However, knowledge of its reproduction is lacking. Over 3 years (from September 2000 to July 2004) we studied the oviposition at Golfo Nuevo, Patagonia by diving. Monthly collections were performed to examine gonadal stages histologically during 2002–2003. Gamete development stages corresponded with the expected period for oviposition occurring from July to November, a time of increasing day length. Oviposition also took place in March when water temperature attained a maximum of 18°C. Following the spawning period, remaining gametes were resorpted in both sexes. Males contained sperm throughout the year, parasperm and eusperm forms were found within the same acinus. Oogonia/oocytes ranged from 20 to 240 μm in diameter during oogenesis. Females commenced laying egg capsules from a shell length of 114 mm. Reproduction is compared with other fishable volutid snails from the Argentine shelf, and suggests the need to apply certain fishing restrictions if the resource begins to be utilized commercially. The imposex condition was found in snails from some shipping areas. The frequency of this condition declined with distance from the port.

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References

  • Ayçaguer C (2002) Anatomía de las volutas del Atlántico Sudoccidental, I: anatomía general y del sistema reproductor de Zidona dufresnei (Donovan, 1823) (Neogastropoda: Volutidae). Comun Soc Malacol Uruguay 76–77:159–180

    Google Scholar 

  • Barroso CM, Moreira MH, Gibbs PE (2000) Comparison of imposex and intersex development in four prosobranch species for TBT monitoring of a southern European estuarine system (Ria de Aveiro, NW Portugal). Mar Ecol Prog Ser 202:221–232. doi:https://doi.org/10.3354/meps201221

    Article  Google Scholar 

  • Bech M (2002) Imposex and tributyltin contamination as a consequence of the establishment of a marina, and increasing yachting activities at Phuket Islande, Thailand. Environ Pollut 117:421–429. doi:https://doi.org/10.1016/S0269-7491(01)00191-9

    Article  CAS  Google Scholar 

  • Bigatti G (2005) Anatomía, ecología y reproducción del caracol rojo Odontocymbiola magellanica (Gastropoda: Volutidae) en golfos norpatagónicos. PhD thesis, Universidad de Buenos Aires, Argentina, p 178

  • Bigatti G, Carranza A (2007) Phenotypic variability associated with the occurrence of imposex in Odontocymbiola magellanica (Gmelin, 1791) from Golfo Nuevo, Patagonia. J Mar Biol Assoc UK 87:755–759. doi:https://doi.org/10.1017/S0025315407055762

    Article  CAS  Google Scholar 

  • Bigatti G, Ciocco NF (2008) Volutid snails as an alternative resource for artisanal fisheries in northern patagonic gulfs availability and first suggestions for diving catches. J Shellfish Res 27:1–5. doi:https://doi.org/10.2983/0730-8000(2008)27[417:VSAAAR]2.0.CO;2

    Article  Google Scholar 

  • Bigatti G, Penchaszadeh PE (2005) Imposex in Odontocymbiola magellanica (Caenogastropoda:Volutidae) in Patagonia. Comun Soc Malacol Uruguay 9:371–375

    Google Scholar 

  • Bigatti G, Penchaszadeh PE, Cledón M (2007) Age, growth and somatic production in the volutid gastropod Odontocymbiola magellanica from Golfo Nuevo, Patagonia Argentina. Mar Biol 150:1199–1204. doi:https://doi.org/10.1007/s00227-006-0401-6

    Article  Google Scholar 

  • Bigatti G, Marzinelli M, Penchaszadeh PE (2008) Seasonal reproduction and sexual maturity of Odontocymbiola magellanica (Neogastropoda: Volutidae) in Patagonian shallow waters, Argentina. Invertebr Biol 127(3):314–326. doi:https://doi.org/10.1111/j.1744-7410.2008.00139.x

    Article  Google Scholar 

  • Bigatti G, Cledón M, Primost MA, Averbuj A, Theobald N, Gerwinski W, Arntz W, Morriconi E, Penchaszadeh PE (2009a) Contamination by TBT and imposex biomonitoring along 4700 km of Argentinean shoreline (SW Atlantic: from 36°S to 54°S). Mar Pollut Bull 58:695–701. doi:https://doi.org/10.1016/j.marpolbul.2009.01.001

    Article  CAS  Google Scholar 

  • Bigatti G, Sánchez Antelo CJM, Miloslavich P, Penchaszadeh PE (2009b) Adelomelon ancilla: a predator neogastropod in Patagonian benthic communities. Nautilus (in press)

  • Branch GM (1981) The biology of limpets: physical factors, energy flow, and ecological interactions. Oceanogr Mar Biol Ann Rev 19:235–380

    Google Scholar 

  • Bryan GW, Gibbs PE, Hummerstone LG, Burt GR (1986) The decline of the gastropods Nucella Lapillus around south-west England: evidence for the effects of tributyltin from antifouling paints. J Marine Biological Association of the United Kingdom. 67:611–640

    Article  Google Scholar 

  • Buckland-Nicks JA (1973) The fine structure of the spermatozooan of Littorina (Gastropoda: Prosobranchia), with special reference to sperm motility. Z Zellforsch 144:111–129

    Article  Google Scholar 

  • Buckland-Nicks JA (1998) Prosobranch parasperm: sterile germ cells that promote paternity? Micron 29:267–280. doi:https://doi.org/10.1016/S0968-4328(97)00064-4

    Article  Google Scholar 

  • Buckland-Nicks JA, Chia F (1977) On the nurse cell and the Spermatozeugma in Littorina sitkana. Cell Tissue Res 179:347–356. doi:https://doi.org/10.1007/BF00221105

    Article  CAS  Google Scholar 

  • Buckland-Nicks JA, Williams D, Chia F, Fontaine A (1982) The fine structure of the polymorphic spermatozoa of Fusitriton oregonensis (Mollusca: Gastropoda), with notes on the cytochemistry of the internal secretions. Cell Tissue Res 227:235–255. doi:https://doi.org/10.1007/BF00210883

    Article  CAS  Google Scholar 

  • Carranza A (2006) Large gastropods by-catch in the hake fishery at the Argentinean-Uruguayan common fishing zones. Comun Soc Malacol Uruguay 9(89):61–67

    Google Scholar 

  • Chase R (2002) Behavior and its neural control in gastropods molluscs. Oxford, New York, p 311

  • Cledón M, Penchaszadeh PE, Arntz W (2005) Gonadal cycle in an Adelomelon brasiliana (Neogastropoda: Volutidae) population off Buenos Aires province, Argentina. Mar Biol 147:439–445. doi:https://doi.org/10.1007/s00227-005-1588-7

    Article  Google Scholar 

  • Cledón M, Theobald N, Gerwinski W, Penchaszadeh P (2006) Imposex and organotin compounds in marine gastropods and sediments from the Mar del Plata coasts, Argentina. J Mar Biol Assoc UK 86:5211–5215. doi:https://doi.org/10.1017/S002531540601366X

    Article  Google Scholar 

  • Cumplido M (2009) Estacionalidad Reproductiva y desarrollo embrionario del caracol Trophon geversianus en el intermareal de Punta Cuevas, Golfo Nuevo. Degree Thesis. Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB), Argentina 75

  • de Castellanos ZJA, Landoni N (1992) Catálogo descriptivo de la malacofauna marina magallánica, Neogastropoda, Volutidae, Volutomitridae, Cancellariidae, Olividae y Marginellidae. Consejo Investigaciones Científicas de la Provincia de Buenos Aires. Fasc 10:43

    Google Scholar 

  • Delucchi F, Tombesi NB, Freije RH, Marcovecchio JE (2007) Butyltin compounds in sediments of the Bahía Blanca Estuary, Argentina. Environ Monit Assess 132(1–3):445–451. doi:https://doi.org/10.1007/s10661-006-9547-4

    Article  CAS  Google Scholar 

  • FAO (2002) Capture production. FAO Yearb Fish Stat 94(1)

  • Gibbs PE, Bryan GW (1994) Biomonitoring of tributyltin (TBT) pollution using the imposex response of neogastropod molluscs. In: Kramer JM (ed) Biomonitoring of coastal waters and estuaries, Kees. CRC Press, Boca Raton

    Google Scholar 

  • Gibbs PE, Bryan GW, Pascoe PL, Burt GR (1987) The use of the the dog-whelk Nucella lapillus as an indicator of tributyltin (TBT) contamination. J Mar Biol Assoc UK 67:507–523

    Article  CAS  Google Scholar 

  • Gibbs PE, Bryan GW, Pascoe PL, Burt GR (1990) Reproductive abnormalities in female Ocenebra erinacea (Gastropda) resulting from tributyltin-induced imposex. J Mar Biol Assoc UK 70:639–656

    Article  Google Scholar 

  • Gibbs PE, Bryan GW, Pascoe PL (1991) TBT-induced imposex in the dogwhelk, Nucella lapillus: geographical uniformity of the response and effects. Mar Environ Res 32:79–87. doi:https://doi.org/10.1016/0141-1136(91)90035-7

    Article  CAS  Google Scholar 

  • Giese AC, Pearse JS (1974) Introduction: general principles. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates, vol 1. Academic, New York, pp 1–49

    Google Scholar 

  • Giménez J, Penchaszadeh PE (2002) Reproductive cycle of Zidona dufresnei. Mar Biol 140:755–761. doi:https://doi.org/10.1007/s00227-001-0748-7

    Article  Google Scholar 

  • Giménez J, Lasta C, Bigatti G, Penchaszadeh P (2005) Exploitation of the volute snail Zidona dufresnei in argentine waters, Southwestern Atlantic Ocean. J Shellfish Res 24:1135–1140

    Article  Google Scholar 

  • Giménez J, Healy J, Hermida G, Lo Nostro F, Penchaszadeh P (2008) Ultrastructure and potential taxonomic importance of euspermatozoa and paraspermatozoa in the volutid gastropods Zidona dufresnei and Provocator mirabilis (Caenogastropoda, Mollusca). Zoomorphology 127:161–173. doi:https://doi.org/10.1007/s00435-008-0060-x

    Article  Google Scholar 

  • Goldberg RN, Averbuj A, Cledón M, Luzzatto D, Sbarbati N (2004) Search for triorganotins along the Mar del Plata (Argentina) marine coast: finding of tributyltin in egg capsules of a snail Adelomelon brasiliana (Lamarck, 1822)[sic] population showing imposex effects. Appl Organomet Chem 18:117–123. doi:https://doi.org/10.1002/aoc.590

    Article  CAS  Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M, Morita M (1994) Imposex and organotin compounds in Thais clavigera and T. Bronni in Japan. J Mar Biol Assoc UK 74:651–669

    Article  CAS  Google Scholar 

  • King N, Miller MC, de Mora SJ (1989) Tributyltin levels for seawater, sediement and selected marine species in coastal Northland and Auckland, New Zeland. NZ J Mar Freshw Res 23:287–294

    Article  CAS  Google Scholar 

  • Krone CA, Brown DW, Burrows DG, Chan S-L, Varanasi U (1989) Butyltin in sediments from marinas and waterways in Puget Sound, Washington State, USA. Mar Pollut Bull 20:528–531. doi:https://doi.org/10.1016/0025-326X(89)90142-2

    Article  CAS  Google Scholar 

  • Lasta ML, Roux A, Bremec C (2000) Caracoles marinos de interés pesquero. Moluscos gasterópodos volútidos. INIDEP Informe técnico 31:1–13

    Google Scholar 

  • Maguire RJ, Tkacz RJ, Chau YK, Bengert GA, Wong PTS (1986) Occurrence of organotin compounds in water and sediment in Canada. Chemosphere 15:253–274. doi:https://doi.org/10.1016/0045-6535(86)90020-2

    Article  CAS  Google Scholar 

  • Melone G, Lora Lamia Donin D, Cotelli F (1978) Aspetti ultrastrutturali degli spermatozoi atypici in Scalidae (Gastropoda, Prosobranchia). Boll Zool 45:261–268

    Article  Google Scholar 

  • Minchin D (2003) Monitoring of tributyl tin contamination in six marine inflets using biological indicators. Mar Environ Health Ser 6:1–15

    Google Scholar 

  • Minchin D, Stroben E, Oehlmann J, Bauer B, Duggan CB, Keatinge M (1996) Biological indicators used to map organotin contamination in Cork Harbour, Ireland. Mar Pollut Bull 32:188–195. doi:https://doi.org/10.1016/0025-326X(95)00120-C

    Article  CAS  Google Scholar 

  • Narvarte MA (2006) Biology and fishery of the whelk Buccinanops globulosum (Kiener, 1834) in northern coastal waters of the San Matías Gulf (Patagonia, Argentina). Fish Res 77:131–137. doi:https://doi.org/10.1016/j.fishres.2005.11.006

    Article  Google Scholar 

  • Oehlmann J (1994) Imposex bei Muriciden (Gastropoda, Prosobranchia). Eine ökotoxikologische Untersuchung zu TBTEffekten, Cuvillier Verlag Göttingen, p 167

    Google Scholar 

  • Oehlmann J, Fioroni P, Stroben E, Markert B (1996) Tributyltin (TBT) effects on Ocinebrina aciculata (Gastropoda: Muricidae): imposex development, sterilization, sex change and population decline. Sci Total Envir 188:205–223

    Article  CAS  Google Scholar 

  • Oehlmann J, Bauer B, Minchin D, Schulte-Oehlmann U, Fioroni P, Markert B (1998) Imposex in Nucella lapillus and intersex in Littorina littorea: interspecific comparison of two TBT-induced effects and their geographical uniformity. Hydrobiologia 378:199–213. doi:https://doi.org/10.1023/A:1003218411850

    Article  Google Scholar 

  • Osorio C (2002) Moluscos Marinos en Chile. Especies de Importancia Económica. Facultad de Ciencias, Universidad de Chile

  • Penchaszadeh PE, Miloslavich P, Lasta M, Costa PMS (1999) Egg capsules in the genus Adelomelon (Caenogastropoda: Volutidae) from the Atlantic coast of South America. Nautilus 113(2):56–63

    Google Scholar 

  • Shim WJ, Hong SH, Yim UH, Kim NS, Oh JR (2002) Horizontal and vertical distribution of butyltin compounds in sediments from shipyards in Korea. Arch Environ Contam Toxicol 43:277–283. doi:https://doi.org/10.1007/s00244-002-0156-0

    Article  CAS  Google Scholar 

  • Smith BS (1981) Male characteristics on female mud snails Nassarius obsoletus = Ilyanassa obsoleta. J Appl Toxicol 1:15–21. doi:https://doi.org/10.1002/jat.2550010105

    Article  CAS  Google Scholar 

  • Stroben E, Oehlmann J, Fioroni P (1992) The morphological expression of imposex in Hinia reticulata (Gastropoda: Buccinidae): a potential indicator of tributultin. Mar Biol 13:625–636. doi:https://doi.org/10.1007/BF00349706

    Article  Google Scholar 

  • Underwood AJ (1979) The ecology of intertidal gastropods. Adv Mar Biol 16:111–210. doi:https://doi.org/10.1016/S0065-2881(08)60293-X

    Article  Google Scholar 

  • Zabala S (2007) Espermatogénesis y morfología del espermatozoide en el caracol Adelomelon ancilla (Caenogastropoda; Volutidae). Degree Thesis, Universidad de Buenos Aires (UBA), Argentina 72

  • Zabala S, Hermida G, Giménez J (2009) Ultrastructure of euspermatozoa and paraspermatozoa in the volutid snail Adelomelon ancilla (Mollusca; Caenogastropoda). Helgol Mar Res. doi:https://doi.org/10.1007/s10152-009-0145-z

    Article  Google Scholar 

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Acknowledgments

Special thanks to Eugenia and Victoria Zavattieri and Oscar Wheeler for sampling and field assistance. Fabián Tricárico (MACN) and Isabel Farías helped with SEM. Miguel Angel Diaz, Julio Rúa, Ricardo Vera, Nestor Ortiz and Fabián Quiroga also helped in field activities and Katherine Noble helped improving the English version of this manuscript. This project was partially support by PIP 5301, UBACyT 171 and PICT 01869 Redes.

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Authors and Affiliations

  1. Facultad de Ciencias Exactas y Naturales, Museo Argentino de Ciencias Naturales Bernardino Rivadavia, CONICET, Universidad de Buenos Aires, Av. Ángel Gallardo 470, Buenos Aires, Argentina

    Pablo E. Penchaszadeh & Carlos Sánchez Antelo

  2. Centro Nacional Patagónico CENPAT, CONICET, Blvd Brown 2915, U9120ACV, Puerto Madryn, Chubut, Argentina

    Soledad Zabala & Gregorio Bigatti

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  1. Pablo E. Penchaszadeh
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  2. Carlos Sánchez Antelo
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  3. Soledad Zabala
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  4. Gregorio Bigatti
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Correspondence to Gregorio Bigatti.

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Communicated by M. Byrne.

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Penchaszadeh, P.E., Antelo, C.S., Zabala, S. et al. Reproduction and imposex in the edible snail Adelomelon ancilla from northern Patagonia, Argentina. Mar Biol 156, 1929–1939 (2009). https://doi.org/10.1007/s00227-009-1225-y

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