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Reproduction and sex reversal of the solitary vermetid gastropod Serpulorbis arenarius

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Abstract

The reproductive biology of the Mediterranean vermetid gastropod Serpulorbis arenarius, a subtidal sessile solitary species that lives in shady rocky communities, was studied at two localities south-east of the Iberian Peninsula. Its population density is usually low, with specimens sometimes sparsely distributed. Its shell often appears to be covered by epibiotic organisms. The sex ratio is biased toward males (63%) in the populations of SE Spain, and the results point towards hermaphroditism with alternating sexuality. The results obtained suggest that all specimens are first males, change to females under some as yet unknown condition and, after the ovogenesis cycle has been completed, revert to the original sexual state (male). The possible adaptive forces that favour hermaphroditism in this species are discussed, and we hypothesise that the seizure of a spermatophore by males may stimulate sex change to female. Brooding females (51% of females studied) were found from March to December. In males, histological study of testes revealed that spermatogenesis seems to occur throughout the year. Females brooded between 5 and 28 (x̄=15) egg capsules, which were attached by stalks to the inner surface of the shell. It is noteworthy that the gonads of two of the specimens brooding egg capsules were developing testes. The newly laid egg capsules were filled with an organic intracapsular matrix, in which 40–153 (x̄=94) eggs were embedded. The mean diameter of the uncleaved ova was 352.5 µm. The organic intracapsular matrix and some nurse eggs were used as an extra-embryonic food source. Hatching occurred at an advanced veliger stage, immediately followed by metamorphosis. Therefore, the larval development of S. arenarius is of a lecithotrophic intracapsular type, with a short, free-swimming/crawling phase.

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References

  • Ankel WE (1936) Prosobranchia. In: Grinpe G, Wagler E (eds) Die Tierwelt der Nord- und Ostsee. Akademische Verlagsgesellschaft, Leipzig, pp 1–240

  • Barash A, Zenziper Z (1985) Structural and biological adaptations of Vermetidae (Gastropoda). Boll Malacol 21:145–176

    Google Scholar 

  • Bieler R, Hadfield MG (1990) Reproductive biology of the sessile gastropod Vermicularia spirata (Cerithioidea: Turritellidae). J Molluscan Stud 56:205–219

    Google Scholar 

  • Bieler R, Mikkelsen PM (1988) Anatomy and reproductive biology of two western Atlantic species of Vitrinellidae, with a case of protandrous hermaphroditism in Rissoacea. Nautilus 102:1–29

    Google Scholar 

  • Boettger CR (1930) Studien zur Physiologie der Nahrungsaufnahme festgewachsener Schnecken. Die Ernährung der Wurmschnecke Vermetus. Biol Zentbl 50:581–598

    Google Scholar 

  • Branch GM (1974) The ecology of Patella oculus from the Cape Peninsula, South Africa. Reproductive cycles. Trans R Soc South Africa 41:111–165

    Google Scholar 

  • Breitburg DL (1985) Development of a subtidal epibenthic community: factors affecting species composition and the mechanisms of succession. Oecologia 65:173–184

    Article  Google Scholar 

  • Calvo M, Templado C (2004) Reproduction and development of the vermetid gastropod Vermetus triquetrus. Invertebr Biol 123:289–303

    Google Scholar 

  • Calvo M, Templado J, Penchaszadeh P (1998) Reproductive biology of the gregarious Mediterranean vermetid gastropod Dendropoma petraeum. J Mar Biol Assoc UK 78:525–549

    Google Scholar 

  • Carrick N (1980) Aspects of the biology of Gazameda gunni (Reeve, 1849), a viviparous mesogastropod and potential “indicator” of perturbation induced by sewage pollution. J Malacol Soc Aust 4:254–255

    Google Scholar 

  • Charnov E, Bull JJ (1989) Non-Fisherian sex ratios with sex change and environmental sex determination. Nature 338:148−150

    Article  Google Scholar 

  • Chen MH, Soong K (2002) Estimation of age in the sex-changing, coral-inhabiting snail Coralliophila violacea from the growth striae on opercula and mark–recapture experiments. Mar Biol 140:337–342

    Article  Google Scholar 

  • Chen MH, Yang YW, Soong K (1998) Preliminary observations on change of sex by the coral inhabiting snail Coralliophila violacea (Lamark) (Gastropoda: Coralliophilidae). J Exp Mar Biol Ecol 230:207–212

    Article  Google Scholar 

  • Choquet M (1966) Biologie de Patella vulgata L. dans le Boulonnais. Cah Biol Mar 7:1–22

    Google Scholar 

  • Collin R (1995) Sex, size, and position: a test of models predicting size at sex change in the protandrous gastropod Crepidula fornicata. Am Nat 146:815–831

    Article  Google Scholar 

  • Collin R (2000) Sex change, reproduction and development of Crepidula adunca and Crepidula lingulata (Gastropoda: Calyptraeidae). Veliger 43:24–33

    Google Scholar 

  • Creese RG, Schiel DR, Kingsford MJ (1990) Sex change in a giant endemic limpet Patella kermadecensis, from the Kermedec Islands. Mar Biol 104:419–426

    Google Scholar 

  • Fretter V, Graham A, Ponder WF, Lindberg DR (1998) Prosobranchia. Introduction. In: Beesley PL, Ross GJB, Wells A (eds) Mollusca, the southern synthesis, part B. Fauna of Australia, vol 5. CSIRO Publishing, Melbourne, pp 605–638

  • Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208

    Article  CAS  PubMed  Google Scholar 

  • Hadfield MG (1966) The reproductive biology of the Californian vermetid gastropods Serpulorbis squamigerus (Carpenter, 1857) and Petaloconchus montereyensis Dall, 1919. PhD dissertation, Standford University, Palo Alto, Calif., USA

  • Hadfield MG (1970) Observations on the anatomy and biology of two California Vermetid gastropods. Veliger 12:301–309

    Google Scholar 

  • Hadfield MG, Hopper CN (1980) Ecological and evolutionary significance of pelagic spermatophores of vermetid gastropods. Mar Biol 57:315–325

    Article  Google Scholar 

  • Haszprunar G (1988) On the origin and evolution of major gastropod groups, with special reference to the Streptoneura. J Molluscan Stud 54:367–441

    Google Scholar 

  • Healy JM (1988) Sperm morphology in Serpulorbis and Dendropoma and its relevance to the systematic position of the Vermetidae (Gastropoda). J Molluscan Stud 54:295–308

    Google Scholar 

  • Heller J (1993) Hermaphroditism in molluscs. Biol J Linn Soc 48:19–42

    Article  Google Scholar 

  • Hoagland KE (1978) Protandry and evolution of environmentally mediated sex change: a study of the Mollusca. Malacologia 17:365–391

    Google Scholar 

  • Hoagland KE (1984) Use of terms protandry, protogyny, and hermaphroditism in malacology. Am Malacol Bull 3:85–88

    Google Scholar 

  • Hoagland KE (1986) Patterns of encapsulation and brooding in the Calyptraeidae (Prosobranchia: Mesogastropoda). Bull Am Malacol Union Inc 4:173–183

    Google Scholar 

  • Houbrick RS (1990) Anatomy, reproductive biology and systematic position of Fossarus ambiguus (Linné) (Fossarinae: Planaxidae: Prosobranchia). Açoreana [Suppl]:October:59–73

  • Joose J, Geraerts PM (1983) The Molluscan. In: Saleuddin ASM, Wilbur KM (ed) The Mollusca physiology, vol 4. Academic, New York, pp 318–406

  • Kennedy JJ (1995) The courtship, pseudo-copulation behaviour and spermatophore of Turritella communis Risso, 1826 (Prosobranchia: Turritellidae). J Molluscan Stud 61:421–434

    Google Scholar 

  • Laursen D (1953) The genus Ianthina: a monograph. Dana Rep 38:1–40

    Google Scholar 

  • Lützen J (1972) Studies on parasitic gastropods from echinoderms. II. On Stilifer Broderip, with special reference to the structure of the sexual apparatus and the reproduction. Biol Skr 19:1–18

    Google Scholar 

  • Mann T (1984) Spermatophores: development, structure, biochemical attributes and role in the transfer of spermatozoa. Zoophysiology, vol 15. Springer, Berlin New York Heidelberg

  • Melone G (1986) Sex changes in Opalia crenata (L.) (Gastropoda: Epitoniidae). In: Heppell D (ed) Abstr 9th Int Malacol Congr. National Museum of Scotland, Edinburgh, p 54

  • Miloslavich P, Penchaszadeh PE (1992) Reproductive biology of Vermetus sp. and Dendropoma corrodens (Orbigny, 1842): two vermetid gastropods from the southern Caribbean. Veliger 35:78–88

    Google Scholar 

  • Morton JE (1951) The structure and adaptation of the New Zealand Vermetidae, part I. The genus Serpulorbis. Trans R Soc NZ 79:1–12

    Google Scholar 

  • Morton JE (1965) Form and function in the evolution of the Vermetidae. Bull Br Mus (Nat Hist) Zool 11:585–630

    Google Scholar 

  • Nelson BV (1982) The adaptive significance of aggregation and hermaphroditism in the sessile gastropod Serpulorbis imbricatus. Diss Abstr Int Sect B Phys Sci Technol 43:971

    Google Scholar 

  • Nishiwaki S (1964) Phylogenetic study on the type of the dimorphic spermatozoa in Prosobranchia. Sci Rep Tokyo Kyoiku Daigaku Sect B 11:238–275

    Google Scholar 

  • Nishiwaki S (1969) Seasonal size variations of the pallial slit in female Serpulorbis imbricatus (Prosobranchia, Vermetidae). Sci Rep Tokyo Kyoiku Daigaku Sect B 14:69–78

    Google Scholar 

  • Nordsieck F, García-Talavera F (1979) Moluscos marinos de Canarias y Madeira (Gastropoda). Aula de Cultura de Tenerife, Tenerife

  • Osman RW (1987) Interactions between the vermetid Serpulorbis squamigerus (Carpenter) and several species of encrusting bryozoans. J Exp Mar Biol Ecol 111:267–284

    Article  Google Scholar 

  • Pasteur-Humbert C (1962) Les mollusques marins testacés du Maroc. Catalogue non critique. I. Les Gastéropodes. Trav Inst Sci Cherifien Fac Sci Rabat Sér Zool 23:1–245

    Google Scholar 

  • Ponder WF (1994) The anatomy and relationships of three species of vitrinelliform gastropods (Caenogastropoda: Rissooidea) from Hong Kong. In: Morton B (ed) The malacofauna of Hong Kong and southern China. Hong Kong University Press, Hong Kong, pp 243–281

  • Ponder WF (1998) Superfamily Vanikoroidea. In: Beesley PL, Ross GJB, Wells A (eds) Mollusca, the southern synthesis, part B. Fauna of Australia, vol 5. CSIRO Publishing, Melbourne, pp 769–772

  • Reid DG (1986) Mainwaringia Nevill, 1885, a littorinid genus from Asiatic mangrove forests, and a case of protandrous hermaphroditism. J Molluscan Stud 52:225–242

    Google Scholar 

  • Richter A, Luque AA (2004) Sex change in two Mediterranean species of Coralliophilidae (Mollusca: Gastropoda: Neogastropoda). J Mar Biol Assoc UK 84:1–10

    Google Scholar 

  • Rivest BR (1983) Development and the influence of nurse egg allotment on hatching size in Searlesia dira (Reeve, 1846) (Prosobranchia: Buccinidae). J Exp Mar Biol Ecol 69:217–241

    Article  Google Scholar 

  • Scheuwimmer A (1979) Sperm transfer in the sessile gastropod Serpulorbis (Prosobranchia: Vermetidae). Mar Ecol Prog Ser 1:65–70

    Google Scholar 

  • Scheuwimmer A, Nishiwaki S (1982) Comparative studies on three Japanese species of Serpulorbis (Prosobranchia: Vermetidae) with description of a new species. Venus 41:85–101

    Google Scholar 

  • Schiaparelli S (1996) Contribution to the knowledge of Vermetidae (Mollusca: Gastropoda) from Ligurian Sea. Boll Malacol 31:267–276

    Google Scholar 

  • Simone LRL (2001) Phylogenetic analyses of Cerithioidea (Mollusca, Caenogastropoda) based on comparative morphology. Arq Zool (Sao Paulo) 36:147–263

    Google Scholar 

  • Soong K, Chen MH (2003) Sex expression of an immobile coral-inhabiting snail, Quoyula monodonta. Mar Biol 143:351–358

    Article  Google Scholar 

  • Spight T (1976) Hatching size and the distribution of nurse eggs among prosobranch embryos. Biol Bull (Woods Hole) 150:491–499

    Google Scholar 

  • Templado J, Calvo M (ed) (2002) Flora y fauna de la Reserva Marina de las islas Columbretes. Secretaría General de Pesca Marítima, Ministerio de Agricultura, Pesca y Alimentación, Madrid

  • Tochimoto T (1967) Comparative histochemical study on the dimorphic spermatozoa of the Prosobranchia with special reference to polysaccharides. Sci Rep Tokyo Kyoiko Daigaku Sect B 13:75–109

    Google Scholar 

  • Warén A (1980) Sexual strategies in Eulimidae (Prosobranchia). J Malacol Soc Aust 4:231

    Google Scholar 

  • Warén A (1983) A generic revision of the family Eulimidae (Gastropoda: Prosobranchia). J Molluscan Stud [Suppl]13:1–96

    Google Scholar 

  • Warén A, Bouchet P (1991) Mollusca Gastropoda: systematic position and revision of Haloceras Dall, 1889 (Caenogastropoda, Haloceratidae fam. nov.). In: Crosnier A, Bouchet P (eds) Résult Camp Musorstom, vol 7. Mem Mus Natl Hist Nat Ser A Zool 150:111–161

    Google Scholar 

  • Warner RR (1988) Sex change and size-advantage model. Trends Ecol Evol 3:133–140

    Article  Google Scholar 

  • Warner RR, Fitch DL, Standish JD (1996) Social control of sex change in the shelf limpet, Crepidula norrisiarum: size-specific responses to local group composition. J Exp Mar Biol Ecol 204:155–167

    Article  Google Scholar 

  • Wright WG (1989) Intraspecific density mediates sex change in the territorial patellacean limpet Lottia gigantea. Mar Biol 100:353–364

    Article  Google Scholar 

  • Yonge C, Iles EJ (1939) On the mantle cavity, pedal gland and evolution of mucus feeding in Vermetidae. Ann Mag Nat Hist 3:536–555

    Google Scholar 

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Acknowledgements

We are much indebted to J. Bedoya (recently deceased) for his technical assistance with scanning electron microscopy at the MNCN, and to J. Fernandez for technical support. P. Penchaszadeh made helpful comments and suggestions in the early phases of the work. We are also indebted to A. Ritcher and S. Schiaparelli, who revised the final version, and G. Giribet, who corrected the English text and suggested improvements. The first author was sponsored by a postdoctoral grant from the Community of Madrid. This work has been partially funded by the projects REN2001-1965-C17-08/GLO and REN2000-0890/GLO of the Spanish Ministry of Science and Technology.

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  1. Museo Nacional Ciencias Naturales (CSIC), Jose Gutierrez Abascal 6, 28006, Madrid, Spain

    M. Calvo & J. Templado

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Correspondence to M. Calvo.

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Communicated by O. Kinne, Oldendorf/Luhe

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Calvo, M., Templado, J. Reproduction and sex reversal of the solitary vermetid gastropod Serpulorbis arenarius. Marine Biology 146, 963–973 (2005). https://doi.org/10.1007/s00227-004-1490-8

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