Shell and body structure of the plesiomorphic pulmonate marine limpet Siphonaria pectinata (Linnaeus, 1758) from Portugal (Gastropoda: Heterobranchia: Siphonariidae)

Luiz Ricardo L. Simone, e-mail:;

Museu de Zoologia da Universidade de São Paulo, 04299-970, Cx. Postal 4249 São Paulo, Brazil

Maria Inês G. L. Seabra, e-mail:

Laboratório de Ciências do Mar (CIEMAR) MARE-Centro de Ciências do Mar e do Ambiente, Universidade de Évora, Apartado 190, 7520-903 Sines, Portugal

The shell and body structure of the plesiomorphic pulmonate false-limpet Siphonaria pectinata (Linnaeus) from the south coast of Portugal is presented in detail. All the systems are described and discussed, in order to create a phenotypic database, since the siphonariid relationships are controversial, and most of the recent attempts at their resolution have been molecular. Most siphonariids show several morphological peculiarities (e.g., flap-like head without tentacles, interrupted shell muscle, anterior portion of genitalia surrounding shell muscle) compared to the remaining pulmonates or even to heterobranchs. On the other hand, the odontophore structure, and the genital system, including the penis retractor muscle connected with the shell muscle, place them close to higher pulmonates. The siphonariids present a new mode of limpetisation, with the visceral structures placed inside the haemocoel instead of being located below the shell apex

Key words
morphology; anatomy; somatic evolution; limpetisation; systematics; comparative biology

Allanson B. R. 1958. On the systematics and distribution of the molluscan genus Siphonaria in South Africa. Hydrobiologia 12: 149–180.
Alvin J., Simone L. R. L., Pimenta A. D. 2014. Taxonomic review of the genus Pleurobranchaea (Gastropoda: Pleurobranchoidea) from Brazil, with description of a new species. J. Mollus. Stud. 80: 604–623.
Black R., Lymbery A., Hill A. 1988. Form and function: size of radular teeth and inorganic content of faeces in a guild of grazing molluscs at Rottnest Island, Western Australia. J. Exp. Mar. Biol. Ecol. 121: 23–35.
Chambers R. J., McQuaid C. D. 1994a. Notes on the taxonomy, spawn and larval development of South African species of the intertidal limpet Siphonaria (Gastropoda: Pulmonata). J. Mollus. Stud. 60: 263–275.
Chambers R. J., McQuaid C. D. 1994b. A review of larval development in the intertidal limpet genus Siphonaria (Gastropoda: Pulmonata). J. Mollus. Stud. 60: 415–423.
Cooke A. H. 1911. A modification in the form of the shell of Siphonaria algesirae Quoy apparently due to locality. Proc. Malac. Soc. London 9: 6.
Costa P. M. S, Simone L. R. L. 2006. A new species of Lucapina from Canopus Bank, N.E. Brazil (Vetigastropoda, Fissurellidae). Strombus 13: 1–5.
Cottrell A. J. 1910. Anatomy of Siphonaria obliquata (Sowerby). Trans. Proc. R. Soc. N. Z. 43: 582–594.
Cottrell A. J. 1911. Vascular system of Siphonaria obliquata Sowerby. Trans. Proc. R. Soc. N. Z. 44: 374–379.
Dall W. H. 1870. Remarks on the anatomy of the genus Siphonaria, with a description of a new species. Amer. J. Conchol. 6: 30–41, pls 4–5.
Dayrat B., Conrad M., Balayan S., White T. R., Albrecht C., Golding R. E., Gomes S. R., Harasewych M. G., Martins A. M. F. 2011. Phylogenetic relationships and evolution of pulmonate gastropods (Mollusca): New insights from increased taxon sampling. Mol. Phylo­genet. Evol. 59: 425–437.
Dayrat B., Goulding T. C., White T. R. 2014. Diversity of Indo-West Pacific Siphonaria (Mollusca: Gastropoda: Euthyneura). Zootaxa 3779: 246–276.
Dinapoli A., Zinssmeister C., Klussmann-Kolb A. 2011. New insights into the phylogeny of the Pyramidellidae. J. Mollus. Stud. 77: 1–7.
Giribet G. 2015. Morphology should not be forgotten in the era of genomics – a phylogenetic perspective. Zool. Anz. 256: 96–103.
Giribet G., Kawauchi G. Y. 2016. How many species of Siphonaria pectinata (Gastropoda: Heterobranchia) are there? J. Mollus. Stud. 82: 137–143.
Grahame J., Branch G. M. 1985. Reproductive patterns of marine invertebrates. Oceanogr. Mar. Biol. Annu. Rev. 23: 373–398.
Grande C., Templado J., Cervera J. L., Zardoya R. 2004. Molecular phylogeny of Euthyneura (Mollusca: Gastropoda). Mol. Biol. Evol. 21: 303–313.
Grande C., Templado J., Zardoya R. 2008. Evolution of gastropod mitochondrial genome arrangements. BMC Evol. Biol. 8: 61.
Güller M., Zelaya, D. G., Ituarte C. 2016. How many Siphonaria species (Gastropoda: Euthyneura) live in Southern South America? J. Mollus. Stud. 82: 80–96.
Haller B. 1893. Die Anatomie von Siphonaria gigas, Less., eines opisthobranchien Gastropoden. Arb. Zool. Inst. Univ. Wien 10: 71–100.
Haszprunar G. 1985. The Heterobranchia – a new concept of the phylogeny of the higher Gastropoda. Z. Zool. Syst. Evol. 23: 15–37.
Hodgson A. N. 1999. The biology of siphonariid limpets (Gastropoda: Pulmonata). Oceanogr. Mar. Biol. Annu. Rev. 37: 245–314.
Hubendick B. 1946. Systematic monograph of the Patelli­formia. K. Sven. Vetensk. Akad. Handl. 23: 5–93.
Hubendick B. 1955. On a small quantity of Siphonaria material from Queensland. Mem. Nat. Mus. Victoria 19: 126–136.
Hubendick B. 1957. Phylogenie and Tiergeographie der Siphonariidae. Zur Kenntnis der Phylogenie in der Ordnung Basommataphora and des Ursprungs der Pulmonatengruppe. Zool. Bidr. Upps. 24: 1–216.
Hutton F. W. 1882. On the New Zealand Siphonariidae. Trans. Proc. N. Z.. Inst. 15: 141–145.
Jablonski D., Lutz R. A. 1983. Larval ecology of marine benthic invertebrates: paleobiological implications. Biol. Rev. 58: 21–89.
Jensen K. R. 2011. Comparative morphology of the mantle cavity organs of shelled Sacoglossa, with a discussion of relationships with other Heterobrancha. Thalassas 27: 169–192.
Kawauchi G. Y., Giribet G. 2011. On the amphi-­Atlantic Siphonaria pectinata (Linnaeus, 1758) (Gastropoda: Heterobranchia: Siphonariidae), invades from the East or endemic? J. Mollus. Stud. 77: 196–201.
Knox G. A. 1955. The development of Kerguelenella stewartiana (Powell) (Gastropoda: Siphonariidae). Pac. Sci. 9: 85–98.
Klussmann-Kolb A., Dinapoli A., Kuhn K., Streit B., Albrecht C. 2008. From sea to land and beyond – new insights into the evolution of euthyneuran Gastropoda (Mollusca). BMC Evol. Biol. 8: 57.
Köhler A. 1894. Beiträge zur Anatomie der Gattung Siphonaria. Zool. Jahrb. Abt. Anat. 7: 1–92.
Leal J. H., Simone L. R. L. 1998. Propilidium curumim, a new species of Lepetidae (Gastropoda, Patellogastropoda) from off Southern and Southeastern Brazil. Bull. Mar. Sci. 63: 157–165.
Leal J. H., Simone L. R. L. 2000. Copulabyssia riosi, a new deep-sea limpet (Gastropoda: Pseudococculinidae) from the continental slope off Brazil with comments on the systematics of the genus. Nautilus 114: 59–68.
Marcus E., Marcus E. 1960. On Siphonaria hispida. Bol.  Fac.  Filos.  Univ.  São  Paulo, Zool. 260: 107–140.
Marcus E., Marcus E. 1970. Opisthobranchs from Curaçao and faunistically related regions. Stud. Fauna Curaçao Carib. Isl. 33: 1–129.
Marshall B. A. 1981. The genus Williamia in the western Pacific (Mollusca: Siphonariidae). N. Z.. J. Zool. 8: 487–492.
McQuaid C. D., Cretchley R., Rayner J. L. 1999. Chemical defence of the intertidal pulmonate limpet Siphonaria capensis (Quoy & Gaimard) against natural predation. J. Exp. Mar. Biol. Ecol. 237:141–154.
Morton J. E. 1955. The functional morphology of the British Ellobiidae (Gastropoda Pulmonata) with special reference to the digestive and reproductive systems. Philos. Trans. Roy. Soc. B 239: 89–160.
Murty K. V. R., Shameem A., Umadevi K. 2013. Feeding, anatomy and digestive enzymes of false limpet Siphonaria guamensis. World J. Fish Mar. Sci. 5: 104–109.
Ocaña T. M. J. 2003. Growth, mortality and longevity in two populations of Siphonaria pectinata (Pulmonata) at Gibraltar. J. Mollus. Stud. 69: 162–164.
Ocaña T. M. J., Fa D. A. 2003. Microalgal availability and consumption by Siphonaria pectinata (L., 1758) on a rocky shore. Bol. Inst. Esp. Oceonogr. 19: 65–73.
Pal P. 2007. Fine structure of reproductive glands in two primitive marine pulmonates (Basommatophora: Siphonariidae). Acta Zool. 88: 145–152.
Pal P., Hodgson A. N. 2002. An ultrastructural study of oogenesis in a planktonic and direct-developing species of Siphonaria (Gastropoda: Pulmonata). J. Mollus. Stud. 68: 337–344.
Pal P., Hodgson A. N. 2003. The structure of the egg ribbons of a planktonic and intracapsular developing siphonariid limpet (Gastropoda: Pulmonata). Invertebr. Reprod. Dev. 43: 243–253.
Pal P., Hodgson A. N. 2005. Reproductive seasonality and simultaneous hermaphroditism in two species of Siphonaria (Gastropoda: Pulmonata) from the southern coast of South Africa. J. Mollus. Stud. 71: 33–40.
Paul M. C., Zubía E., Ortega M. J., Salvá J. 1997. New polypropionates from Siphonaria pectinata. Tetrahedron 56: 2303–2308.
Pinchuck S. C., Hodgson A. N. 2009. Comparative structure of the lateral pedal defensive glands of three species of Siphonaria (Gastropoda: Basommatophora). J. Mollus. Stud. 75: 371–380.
Ruthensteiner B. 2006. Redescription and 3D morphology of Williamia gussonii (Gastropoda: Siphonariidae. J. Mollus. Stud. 72: 327–336.
Ruthensteiner B., Lobbe E., Schopf S. 2007. Genital system development of Williamia radiata (Gastropoda, Siphonariidae). Zoomorphology 126: 17–29.
Ruthensteiner B., Stocker B. 2009. Genital ­system anatomy and development of Ovatella myositis by three-dimensional computer visualization. Acta Zool. 90: 166–178.
Saleuddin A. S. M., Ashton M. L., Khan H. R. 1997. An electron microscopic study of the endocrine dorsal bodies in reproductively active and inactive Siphonaria pectinata (Pulmonata: Mollusca). Tissue Cell 29: 267–275.
San-Martín A., Rovirosa J., Gaeta K., Olea A., Ampuero J. 2009. Mantle defensive response of marine pulmonate Trimusculus peruvianus. J. Exp. Mar. Biol. Ecol. 376: 43–47.
Schrödl M. 2014. Opinion: time to say “Bye-bye Pulmonata”? Spixiana 37: 161–164.
Simone L. R. L. 1996. Addisonia enodis, a new species of Addisoniidae (Mollusca, Archaeogastropoda) from the southern Brazilian coast. Bull. Mar. Sci. 58: 775–785.
Simone L. R. L. 1998. Morphological study on Littorina flava (King & Broderip) from Brazil (Caenogastropoda, Littorinidae). Rev. Bras. Zool. 15: 875–887.
Simone L. R. L. 2002. Comparative morphological study and phylogeny of representatives of the superfamily Calyptraeoidea (including Hipponicoidea) (Mollusca, Caenogastropoda). Biota Neotropica 2: 1–137.
Simone L. R. L. 2008. A new species of Fissurella from São Pedro e São Paulo Archipelago, Brazil (Vetigastropoda, Fissurellidae). Veliger 50: 292–304.
Simone L. R. L. 2011. Phylogeny of the Caenogastropoda (Mollusca), based on comparative morphology. Arq. Zool. 42: 161–323.
Simone L. R. L., Bunioto T. C., Avelar W. A. P., Hayashi C. 2012. Morphology and biological aspects of Gundlachia ticaga from S.E. Brazil (Gastropoda: Basommatophora: Ancylidae). Arch. Molluskenkd. 141: 21–30.
Simone L. R. L., Cunha C. M. 2003. Pseudococculina rimula, a new species (Cocculiniformia: Pseudococculinidae) from off southeastern Brazil. Nautilus 117: 69–77.
Tablado A., López Gappa J. 2001. Morphometric diversity of the pulmonate limpet Siphonaria lesson in different coastal environments. Sci. Mar. 65: 33–41.
Teske P. R., Barker N. P., Mcquaid C. D. 2007. Lack of genetic differentiation among four sympatric southeast African intertidal limpets (Siphonariidae): phenotypic plasticity in a single species? J. Mollus. Stud. 73: 223–228.
Tillier S., Masselot M., Hevré P., Tillier A. 1992. Phylogénie moléculaire des Gastropodes (Mollusca) fondée sur le séquençage partiel de l’ARN ribosomique 28 S. C. R. Acad. Sci. III 134: 79–85.
Villiers C. J. de, Hodgson A. N. 1987. The structure of the secondary gill of Siphonaria capensis (Gastropoda: Pulmonata). J. Mollus. Stud. 53: 129–138.
Voss N. A. 1959. Studies on the pulmonate gastropod Siphonaria pectinata (Linnaeus) from the southeast coast of Florida. Bull. Mar. Sci. 9: 84–99.
Wells R. M. G., Wong P. P. S. 1978. Respiratory functions of the blood in the limpet Siphonaria zelandica (Gastropoda: Pulmonata). N. Z. J. Zool. 5: 417–420.
White T. R., Conrad M. M., Tseng R., Balayan S., Golding R., Martins A. M. F., Dayrat B. A. 2011. Ten new complete mitochondrial genomes of pulmonates (Mollusca: Gastropoda) and their impact on phylogenetic relationships. BMC Evol. Biol. 11: 295.
White T. R., Dayrat B. 2012. Checklist of genus- and species-group names of the false limpets Siphonaria (Mollusca: Gastropoda: Euthyneura). Zootaxa 3538: 54–78.
WoRMS Editorial Board 2017. World Register of Marine Species. Available from at VLIZ. Accessed 2017-05-08.
Yonge C. M. 1952. The mantle cavity in Siphonaria alternata Say. Proc. Malac. Soc. London 29: 190–199.

Folia Malacologica (2017) 25: 147-164
First published on-line: 2017-09-01 00:00:00
Full text (.PDF) BibTeX Mendeley Back to list