Skip to main content
SpringerLink
Log in

Distribution pattern, reproductive traits, and molecular analysis of two coexisting vermetid gastropods of the genus Petaloconchus: a Caribbean endemic and a potential invasive species

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Vermetid gastropods are characterized by complex taxonomy and unusual ecology. A survey of the fouling community in the intake channel at the Planta Centro Power Plan in Puerto Cabello, Venezuela, found massive colonies of vermetid gastropods of the genus Petaloconchus. We arbitrarily named two prevalent varieties as black and brown-orange morphs, distinguishing based on the color of their soft bodies. Spatial distribution was different for the morphs. The black morph was present along the jetty, with higher average densities in the shallower intertidal area (410 vs. 143 ind m−2), while the brown-orange morph was only present at the initial part of the channel (μ = 83 ind m−2). Both produced small eggs (142 vs. 180 μm diameter on average), with the orange-brown eggs being slightly larger, but the morphs differed in other reproductive aspects. The brown-orange morph produced significantly fewer capsules (up to nine simultaneously per female) with fewer embryos (average of 27 viable embryos/capsule) that hatched at a larger size (577 μm on average), allocating about 17.64% of the initial egg production to nurse eggs. In contrast, the black morph produced up to 14 capsules simultaneously, hatched an average of 178 veligers of 212 μm, and produced no nurse eggs. The intra-capsular development reached a more advanced stage in the brown-orange morph than in the black one. Several cytochrome subunit I (COI) and 16S rRNA (16S) haplotypes were found for the black morph, when compared to only one haplotype for both genes present for the brown-orange morph. Preliminary phylogenetic analyses separated the morphs into different clades, supported by robust bootstrap values and posterior probabilities (>98). Our results indicate that the morphs are two different species: the black morph was identified as Petaloconchus cf. varians and the brown-orange morph as a non-described species, Petaloconchus sp. (orange). The first is endemic to the Caribbean, while the second is potentially an introduced species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abbot RT (1974) American seashells. Van Nostrand Reinhold Company, New York, pp 99–100

    Google Scholar 

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, USA

    Google Scholar 

  • Azzopardi L, Schembri PJ (1997) Vermetid crusts from the maltese islands (Central Mediterranean). Mar Life 7:7–16

    Google Scholar 

  • Bieler R (1989) Marine “Wormsnails”: a phylogenetic approach. [Abstract]. 10th International Malacological Congress, Tübingen, p 26

  • Bieler R (1995) Vermetid gastropods from Sao Miguel, Azores: Comparative anatomy, systematic position and biogeographic affiliation. Açoreana Supplement:173–192

  • Bieler R (1996) Mörch’s Worm-snail taxa (Caenogastropoda: Vermetidae, Siliquariidae, Turritellidae). Am Malacol Bull 13:23–35

    Google Scholar 

  • Bohonak AJ (1999) Dispersal, gene flow, and population structure. Qart Rev Biol 74(1):21–45

    Article  CAS  Google Scholar 

  • Burton RS, Feldman MW (1982) Population genetics of coastal and estuarine invertebrates: does larval behavior influence population structure? In: Kennedy VS (ed) Estuarine comparisons. Academic, New York, pp 537–551

    Google Scholar 

  • Byers JE, Pringle JM (2006) Going against the flow: retention, range limits and invasion in advective environments. Mar Ecol Prog Ser 313:27–41

    Article  Google Scholar 

  • Calvo M, Templado J (2004a) Reproduction and development in a vermetid gastropod, Vermetus triquetrus. Invertebr Biol 123:289–303

    Article  Google Scholar 

  • Calvo M, Templado J (2004b) Reproduction and sex reversal of the solitary vermetid gastropod Serpulorbis arenarius. Mar Biol 146:963–973

    Article  Google Scholar 

  • Calvo M, Templado J (2005) Spermatophores of three Mediterranean species of vermetid gastropods (Caenogastropoda). J Moll Stud 71:301–303

    Article  Google Scholar 

  • Calvo M, Templado J, Penchaszadeh PE (1998) Reproductive biology of the gregarious mediterranean vermetid gastropod Dendropoma petraeum. J Mar Biol Assoc United King 78:1–25

    Article  Google Scholar 

  • Calvo M, Templado J, Oliverio M, Machordom A (2009) Hidden Mediterranean biodiversity: molecular evidence for a cryptic species complex within the reef building vermetid gastropod Dendropoma petraeum (Mollusca: Caenogastropoda). Biol J Linn Soc 96:898–912

    Article  Google Scholar 

  • Carlton JT (2000) Global change and biological invasions in the oceans. In: Moonaey HA, Hobbs RJ (eds) Invasive species in a changing world. Island, Washington DC, pp 31–53

    Google Scholar 

  • Carvahlo Rios E (1994) SeaShells of Brazil, 2nd edn. Editora de Furg, Rio Grande, Rio de Janeiro, p 225

    Google Scholar 

  • Costello MJ, Stocks K, Zhang Y, Grassle JF, Fautin DG (2007) About the ocean biogeographic MA. Information System. Retrieved on 2009 www.iobis.org

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invisibility. J Ecol 88:528–534

    Article  Google Scholar 

  • Ekdale AA (1974) Marine mollusks from shallow-water environments (0 to 60 meters) off the northeast Yucatan coast, Mexico. Bull Mar Sci 24:638–668

    Google Scholar 

  • Elgar MA (1990) Evolutionary compromise between a few large and many small eggs: comparative evidence in teleost fish. Oikos 59:283–287

    Article  Google Scholar 

  • Faucci A, Hadfield MG (2003) Influence of larval mode on dispersal and genetic population structure of Hawaiian vermetids (Vermetidae: Gastropoda). Annual Meeting of The Society for Integrative and Comparative Biology, San Diego 43(6):936

  • Faucci A, Toonen RJ, Hadfield MG (2007) Phylogeography and population connectivity of vermetid gastropods in the Hawaiian Island. Third International Biogeography Society Conference, Tenerife

  • Flores-Rodriguez P, Flores-Garza R, García Ibáñez S, Valdez-Gonzáles A (2007) Variation in the diversity of mollusks from the rocky intertidal of playa Troncones, la Unión, Guerrero, Mexico. Revista Mexicana de Biodiversidad 78:335–405

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  Google Scholar 

  • Gilg MR, Hilbish TJ (2003) The geography of marine larval dispersal: coupling genetics with fine-scale physical oceanography. Ecology 84:2989–2998

    Article  Google Scholar 

  • Gould SJ (1994) Petaloconchus sculpturatus alaminatus, a new Pliocene subspecies of vermetid gastropods lacking its defining generic character, with comments on vermetid systematics in general. J Paleontol 68:1025–1036

    Google Scholar 

  • Grantham BA, Eckert GL, Shanks AL (2003) Dispersal potential of marine invertebrates in diverse habitat. Ecol Appl 13:S108–S116

    Article  Google Scholar 

  • Grimm V, Reise K, Strasser M (2003) Marine Metapopulation: a useful concept? Helgol Mar Res 56:222–228

    Google Scholar 

  • Grosberg RK, Cunningham CW (2001) Genetic structure in the sea: from populations to communities. In: Bertness MD, Gaines S, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 61–84

    Google Scholar 

  • Haase M, Misof B, Wirth T, Baminger H, Baur B (2003) Mitochondrial differentiation in a polymorphic land snail: evidence for Pleistocene survival within the boundaries of permafrost. J Evol Biol 16:415–428

    Article  CAS  Google Scholar 

  • Hadfield MG (1989) Latitudinal effects on juvenile size and fecundity in petaloconchus (Gastropoda). Bull Mar Sci 45(2):369–375

    Google Scholar 

  • Hadfield MG, Iaea DK (1989) Velum of encapsulated veligers of petaloconchus (Gastropoda), and the problem of re-evolution of planktotrophic larvae. Bull Mar Sci 45:377–386

    Google Scholar 

  • Hadfield MG, Kay EA, Gillete MU, Lloyd MC (1972) The Vermetidae (Mollusca: Gastropoda) of the Hawaiian islands. Mar Biol 12:81–98

    Google Scholar 

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

    Article  Google Scholar 

  • Huelsenbeck JP (2000) MrBayes: bayesian inference of phylogeny. University of Rochester, Department of Biology, Rochester

    Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  Google Scholar 

  • Hughes RN (1979) Notes on the reproductive strategies of the South African vermetid gastropods Dendropoma corallinaceum and Serpulorbis natalensis. Veliger 21:423–427

    Google Scholar 

  • Hughes RN (1983) The vermetid gastropod of Hong Kong. In: Morton JE (ed) Proceedings of the Second International Workshop on the Malacofauna of Hong Kong and Southern China, Hong Kong, pp 127–138

  • Hughes RN (1993) The vermetid gastropods of Rottnest Island, western Australia. In: Wells FE, Walker DI, Kirkman H, Lethbridge R (eds) The marine flora and fauna of Rottnest Island, western Australia, vol 1. Western Australia Museum, Perth, pp 193–205

    Google Scholar 

  • Hughes RN, Lewis AH (1974) On the distribution, feeding and reproduction of the vermetid gastropod Dendropoma maximum. J Zool Lond 172:531–547

    Article  Google Scholar 

  • Hulbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211

    Article  Google Scholar 

  • Imron JB, Hale P, Degnan BM, Degnan SM (2007) Pleistocene isolation and recent gene flow in Haliotis asinina, an Indo-Pacific vetigastropod with limited dispersal capacity. Mol Ecology 16:289–304

    Google Scholar 

  • Jablonski D, Lutz RL (1983) Larval ecology of marine benthic invertebrates: paleo-biological implications. Biol Rev 58:21–89

    Article  Google Scholar 

  • Johannesson K (1988) The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)? Mar Biol 99:507–513

    Article  Google Scholar 

  • Jones B, Hunter IG (1995) Vermetid buildups from Grand Cayman, British West Indies. J Coast Res 11(4):973–983

    Google Scholar 

  • Keen AM (1961) A proposed reclassification of the gastropod family Vermetidae. Bull Brit Mus (Nat Hist Zool) 7:183–214 pls. 54–55

    Google Scholar 

  • Keen AM (1982) Spiroglyphus and Stoa, taxonomic problems in the Vermetidae. Veliger 22:388–391

    Google Scholar 

  • Laborel J (1977) Are reef-building vermetids disappearing in the South Atlantic? Proc Third Inter Coral Reef Symp, Miami, pp 233–237

  • Lockwood JL, Hoopes MF, Marchetti MP (2008) Invasion ecology. Blackwell Publishing, USA

    Google Scholar 

  • Losada F, Martín A, Feragotto W, Alamo C (1988) Interacciones biológicas en el canal de toma de la planta termoeléctrica del centro Punta Morón, Venezuela. Ecotropicos 1:55–70

    Google Scholar 

  • Lydeard C, Holznagel WE, Glaubrecht M, Ponder WF (2002) Molecular phylogeny of a circum-global, diverse gastropod superfamily (Cerithioidea: Mollusca: Caenogastropoda): Pushing the deepest phylogenetic limits of mitochondrial LSU rDNA sequences. Mol Phylogenet Evol 22:399–406

    Article  CAS  Google Scholar 

  • Machordom A, Araujo R, Erpenbeck D, Ramos MA (2003) Phylogeography and conservation genetics of endangered European Margaritiferidae (Bivalvia: Unionidae). Biol J Linn Soc 78:235–252

    Article  Google Scholar 

  • Miller KJ, Ayre DJ (2008) Population structure is not a simple function of reproductive mode and larval type: insights from tropical corals. J Anim Ecol 77:713–724

    Article  Google Scholar 

  • Miloslavich PA (1987) Biología y estrategias reproductivas de Vermetus sp. y Dendropoma corrodens, dos especies pertenecientes a la familia Vermetidae. Bachelor Dissertation, Simón Bolívar University

  • Miloslavich PA (1996) Nurse egg feeding prosobranchs: a comparative biochemical and electrophoretic analysis of eggs and hatchlings. Am Malacol Bull 13:37–46

    Google Scholar 

  • Miloslavich PA (2002) Balance de proteínas en los embriones de Caenogasterópodos durante su desarrollo intracapsular. V Congreso Latinoamericano de Malacología, Sao Paulo, Brazil, p 28

    Google Scholar 

  • Miloslavich PA, Dufresne L (1994) Development and effect of female size on egg and juvenile production in the Neogastropod Buccinum cyaneum from the Saguenay fjord. Can J Fish Aqua Sci 51:2866–2872

    Article  Google Scholar 

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

    Google Scholar 

  • Miloslavich P, Penchaszadeh P, Klein E (2003) Reproduction of Crepidula navicula Morch, 1877 and Crepidula aplysioides Reeve, 1859 (Caenogastropoda) from Morrocoy and La Restinga lagoon, Venezuela. Naut 117:121–134

    Google Scholar 

  • Miloslavich P, Klein E, Penchaszadeh P (2009) Gametogenic cycle of the tropical vermetids Eualetes tulipa and Dendropoma corrodens (Mollusca: Caenogastropoda: Vermetidae). J Mar Biol Ass UK (in press)

  • Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492

    Article  Google Scholar 

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

    Google Scholar 

  • Nishiwaki S (1969) Seasonal size variations of the pallial slit in female Serpulorbis imbricatus (Prosobranchia, Vermetidae). Sci Rep Tokyo Kyoiku Daigaku (Sec. B) 14(208):69–78

  • Olsson AA, Harbison A (1953) Pliocene Mollusca of Southern Florida, with special reference to those from North Saint Petersburg. Mon Acad Nat Sci Phil 8: vii + 459, 65 pls

  • Olsson AA, McGinty TL (1958) Recent marine mullusks from the Caribbean Coast of Panama with the description of some new genera and species. Bull Am Paleont 39(327)

  • Palumbi SR (1995) Using genetics as an indirect estimator of larval dispersal. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, New York, pp 369–387

    Google Scholar 

  • Palumbi SR (1996a) Nucleic acids II: the polymerase chain reaction. In: molecular systematics. Hillis DM, Moritz C, Mable BK (eds) Sinauer Associates, Sunderland, pp 205–248

  • Palumbi SR (1996b) Macrospatial genetic structure and speciation in marine taxa with high dispersal abilities. In: Ferraris JD, Palumbi SR (eds) Molecular zoology: advances, strategies and protocols. Wiley-Liss John Wiley & Sons, INC, USA, pp 101–117

    Google Scholar 

  • Ponder WF, Lindberg DR (1997) Towards a phylogeny of gastropod molluscs: an analysis using morphological characters. Zool J Linn Soc 9:83–265

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinf 1:817–818

    Article  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R foundation for statistical computing Vienna, Austria, ISBN 3-90005107-0. http://www.R-proyect.org

  • Radwin GE (1969) A recent molluscan fauna from the Caribbean coast of southeastern Panamá. Trans San Diego Soc Nat Hist 15 (14):229–236

    Google Scholar 

  • Rawlings TA, Collins TM, Bieler R (2001) Major mitochondrial gene rearrangement among closely related species. Mol Biol Evol 18:1604–1609

    Article  CAS  Google Scholar 

  • Rosenberg G (2005) Malacolog 4.1.0: a database of Western Atlantic Marine Mollusca. WWW database (version 4.1.0). Available via DIALOG. http://www.malacolog.org/. Accessed May 2009

  • Roughgarden J (1996) Theory of population genetics and evolutionary ecology: an introduction. Prentice Hall, USA

    Google Scholar 

  • Safriel UN, Hadfield MG (1988) Sibling speciation by life-history divergence in Dendropoma (Gastropoda: Vermetidae). Biol J Linn Soc 35:1–13

    Article  Google Scholar 

  • Schiaparelli S (1995) Contribution to the knowledge of Vermetidae (Mollusca: Gastropoda) from the Ligurian Sea. Boll Malacolog 31:267–276

    Google Scholar 

  • Schiaparelli S, Cattaneo-Vietti R (1999) Functional morphology of vermetid feeding-tubes. Lethaia 32:41–46

    Article  Google Scholar 

  • Schiaparelli S, Métivier B (2000) On the identity of “Vermetus” roussaei Vaillant, 1871 (Mollusca, Caenogastropoda, Vermetidae), with the description of a new species. Zoosyst 22(4):677–687

    Google Scholar 

  • Schiaparelli S, Guidetti P, Cattaneo-Vietti R (2003) Can mineralogical features affect the distribution patterns of sessile gastropods? The Vermetidae case in the Mediterranean Sea. J Mar Biol Assoc UK 83:1267–1268

    Article  Google Scholar 

  • Schiaparelli S, Albertelli G, Cattaneo-Vietti R (2006) Phenotypic plasticity of Vermetidae suspension feeding: a potential bias in their use as Biological Sea-Level Indicators. Mar Ecol 27:44–53

    Article  Google Scholar 

  • Statsoft Inc (2003) STATISTICA (Data analysis software system). Version 6. www.statsoft.com

  • Strathmann R (1974) The Spread of Sibling Larvae of Sedentary Marine Invertebrates. Am Nat 108:29–44

    Article  Google Scholar 

  • Strathmann R (1980) Why does a larva swim so long? Paleobiol 6:373–376

    Google Scholar 

  • Strathmann MF, Strathmann RR (2006) A vermetid with complex intracapsular cannibalism of nurse eggs and sibling larvae and a high potential for invasion. Pac Sci 60:97–108

    Article  Google Scholar 

  • Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4 beta 10. Sinauer Associates, Massachusetts

    Google Scholar 

  • Tello J (1975) Catálogo de la Fauna Venezolana. VIII. Mollusca, Arte, Caracas

  • Underwood AJ, Chapman MG, Richards SA, Sage MB (1997) GMAV5 for windows. Institute of Marine Ecology, University of Sydney, Sydney

    Google Scholar 

  • Warmke GL, Abbot RT (1961) Caribbean seashells. Livingston, Col Narberth

  • Warmke GC, Abbot RT (1962) Caribbean seashells: a guide to the Marine Mollusks of Puerto Rico and other West Indian Islands, Bermuda and the lower Florida keys. Livingston, Wynnewood, p 346

  • Weir BS (1996) Intraspecific differentiation. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. Sinauer Associates Inc. Publishers, USA, pp 385–406

    Google Scholar 

Download references

Acknowledgments

We are indebted to the BBVA Foundation (Spain) for providing funds for the internship of Vanessa Weinberger at the Museo Nacional de Ciencias Naturales de Madrid (MNCN). The Decanato de Investigación y Desarrollo and the Decanato de Estudios Profesionales of the Universidad Simón Bolívar, Venezuela also supported this research. We wish to express our gratitude to Dr. Rudiger Bieler from the Field Museum for his help in the identification of the species, Dr. Juan Cruz from the Universidad Simon Bolivar for our discussions on the experimental design and Darlene Trew Crist from the University of Rhode Island for her editorial comments. We also thank the numerous people that provided invaluable help with the field work and the staff of the Planta Centro power plant, Dirección de Seguridad Industrial e Higiene, for allowing us access to the channel. This research is part of the activities of the Census of Marine Life—Caribbean Regional Committee in the Southern Caribbean.

Author information

Authors and Affiliations

  1. Laboratorio de Biología Marina, Universidad Simón Bolívar (USB), Pab I 1-3, Sartenejas, Caracas, 1080, Venezuela

    V. P. Weinberger & P. Miloslavich

  2. Museo Nacional de Ciencias Naturales (CSIC), José Gutiérrez Abascal 2, 28006, Madrid, Spain

    A. Machordom

Authors
  1. V. P. Weinberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Miloslavich
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Machordom
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. P. Weinberger.

Additional information

Communicated by S. Uthicke.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weinberger, V.P., Miloslavich, P. & Machordom, A. Distribution pattern, reproductive traits, and molecular analysis of two coexisting vermetid gastropods of the genus Petaloconchus: a Caribbean endemic and a potential invasive species. Mar Biol 157, 1625–1639 (2010). https://doi.org/10.1007/s00227-010-1435-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-010-1435-3

Keywords

Search

Navigation