Integrative systematics of the genus Limacia O. F. Müller, 1781 (Gastropoda, Heterobranchia, Nudibranchia, Polyceridae) in the Eastern Pacific

  • Roberto A. Uribe
  • Fabiola Sepúlveda
  • Jeffrey H. R. Goddard
  • Ángel Valdés
Original Paper

Abstract

Morphological examination and molecular analyses of specimens of the genus Limacia collected in the Eastern Pacific Ocean indicate that four species of Limacia occur in the region. Limacia cockerelli, previously considered to range from Alaska to Baja California, is common only in the northern part of its former range. An undescribed pseudocryptic species, previously included as L. cockerelli, occurs from Northern California to the Baja California Peninsula and is the most common species of Limacia in Southern California and Northern Mexico. Another new species similar to L. cockerelli is described from Antofagasta, Chile and constitutes the first record of the genus Limacia in the Southeastern Pacific Ocean. These two new species are formally described herein. Finally, Limacia janssi is a genetically and morphologically distinct tropical species ranging from Baja California to Panama. Species delimitation analyses based on molecular data and unique morphological traits from the dorsum, radula, and reproductive systems are useful in distinguishing these species

Keywords

Mollusca New species Molecular taxonomy Pseudocryptic species 

Supplementary material

12526_2017_676_MOESM1_ESM.docx (588 kb)
ESM 1(DOCX 588 kb)

References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–722CrossRefGoogle Scholar
  2. Angulo-Campillo OJ (2003) Variación espacio-temporal de las poblaciones de opistobranquios (Mollusca: Opisthobranchia) en tres localidades de B.C.S., Mexico. Master of Science Thesis, Departamento de Pesquerías y Biología Marina, Centro Interdisciplinario de Ciencias Marinas: La Paz, Baja California Sur, Mexico (unpublished).Google Scholar
  3. Angulo-Campillo O (2005) A four year survey of the opisthobranch fauna (Gastropoda, Opisthobranchia) from Baja California Sur, Mexico. Vita Malacologica 3:43–50Google Scholar
  4. Baba K (1937) Opisthobranchia of Japan (II). Jour. Dept. Agr. Kyushu Imp. Univ. 5:289–344, pls.1–2.Google Scholar
  5. Behrens (2004) Pacific Coast Nudibranchs, Supplement II New Species to the Pacific Coast and New Information on the Oldies. Proc Calif Acad Sci 55(2):11–54Google Scholar
  6. Behrens DW, Hermosillo A (2005) Eastern Pacific nudibranchs, a guide to the opisthobranchs from Alaska to Central America. Sea Challengers, Monterey, California. 137 pp., 314 photos.Google Scholar
  7. Bertsch H (2014) Biodiversity in La Reserva de la Biósfera Bahía de los Ángeles y Canales de Ballenas y Salsipuedes: Naming of a new genus, range extensions and new records, and species list of Heterobranchia (Mollusca: Gastropoda), with comments on biodiversity conservation within marine reserves. The Festivus 46:158–177Google Scholar
  8. Bertsch H, Ferreira AJ (1974) Four new species of nudibranchs from tropical West America. The Veliger 16:343–353Google Scholar
  9. Briggs JC, Bowen BW (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. J Biogeogr 39:12–30CrossRefGoogle Scholar
  10. Caballer M, Almón B, Pérez J (2016) The sea slug genus Limacia Müller, 1781 (Mollusca: Gastropoda: Heterobranchia) in Europe. Cah Biol Mar 57:35–42Google Scholar
  11. Clark T (2006) ‘Limacia cockerelli.’ Available at http://week.divebums.com/2006/Jun12-2006/index.html [7th image from top]. Accessed 15 July 2016.
  12. Coleman N (2008) Nudibranchs Encyclopedia. Catalogue of Asia/Indo-Pacific sea slugs. Neville Coleman’s Underwater Geographic Pty: Springwood Queensland, Australia, 416 ppGoogle Scholar
  13. Cooke S, Hanson D, Hirano Y, Ornelas-Gatdula E, Gosliner TM, Chernyshev AV, Valdés A (2014) Cryptic diversity of Melanochlamys sea slugs (Gastropoda, Aglajidae) in the North Pacific. Zool Scripta 43:351–369CrossRefGoogle Scholar
  14. Di Lorenzo E, Mantua NJ (2016) Multi-year persistence of the 2014/15 North Pacific marine heatwave. Nat Clim Chang. doi:10.1038/nclimate3082 Google Scholar
  15. Filatov D (2002) Proseq: a software for preparation and evolutionary analysis of DNA sequence data sets. Mol Ecol Not 2:621–624CrossRefGoogle Scholar
  16. 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 3:294–299PubMedGoogle Scholar
  17. Goddard JHR (1984) The opisthobranchs of Cape Arago, Oregon, with notes on their biology and a summary of benthic opisthobranchs known from Oregon. The Veliger 27:143–163Google Scholar
  18. Goddard JHR (1998) A summary of the prey of nudibranch molluscs from Cape Arago, Oregon. Opisthobranch Newsletter 24:11–14Google Scholar
  19. Goddard JHR (2004) Developmental mode in benthic opisthobranch molluscs from the northeast Pacific Ocean: feeding in a sea of plenty. Can J Zool 82:1954–1968CrossRefGoogle Scholar
  20. Gonsalves-Jackson DC (2004) Opisthobranch mollusks across the Isthmus of Panama: systematics and biogeographic distribution of developmental types. Dissertation, Florida Institute of Technology (unpublished).Google Scholar
  21. Gosliner TM, Valdés A, Behrens DW (2015) Nudibranch and sea slug identification, Indo-Pacific. New World Publication: Jacksonville, Florida 408 pp.Google Scholar
  22. Gosliner TM, Behrens DW, Valdés Á (2008) Indo-Pacific Nudibranchs and Sea Slugs. A field guide to the World’s most diverse fauna. Sea Challengers Natural History Books and California Academy of Sciences: California 426 pp.Google Scholar
  23. Green B (2007) Sea scallop and Cockerell’s dorid (Limacia cockerelli). Available at https://www.flickr.com/photos/lemurdillo/1369606503 Accessed 15 July 2016
  24. Guernsey M (1912) Some of the Mollusca of Laguna Beach. In: First Annual Report of the Laguna Marine Laboratory pp. 68–82. Department of Biology, Pomona College: Claremont, CaliforniaGoogle Scholar
  25. Hebert P, Penton E, Burns J, Janzen D, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci 101:14812–14817CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hermosillo A (2004) Opisthobranch mollusks of Parque Nacional de Coiba, Panamá (tropical Eastern Pacific). The Festivus 36:105–117Google Scholar
  27. Hermosillo A, Behrens DW, Ríos-Jara E (2005) Opistobranquios de México. CONABIO: Guadalajara, Mexico, 143 ppGoogle Scholar
  28. Hershman D (2016) Limacia cockerelli. Available at: https://www.flickr.com/photos/hershman/26068755511 Accessed 17 February 2017
  29. Hoover C, Lindsay T, Goddard JHR, Valdés Á (2015) Seeing double: pseudocryptic diversity in the Doriopsilla albopunctataDoriopsilla gemela species complex of the north‐eastern Pacific. Zool Scripta 44:612–631CrossRefGoogle Scholar
  30. Huelsenbeck J, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefPubMedGoogle Scholar
  31. Johnson ME, Snook HJ (1927) Seashore animals of the Pacific coast. Macmillan Company: New York; reprinted 1967 by Dover Publications: New York, 633 ppGoogle Scholar
  32. Keen AM (1971) Seashells of Tropical West America: Marine Mollusks from Baja California to Peru. Stanford University Press, California, 1064 ppGoogle Scholar
  33. Kienberger K, Carmona L, Pola M, Padula V, Gosliner TM, Cervera JL (2016) Aeolidia papillosa (Linnaeus, 1761) (Mollusca: Heterobranchia: Nudibranchia), single species or a cryptic species complex? A morphological and molecular study. Zool J Linn Soc 177:481–506CrossRefGoogle Scholar
  34. Klug D (2014) Nudibranch5April18-14. Available at: https://www.flickr.com/photos/diverdoug/14344674700 Accessed 17 February 2017
  35. Krug PJ, Ellingson RA, Burton R, Valdés A (2007) A new poecilogonous species of sea slug (Opisthobranchia: Sacoglossa) from California: Comparison with the planktotrophic congener Alderia modesta (Lovén, 1844). J Molluscan Stud 73:29–38CrossRefGoogle Scholar
  36. Lance JR (1961) A distributional list of Southern California opisthobranchs. The Veliger 4:64–69Google Scholar
  37. Larkin M, Blackshields G, Brown N, Chenna R, Mcgettigan P, Mcwilliam H, Valentin F, Wallace I, Wilm A, Lopez R, Thompson et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948Google Scholar
  38. Lawrence KT, Liu Z, Herbert TD (2006) Evolution of the eastern tropical Pacific through Plio-Pleistocene glaciation. Science 312:79–83CrossRefPubMedGoogle Scholar
  39. Lindsay T, Valdés A (2016) The model organism Hermissenda crassicornis (Gastropoda: Heterobranchia) is a species complex. PLoS One 11:e0154265CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lindsay T, Kelly J, Chichvarkhin A, Craig S, Kajihara H, Mackie J, Valdés Á (2016) Changing spots: pseudocryptic speciation in the North Pacific dorid nudibranch Diaulula sandiegensis (Cooper, 1862) (Gastropoda: Heterobranchia). J Molluscan Stud. doi:10.1093/mollus/eyw026 Google Scholar
  41. MacFarland FM (1905) A preliminary account of the Dorididae of Monterey Bay, California, and vicinity. Proc Biol Soc Wash 18:35–54Google Scholar
  42. MacFarland FM (1906) Opisthobranchiate Mollusca from Monterey Bay, California, and vicinity. Bull US Bur Fish 25:109–151, pls. 18–31.Google Scholar
  43. Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75 http://mesquiteproject.org Accessed 30 July 2016
  44. McDonald GR (1983) A review of the nudibranchs of the California coast. Malacologia 24:114–276Google Scholar
  45. McDonald GR, Nybakken JW (1978) Additional notes on the food of some California nudibranchs with a summary of known food habits of California species. The Veliger 21:110–118Google Scholar
  46. McDonald GR, Nybakken JW (1980) Guide to the nudibranchs of California. American Malacologists, inc., Melbourne, Florida, 72 ppGoogle Scholar
  47. Miller S, Dykes D, Polesky H (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215CrossRefPubMedPubMedCentralGoogle Scholar
  48. O’Donoghue CS, O’Donoghue E (1922) Notes on the nudibranchiate Mollusca from the Vancouver Island region. II. The spawn of certain species. Trans R Can Inst 14:131–143Google Scholar
  49. Ortea J, Quero A, Rodríguez G, Valdés A (1989) Estudio de Limacia clavigera (Müller, 1776) (Mollusca: Nudibranchia) con nota sobre su distribución geográfica y la validez del género Laila MacFarland, 1905. Rev Biol Univ Oviedo 7:99–107Google Scholar
  50. Palumbi S, Martin A, Romano S, Owen MacMillan W, Stice L, Grabowski G (1991) The Simple Fool’s Guide to PCR. Department of Zoology, University of Hawaii, Honolulu, 45 ppGoogle Scholar
  51. Pola M, Cervera JL, Gosliner TM (2007) Phylogenetic relationships of Nembrothinae (Mollusca: Doridacea: Polyceridae) inferred from morphology and mitochondrial DNA. Mol Phylogenet Evol 43:726–742CrossRefPubMedGoogle Scholar
  52. Pola M, Gosliner TM (2010) The first molecular phylogeny of cladobranchian opisthobranchs (Mollusca, Gastropoda, Nudibranchia). Mol Phylogenet Evol 56:931–941CrossRefPubMedGoogle Scholar
  53. Posada D (2008) JModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefPubMedGoogle Scholar
  54. Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol 21:1864–1877CrossRefPubMedGoogle Scholar
  55. Radulovici A, Archambault P, Dufresne F (2010) DNA barcoding for marine biodiversity: moving fast forward? Diversity 2:450–472CrossRefGoogle Scholar
  56. Roy K, Jablonski D, Valentine JW (1995) Thermally anomalous assemblages revisited: patterns in the extraprovincial latitudinal range shifts of Pleistocene marine mollusks. Geology 23:1071–1074CrossRefGoogle Scholar
  57. Schrödl M, Grau JH (2006) Nudibranchia from the remote southern Chilean Guamblin and Ipún islands (Chonos Archipelago, 44–45°S), with re-description of Rostanga pulchra MacFarland, 1905. Rev Chil Hist Nat 79:3–12CrossRefGoogle Scholar
  58. Schrödl M (2003) Sea slugs of southern South America: Systematics, biogeography and biology of Chilean and Magellanic Nudipleura (Mollusca: Opisthobranchia). Conch-Books, Hackenheim, Germany, 165 ppGoogle Scholar
  59. Stamatakis A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690CrossRefPubMedGoogle Scholar
  60. Stanley SM (1984) Temperature and biotic crises in the marine realm. Geology 12:205–208CrossRefGoogle Scholar
  61. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mole Biol Evol 30:2725–2729CrossRefGoogle Scholar
  62. Thollesson M (2000) Increasing fidelity in parsimony analysis of dorid nudibranchs by differential weighting, or a tale of two genes. Mol Phylogenet Evol 16(2):161–172CrossRefPubMedGoogle Scholar
  63. Vitsky A (2008) Limacia cockerelli. Available at http://week.divebums.com/2008/Sep08-2008/index.html [2nd image from top] Accessed 15 July 2016.
  64. Wakeling M (2001) Laila cockerelli colour forms from Canada. Available at http://www.seaslugforum.net/find/5549Accessed 17 February 2017
  65. Zade R (2008) Limacia cockerelli and scaleworm. Available at http://www.seaslugforum.net/find/21852 Accessed 17 February 2017

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Roberto A. Uribe
    • 1
  • Fabiola Sepúlveda
    • 2
  • Jeffrey H. R. Goddard
    • 3
  • Ángel Valdés
    • 4
  1. 1.Laboratorio de Biodiversidad y Ecología BentónicaInstituto del Mar del Perú – IMARPEChimbotePerú
  2. 2.Laboratorio de Ecología Parasitaria y Epidemiología Marina LEPyEM, Facultad de Ciencias del Mar y Recursos BiológicosUniversidad de AntofagastaAntofagastaChile
  3. 3.Marine Science InstituteUniversity of CaliforniaSanta BarbaraUSA
  4. 4.Department of Biological SciencesCalifornia State Polytechnic UniversityPomonaUSA

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