Skip to main content
SpringerLink
Log in

Molecular identification of two species of the carnivorous sea slug Philine, invaders of the US west coast

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Open-coast and deep-water ecosystems have been less disrupted by invasion than estuaries, but a notable exception is the establishment of multiple species of the sea slug genus Philine in the northeastern Pacific. These large slugs spread from San Francisco Bay to the whole of the US west coast in 5 years during the 1990s, and are abundant from intertidal mudflats to soft-sediment bottoms >300 m deep along the open coast. Voracious predators that secrete acid, Philine spp. have few natural enemies and substantial impacts on native bivalve communities. Despite their ecological significance, the identity and number of invasive Philine spp. in the US has remained controversial. Here, we adopt a molecular approach to identify the species commonly found along the US west coast. We compared mitochondrial 16S gene sequences of reference specimens from the native range of seven possible invaders against sequences of 66 specimens collected from southern California to Oregon from intertidal and subtidal habitats. All slugs from southern California and Oregon were confirmed as P. auriformis, and most shared haplotypes with samples from New Zealand. Larger slugs from San Francisco, Tomales Bay and Bodega Harbor, believed to represent 3–4 species, were all identified as P. orientalis. Molecular data support a recent morphological analysis that erected two proposed species, P. paucipapillata from Hong Kong and P. quadripartita from Europe, which are genetically distinct from anatomically similar species. For taxonomically challenging groups like sea slugs, genetic data can illuminate cryptic invasions and provide a backdrop for further studies of the ecological impacts of introduced marine species.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

References

  • Andreakis N, Procaccini G, Maggs C, Kooistra W (2007) Phylogeography of the invasive seaweed Asparagopsis (Bonnemaisoniales, Rhodophyta) reveals cryptic diversity. Mol Ecol 16:2285–2299

    Article  PubMed  CAS  Google Scholar 

  • Anthes N, Schulenburg H, Michiels NK (2008) Evolutionary links between reproductive morphology, ecology and mating behavior in opisthobranch gastropods. Evolution 62:900–916

    Article  PubMed  Google Scholar 

  • Armstrong KF, Ball SL (2005) DNA barcodes for biosecurity: invasive species identification. Phil Trans Roy Soc B 360:1813–1823

    Google Scholar 

  • Asif JH, Krug PJ (2011) Lineage distribution and barriers to gene flow among populations of the globally invasive marine mussel Musculista senhousia. Biol Invasions. doi:10.1007/s10530-011-0169-6

  • Bastrop R, Blank M (2006) Multiple invasions: a polychaete genus enters the Baltic Sea. Biol Inv 8:1195–1200

    Article  Google Scholar 

  • Bax N, Carlton JT, Mathews-Amos A, Haedrich RL, Howarth FG, Purcell JE, Rieser A, Gray A (2001) The control of biological invasions in the world’s oceans. Conserv Biol 15:1234–1246

    Article  Google Scholar 

  • Behrens DW (1991) Pacific coast nudibranchs, 2nd edn. Sea Challengers, Monterey

    Google Scholar 

  • Behrens DW (2004) Pacific coast nudibranchs, supplement II. Proc Cal Acad Sci 55:11–54

    Google Scholar 

  • Cadien DB, Ranasinghe JA (2003) Invaders in the open sea: establishment of the New Zealand snail Philine auriformis in southern California coastal waters. In Weisberg SB, Elmore D (eds) Annual report of the Southern California coastal water research project, Westminster, pp 253–265

  • Carlton JT (1979) History, biogeography, and ecology of the introduced marine and estuarine invertebrates of the Pacific coast of North America. Ph.D. dissertation, UC Davis

  • Carlton JT (1996a) Biological invasions and cryptogenic species. Ecology 77:1653–1655

    Article  Google Scholar 

  • Carlton JT (1996b) Pattern, process, and prediction in marine invasion ecology. Biol Conserv 78:97–106

    Article  Google Scholar 

  • Chow MM (2001) Ecological impacts of introduced opisthobranchs, Philine spp., on the Bodega Harbor mudflats. M.S. thesis, San Francisco State University

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Google Scholar 

  • Cohen AN, Carlton JT (1995) Non-indigenous aquatic species in a United States estuary; a case study of the biological invasions of the San Francisco Bay and Delta. United States Fish and Wildlife Service, Washington

    Google Scholar 

  • Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558

    Article  PubMed  CAS  Google Scholar 

  • Darling JA, Blum MJ (2007) DNA-based methods for monitoring invasive species: a review and prospectus. Biol Inv 9:751–765

    Article  Google Scholar 

  • Deagle BE, Bax N, Patil JG (2003) Development and evaluation of a PCR-based test for detection of Asterias (Echinodermata: Asteroidea) larvae in Australian plankton samples from ballast water. Mar Freshwater Res 54:709–719

    Article  CAS  Google Scholar 

  • DeSalle R, Egan MG, Siddall M (2005) The unholy trinity: taxonomy, species delimitation and DNA barcoding. Phil Trans Roy Soc Lond Ser B 360:1905–1916

    Article  CAS  Google Scholar 

  • Douady CJ, Delsuc F, Boucher Y, Doolittle WF, Douzery JP (2003) Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Mol Biol Evol 20:248–254

    Article  PubMed  CAS  Google Scholar 

  • Ellingson RA, Krug PJ (2006) Evolution of poecilogony from planktotrophy: cryptic speciation, phylogeography, and larval development in the gastropod genus Alderia. Evolution 60:2293–2310

    PubMed  CAS  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Galtier N, Depaulis F, Barton NH (2000) Detecting bottlenecks and selective sweeps from DNA sequence polymorphism. Genetics 155:981–987

    PubMed  CAS  Google Scholar 

  • Geller JB (1999) Decline of a native mussel masked by sibling species invasion. Conserv Biol 13:661–664

    Article  Google Scholar 

  • Geller JB, Walton ED, Grosholz ED, Ruiz GM (1997) Cryptic invasions of the crab Carcinus detected by molecular phylogeography. Mol Ecol 6:901–906

    Article  PubMed  CAS  Google Scholar 

  • Gibson GD, Chia F-S (1989) Description of a new species of Haminoea, Haminoea callidegenita (Mollusca: Opisthobranchia), with a comparison with two other Haminoea species found in the northeast Pacific. Can J Zool 67:914–922

    Article  Google Scholar 

  • Goddard J (1998) Philine in Oregon (http://www.seaslugforum.net/find/217)

  • Gosliner TM (1995) Introduction and spread of Philine auriformis (Gastropoda: Opisthobranchia) from New Zealand to San Francisco Bay and Bodega Harbor. Mar Biol 122:249–255

    Google Scholar 

  • Gosliner TM (1998) A third Philine in California (http://www.seaslugforum.net/find/230)

  • Gosliner TM, Behrens DW (2006) Anatomy of an invasion: systematics and distribution of the introduced opisthobranch snail, Haminoea japonica Pilsbry, 1895 (Gastropoda: Opisthobranchia: Haminoeidae). Proc Cal Acad Sci 57:1003–1010

    Google Scholar 

  • Grande C, Templado J, Cervera JL, Zardoya R (2004) Molecular phylogeny of Euthyneura (Mollusca: Gastropoda). Mol Biol Evol 21:303–313

    Google Scholar 

  • Grosholz ED (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27

    Article  Google Scholar 

  • Hanfling B, Carvalho GR, Brandl R (2002) mtDNA sequences and possible invasion pathways of the Chinese mitten crab. Mar Ecol Prog Ser 238:307–310

    Article  CAS  Google Scholar 

  • Hirano YJ, Hirano YM (1991) Poecilogony or cryptic species? Two geographically different development patterns observed in ‘Cuthona pupillae (Baba, 1961)’ (Nudibranchia: Aeolidoidea). J Molluscan Stud 57:133–141

    Google Scholar 

  • Holland BS (2000) Genetics of marine bioinvasions. Hydrobiologia 420:63–71

    Article  CAS  Google Scholar 

  • Holland BS, Dawson MN, Crow GL, Hofmann DK (2004) Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Mar Biol 145:1119–1128

    Article  Google Scholar 

  • Huelsenbeck JP, Rannala B (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol 53:904–913

    Article  PubMed  Google Scholar 

  • Jensen KR (1993) Morphological adaptations and plasticity of radular teeth of the Sacoglossa (= Ascoglossa) (Mollusca: Opisthobranchia) in relation to their food plants. Biol J Linn Soc 48:135–155

    Article  Google Scholar 

  • Krug PJ, Ellingson RA, Burton RA, Valdés Á (2007) A new poecilogonous species of sea slug (Opisthobranchia: Sacoglossa) from California: comparison with the planktotrophic congener Alderia modesta (Lovén, 1844). J Molluscan Stud 73:29–38

    Article  Google Scholar 

  • Krug PJ, Morley MS, Asif JH, Hellyar LL, Blom WM (2008) Molecular confirmation of species status for the rare cephalaspidean Melanochlamys lorrainae (Rudman, 1968), and comparison with its sister species M. cylindrica Cheeseman, 1881. J Molluscan Stud 74:267–276

    Article  Google Scholar 

  • Krug PJ, Händeler K, Vendetti JE (2012) Genes, morphology, development and photosynthetic ability support the resurrection of Elysia cornigera (Heterobranchia: Plakobranchoidea) as distinct from the solar-powered sea slug E. timida. Invert Syst (in press)

  • Lavoie DM, Smith LD, Ruiz GM (1999) The potential for intracoastal transfer of non-indigenous species in the ballast water of ships. Est Coast Shelf Sci 48:551–564

    Article  Google Scholar 

  • Lindholm AK, Breden F, Alexander HJ, Chan W-K, Thakurta SG, Brooks R (2005) Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia. Mol Ecol 14:3671–3682

    Article  PubMed  CAS  Google Scholar 

  • Lydeard C, Holznagel WE, Schnare MN, Gutell RR (2000) Phylogenetic analysis of molluscan mitochondrial LSU rDNA sequences and secondary structures. Mol Phylog Evol 15:83–102

    Article  CAS  Google Scholar 

  • Martel C, Viard F, Bourguet D, Garcia-Meunier P (2004) Invasion by the marine gastropod Ocinebrellus inornatus in France I. Scenario for the source of introduction. J Exp Mar Biol Ecol 305:155–170

    Article  Google Scholar 

  • McDonald JH, Koehn RK (1988) The mussels Mytilus galloprovincialis and M. trossulus on the Pacific coast of North America. Mar Biol 99:111–118

    Article  Google Scholar 

  • Medina M, Walsh PJ (2000) Molecular systematics of the order Anaspidea based on mitochondrial DNA sequence (12S, 16S, and COI). Mol Phylog Evol 15:41–58

    Article  CAS  Google Scholar 

  • Meyer CP, Paulay G (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biol 3:e422. doi:10.1371/journal.pbio.0030422

    Article  PubMed  Google Scholar 

  • Morrow C, Thorpe J, Picton B (1992) Genetic divergence and cryptic speciation in two morphs of the common subtidal nudibranch Doto coronata (Opisthobranchia: Dendronotacea: Dotoidae) from the northern Irish Sea. Mar Ecol Prog Ser 84:53–61

    Article  Google Scholar 

  • Pagel M, Meade A (2004) A phylogenetic mixture model for detecting pattern-heterogeneity in gene sequence or character-state data. Syst Biol 53:571–581

    Article  PubMed  Google Scholar 

  • Palumbi SR (1996) Nucleic acids II: the polymerase chain reaction. In: Hillis D, Moritz C, Mable B (eds) Molecular systematics. Sinauer, Sunderland, pp 205–247

    Google Scholar 

  • Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • Posada D (2004) Collapse ver. 1.2. Available from http://darwin.uvigo.es

  • Price RM, Gosliner TM, Valdés A (2011) Systematics and phylogeny of Philine (Gastropoda: Opisthobranchia), with emphasis on the Philine aperta species complex. Veliger 51:1–58

    Google Scholar 

  • Ranasinghe JA, Mikel TK, Velarde RG, Weisberg SB, Montagne DE, Cadien DB, Dalkey A (2005) The prevalence of non-indigenous species in southern California embayments and their effects on benthic macroinvertebrate communities. Biol Inv 7:679–686

    Article  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc B 273:2453–2459

    Article  PubMed  Google Scholar 

  • Rudman WB (1972) The genus Philine (Opisthobranchia, Gastropoda). Proc Malac Soc Lond 40:171–187

    Google Scholar 

  • Rudman WB (1998) Comment on the identity of Californian Philine auriformis. (http://www.seaslugforum.net/find/200)

  • Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasions of coastal marine communities in North America: apparent patterns, processes, and biases. Ann Rev Ecol Syst 31:481–531

    Article  Google Scholar 

  • Saunders GW (2007) Routine DNA barcoding of Canadian Gracilariales (Rhodophyta) reveals the invasive species Gracilaria vermiculophylla in British Columbia. Mol Ecol Res 9:S140–S150

    Article  Google Scholar 

  • See KE, Feist BE (2010) Reconstructing the range expansion and subsequent invasion of introduced European green crab along the west coast of the United States. Biol Inv 12:1305–1318

    Article  Google Scholar 

  • Simmons MP, Pickett KM, Miya M (2004) How meaningful are Bayesian support values? Mol Biol Evol 21:188–199

    Article  PubMed  CAS  Google Scholar 

  • Sisson CG (2002) Dichotomous life history patterns for the nudibranch Dendronotus frondosus (Ascanius, 1774) in the Gulf of Maine. Veliger 45:290–298

    Google Scholar 

  • Stepien CA, Tumeo MA (2006) Invasion genetics of Ponto-Caspian gobies in the Great Lakes: a ‘cryptic’ species, absence of founder effects, and comparative risk analysis. Biol Invasions 8:61–78

    Google Scholar 

  • Strub PT, James C (2000) Altimeter-derived variability of surface velocities in the California Current System: 2. Seasonal circulation and eddy statistics. Deep-Sea Res II 47:831–870

    Article  Google Scholar 

  • Suter HH (1909) Descriptions of new species and subspecies of New Zealand Mollusca, with notes on a few species. Proc Malacol Soc 8:253–265

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. doi:10.1093/molbev/msr121

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 24:4876–4882

    Article  Google Scholar 

  • Trowbridge CT (1997) Dietary induction of opisthobranch morphology: Placida dendritica (Alder & Hancock, 1843) on different green algal hosts. J Molluscan Stud 63:29–38

    Article  Google Scholar 

  • Turner LM, Wilson NG (2007) Polyphyly across oceans: a molecular phylogeny of the Chromodorididae (Mollusca, Nudibranchia). Zool Scripta 37:23–42

    Google Scholar 

  • Valdés Á (2003) Preliminary molecular phylogeny of the radula-less dorids (Gastropoda: Opisthobranchia), based on 16S mtDNA sequence data. J Molluscan Stud 69:75–80

    Article  Google Scholar 

  • Voisin M, Engel CR, Viard F (2005) Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects. Proc Natl Acad Sci 102:5432–5437

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank R. Willan, B. Pernet, Y. Ralph, H. Weiskel and J. Goddard for collecting and sharing specimens, R. Portela Miguez for assistance with loaned material from the Natural History Museum of London, and C. Stepien and an anonymous reviewer for suggestions that greatly improved the manuscript. This study was supported by awards to PJK from the US National Science Foundation (OCE 06-48606 and 11-30072, DEB 08-17084), a faculty-student collaborative grant from the California State University Program for Education and Research in Biotechnology (CSUPERB), and an NSF GK-12 fellowship to J. Asif.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, California State University, Los Angeles, CA, 90032-8201, USA

    Patrick J. Krug, Jamal H. Asif & Isabel Baeza

  2. Auckland War Memorial Museum, Auckland, New Zealand

    Margaret S. Morley & Wilma M. Blom

  3. California Academy of Sciences, Golden Gate Park, San Francisco, CA, 94118, USA

    Terry M. Gosliner

Authors
  1. Patrick J. Krug
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jamal H. Asif
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Isabel Baeza
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Margaret S. Morley
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wilma M. Blom
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Terry M. Gosliner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patrick J. Krug.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 40 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krug, P.J., Asif, J.H., Baeza, I. et al. Molecular identification of two species of the carnivorous sea slug Philine, invaders of the US west coast. Biol Invasions 14, 2447–2459 (2012). https://doi.org/10.1007/s10530-012-0242-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-012-0242-9

Keywords

Search

Navigation