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First records of Ptilohyale littoralis (Amphipoda: Hyalidae) and Boccardia proboscidea (Polychaeta: Spionidae) from the coast of the English Channel: habitat use and coexistence with other species

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Abstract

This paper presents the first record of Ptilohyale littoralis (Stimpson, 1853) and Boccardia proboscidea (Hartman, 1940) from the French coast of the eastern English Channel. This record is the second for P. littoralis in European waters following a record from the Netherlands, which is suspected as the site of initial introduction from the Atlantic coast of North America. The observed high densities (up to 270 ind. 0.25 m−2), together with the presence of ovigerous females, suggest that the species could be considered as naturalised in the area. Ptilohyale littoralis was consistently found in the same habitat (mussel beds) as Apohyale prevostii (Milne Edwards, 1830). There was an apparent spatial segregation between these two species and the melitid Melita palmata (Montagu, 1804), the latter being associated with boulders covered with mud. Boccardia proboscidea, native from the west coast of North America and Japan, has already been recorded in European waters (Spain, Ireland, North Sea and French coast of Bay of Biscay), but the present record is the first for the English Channel. The species was found inhabiting the same habitat as M. palmata, i.e. boulders covered with mud. Further investigations are, however, needed along the coast of the English Channel and the North Sea to clarify the pathways of introduction and the status (casual, naturalised or invasive) of P. littoralis and B. proboscidea in European waters.

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References

  • Arresti A (1989) Parhyale explorator, a new species of talitroid amphipod from the bay of Arcachon, France. Bull Mus Natl Hist Nat Sect A Zool Biol Ecol Anim 11:101–115

    Google Scholar 

  • Arribas LP, Donnarumma L, Palomo MG, Scrosati RA (2014) Intertidal mussels as ecosystem engineers: their associated invertebrate biodiversity under contrasting wave exposure. Mar Biodivers 44:203–211

    Article  Google Scholar 

  • Ashton GV, Stevens MI, Hart MC, Green DH, Burrows MT, Cook EJ, Willis KJ (2008) Mitochondrial DNA reveals multiple northern hemisphere introductions of Caprella mutica (Crustacea, Amphipoda). Mol Ecol 17:1293–1303

    Article  PubMed  CAS  Google Scholar 

  • Bailey-Brock JH (2000) A new record of the polychaete Boccardia proboscidea (family Spionidae), imported to Hawai’i with oysters. Pac Sci 54:27–30

    Google Scholar 

  • Blasi JC, O’Connor NJ (2016) Amphipods as potential prey of the Asian shore crab Hemigrapsus sanguineus: laboratory and field experiments. J Exp Mar Biol Ecol 474:18–22

    Article  Google Scholar 

  • Borthagaray AI, Carranza A (2007) Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Acta Oecol 31:243–250

    Article  Google Scholar 

  • Bosc LAG (1802) Histoire naturelle des vers, contenant leur description et leurs mœurs, avec figures dessinées d’après nature. Deterville, Paris

    Book  Google Scholar 

  • Bouma TJ, Olenin S, Reise K, Ysebaert T (2009) Ecosystem engineering and biodiversity in coastal sediments: posing hypotheses. Helgol Mar Res 63:95–106

    Article  Google Scholar 

  • Bousfield EL, Hendrycks EA (2002) The talitroidean amphipod family Hyalidae revised, with emphasis on the North Pacific fauna: systematics and distributional ecology. Amphipacifica 3:17–134

    Google Scholar 

  • Buschbaum C, Dittmann S, Hong JS, Hwang IS, Strasser M, Thiel M, Valdivia N, Yoon SP, Reise K (2009) Mytilid mussels: global habitat engineers in coastal sediments. Helgol Mar Res 63:47–58

    Article  Google Scholar 

  • Carlton JT (2011) The global dispersal of marine and estuarine crustaceans. In: Galil BS, Clark PF, Carlton JT (eds) In the wrong place—alien marine crustaceans: distribution, biology and impacts. Springer, Dordrecht, pp 3–23

    Chapter  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, Plymouth

    Google Scholar 

  • Comtet T, Sandionigi A, Viard F, Casiraghi M (2015) DNA (meta) barcoding of biological invasions: a powerful tool to elucidate invasion processes and help managing aliens. Biol Invasions 17:905–922

    Article  Google Scholar 

  • Dauvin JC, Bellan-Santini D (2002) Les crustacés amphipodes Gammaridea benthiques des côtes Françaises métropolitaines: bilan des connaissances. Crustaceana 75:299–340

    Article  Google Scholar 

  • Dauvin JC, Dufossé F (2011) Hemigrapsus sanguineus (De Haan, 1835) (Crustacea: Brachyura: Grapsoidea) a new invasive species in European waters: the case of the French English Channel coast (2008–2010). Aquat Invasions 6:329–338

    Article  Google Scholar 

  • Dauvin JC, Dewarumez JM, Gentil F (2003) Liste actualisée des espèces d’Annélides Polychètes présentes en Manche. Cah Biol Mar 44:67–95

    Google Scholar 

  • Dauvin JC, Tous Rius A, Ruellet T (2009) Recent expansion of two invasive crab species Hemigrapsus sanguineus (de Haan, 1835) and H. takanoi Asakura and Watanabe 2005 along the Opal Coast, France. Aquat Invasions 4:451–465

    Article  Google Scholar 

  • De Haan W (1835) Crustacea. In: von Siebold PF Fauna Japonica sive Descriptio Animalium, quae in Itinere per Japoniam, Jussu et Auspiciis Superiorum, qui Summum In India Batava Imperium Tenent, Suspecto, Annis 1823–1830 Collegit, Notis, Observationibus et Adumbrationibus Illustravit

  • Dewarumez JM, Gevaert F, Massé C, Foveau A, Desroy N, Grulois D (2011) Les espèces marines animales et végétales introduites dans le bassin Artois-Picardie. UMR CNRS 8187 LOG et Agence de l’Eau Artois-Picardie

  • Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263

    Article  Google Scholar 

  • Elías R, Jaubet ML, Llanos EN, Sanchez MA, Rivero MS, Garaffo GV, Sandrini-Neto L (2015) Effect of the invader Boccardia proboscidea (Polychaeta: Spionidae) on richness, diversity and structure of SW Atlantic epilithic intertidal community. Mar Pollut Bull 91:530–536

    Article  PubMed  CAS  Google Scholar 

  • Faasse MA (2014) Introduction of Ptilohyale littoralis to The Netherlands. Mar Biodivers Rec 7:1–5

    Article  Google Scholar 

  • Fenchel TM, Kolding S (1979) Habitat selection and distribution patterns of five species of the amphipod genus Gammarus. Oikos 33:316–322

    Article  Google Scholar 

  • Galil BS, Marchini A, Occhipinti-Ambrogi A, Minchin D, Narščius A, Ojaveer H, Olenin S (2014) International arrivals: widespread bioinvasions in European Seas. Ethol Ecol Evol 26:152–171

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gestoso I, Olabarria C, Troncoso JS (2014) Selection of habitat by a marine amphipod. Mar Ecol 35:103–110

    Article  Google Scholar 

  • Gibson GD, Smith HL (2004) From embryos to juveniles: morphogenesis in the spionid Boccardia proboscidea (Polychaeta). Invertebr Biol 123:136–145

    Article  Google Scholar 

  • Gothland M, Dauvin JC, Denis L, Jobert S, Ovaert J, Pezy JP, Spilmont N (2013) Additional records and distribution (2011–2012) of Hemigrapsus sanguineus (De Haan, 1835) along the French coast of the English Channel. Manag Biol Invasions 4:305–315

    Article  Google Scholar 

  • Goulletquer P (2016) Guide des organismes exotiques marins. Belin, Paris

    Google Scholar 

  • Hänfling B, Edwards F, Gherardi F (2011) Invasive alien Crustacea: dispersal, establishment, impact and control. BioControl 56:573–595

    Article  Google Scholar 

  • Hartman O (1940) Boccardia proboscidea, a new species of spionid worm from California. J Wash Acad Sci 30:382–387

    Google Scholar 

  • Haswell WA (1885) On a destructive parasite of the rock-oyster (Polydora ciliata and Polydora polybranchia n. sp.). Proc Linnean Soc NSW 10:273–279

    Google Scholar 

  • Hatton J, Pearce B (2013) The first documented record of the non-native spionid Boccardia proboscidea in UK waters. Mar Biodivers Rec 6:1–4

    Article  Google Scholar 

  • Hewitt CL, Campbell ML, Thresher RE, Martin RB, Boyd S, Cohen BF, Currie DR, Gomon MF, Keough MJ, Lewis JA, Lockett MM, Mays N, McArthur MA, O’Hara TD, Poore GCB, Ross DJ, Storey MJ, Watson JE, Wilson RS (2004) Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia. Mar Biol 144:183–202

    Article  Google Scholar 

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637

    Article  PubMed  CAS  Google Scholar 

  • Jaubet ML, Garaffo GV, Vallarino EA, Elías R (2015) Invasive polychaete Boccardia proboscidea Hartman, 1940 (Polychaeta: Spionidae) in sewage-impacted areas of the SW Atlantic coasts: morphological and reproductive patterns. Mar Ecol 36:611–622

    Article  Google Scholar 

  • Johnston G (1838) Miscellanea Zoologica Aricadae. Mag Zool Bot 2:63–73

    Google Scholar 

  • Katsanevakis S, Gatto F, Zenetos A, Cardoso AC (2013) How many marine aliens in Europe? Manag Biol Invasions 4:37–42

    Article  Google Scholar 

  • Kerckhof F, Faasse MA (2014) Boccardia proboscidea and Boccardiella hamata (Polychaeta: Spionidae: Polydorinae), introduced mud worms new for the North Sea and Europe, respectively. Mar Biodivers Rec 7:1–9

    Article  Google Scholar 

  • Lagadeuc Y, Brylinski JM (1987) Transport larvaire et recrutement de Polydora ciliata (Annélide, Polychète) sur le littoral boulonnais. Cah Biol Mar 28:537–549

    Google Scholar 

  • Lincoln RJ (1979) British marine Amphipoda: Gammaridea. British Museum (Natural History), London

    Google Scholar 

  • Linnaeus C (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Editio decima, reformata. Laurentius Salvius: Holmiae

  • Little C, Kitching JA (1996) The biology of rocky shores. Oxford University Press, Oxford

    Google Scholar 

  • Lockwood JL, Hoopes MF, Marchetti MP (2007) Invasion ecology. Blackwell, Oxford

    Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton and Oxford

    Google Scholar 

  • Mainka SA, Howard GW (2010) Climate change and invasive species: double jeopardy. Integr Zool 5:102–111

    Article  PubMed  Google Scholar 

  • Martínez J, Adarraga I, López E (2006) Nuevos datos del género Boccardia Carazzi, 1893 (Polychaeta: Spionidae) para la península Ibérica y el Océano Atlántico. Bol Ins Esp Oceanogr 22:53–64

    Google Scholar 

  • Milne Edwards H (1830) Extrait de recherches pour servir à l’histoire naturelle des crustacés amphipodes. Ann Sci Nat 20:353–399

    Google Scholar 

  • Minchin D, Cook EJ, Clark PF (2013) Alien species in British brackish and marine waters. Aquat Invasions 8:3–19

    Article  Google Scholar 

  • Montagu G (1804) Description of several marine animals found on the south coast of Devonshire. Trans Linnean Soc Lond 7:61–85

    Article  Google Scholar 

  • Noël PY (2011) Checklist of cryptogenic and alien Crustacea of the European Atlantic coast. In: Galil BS, Clark PF, Carlton JT (eds) In the wrong place—alien marine crustaceans: distribution, biology and impacts. Springer, Dordrecht, pp 345–375

    Chapter  Google Scholar 

  • Occhipinti-Ambrogi A (2007) Global change and marine communities: alien species and climate change. Mar Pollut Bull 55:342–352

    Article  PubMed  CAS  Google Scholar 

  • O’Connor NE, Crowe TP (2007) Biodiversity among mussels: separating the influence of sizes of mussels from the ages of patches. J Mar Biol Assoc UK 87:551–557

    Article  Google Scholar 

  • Olsgard F, Somerfield PJ, Carr MR (1997) Relationships between taxonomic resolution and data transformations in analyses of a macrobenthic community along an established pollution gradient. Mar Ecol Prog Ser 149:173–181

    Article  Google Scholar 

  • Örsted AS (1843) Annulatorum danicorum conspectus. Volume Fasc. 1 Maricolae (Quaestio ab universitate Hafniensi ad solvendum proposita et proemio ornata). Librariae Wahlianae. Hafniae, Copenhagen

  • Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, Williamson MH, Von Holle BM, Moyle PB, Byers JE, Goldwasser L (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19

    Article  Google Scholar 

  • Pezy JP, Dauvin JC (2015) Are mussel beds a favourable habitat for settlement of Hemigrapsus sanguineus (De Haan, 1835)? Aquat Invasions 10:51–56

    Article  Google Scholar 

  • Radashevsky VI (2012) Spionidae (Annelida) from shallow waters around British Islands: an identification guide for the NMBAQC scheme with an overview of spionid morphology and biology. Zootaxa 3152:1–35

    Google Scholar 

  • Rathke H (1843) Beiträge zur Fauna Norwegens. Amphipoda. Nova Acta Leopold 20:63–98

    Google Scholar 

  • Richardson DM, Pysek P, Carlton JT (2011) A compendium of essential concepts and terminology in invasion ecology. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton, 1st edn. Blackwell, Oxford, pp 409–420

    Google Scholar 

  • Saier B (2002) Subtidal and intertidal mussel beds (Mytilus edulis L.) in the Wadden Sea: diversity differences of associated epifauna. Helgol Mar Res 56:44–50

    Article  Google Scholar 

  • Sato-Okoshi W, Okoshi K (1997) Survey of the genera Polydora, Boccardiella and Boccardia (Polychaeta, Spionidae) in Barkley Sound (Vancouver Island, Canada), with special reference to boring activity. Bull Mar Sci 60:482–493

    Google Scholar 

  • Savaria MC, O’Connor NJ (2013) Predation of the non-native Asian shore crab Hemigrapsus sanguineus by a native fish species, the cunner (Tautogolabrus adspersus). J Exp Mar Biol Ecol 449:335–339

    Article  Google Scholar 

  • Schurin A (1935) Zur Fauna der Caprelliden der Bucht Peter der Grossen (Japanisches Meer). Zool Anz 122:198–203

    Google Scholar 

  • Seeley B, Sewell J, Clark PF (2015) First GB records of the invasive Asian shore crab, Hemigrapsus sanguineus from Glamorgan, Wales and Kent, England. Mar Biodivers Rec 8:1–4

    Article  Google Scholar 

  • Simon CA, Thornhill DJ, Oyarzun F, Halanych KM (2009) Genetic similarity between Boccardia proboscidea from Western North America and cultured abalone, Haliotis midae, in South Africa. Aquaculture 294:18–24

    Article  CAS  Google Scholar 

  • Stachowicz JJ, Tilman D (2005) Species invasions and the relationships between species diversity, community saturation, and ecosystem functioning. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland, pp 41–64

    Google Scholar 

  • Stimpson W (1853) Synopsis of the marine invertebrata of Grand Manan: or the region about the mouth of the Bay of Fundy, New Brunswick. Smithsonian Contrib Knowl 6:1–66

    Google Scholar 

  • Stimpson W (1857) On the crustacea and echinodermata of the pacific shores of North America. Boston J Nat Hist 6:1–92

    Google Scholar 

  • Thiel M, Dernedde T (1994) Recruitment of shore crabs Carcinus maenas on tidal flats: mussel clumps as an important refuge for juveniles. Helgoländer Meeresun 48:321–332

    Article  Google Scholar 

  • Weiher E, Keddy P (1999) Ecological assembly rules: perspectives, advances, retreats. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Wijsman JWM, Smaal AC (2006) Risk analysis of mussels transfer. Wageningen IMARES. Report number C044/06

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, Upper Saddle River

    Google Scholar 

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Acknowledgements

The authors thank S. Reubrecht, B. Doucet and V. Serreau for their help in the field, K. Butelle and V. Serreau for sorting macrofauna samples, and P.-G. Sauriau and F. Aubert for providing data from La Rochelle. We also thank the two anonymous referees and the associate editor who helped improve the manuscript. J.J. identified the specimens of P. littoralis in the framework of activities founded by the RESOMAR network.

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Correspondence to Nicolas Spilmont.

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Spilmont, N., Hachet, A., Faasse, M.A. et al. First records of Ptilohyale littoralis (Amphipoda: Hyalidae) and Boccardia proboscidea (Polychaeta: Spionidae) from the coast of the English Channel: habitat use and coexistence with other species. Mar Biodiv 48, 1109–1119 (2018). https://doi.org/10.1007/s12526-016-0557-3

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