European expansion of the introduced amphipod Caprella mutica Schurin 1935

The amphipod Caprella mutica is one of the most rapidly invading species in Europe and has extended its range throughout North Sea and Celtic Sea coasts and the English Channel in less than fourteen years. It was first described from sub-boreal areas of north-east Asia in 1935 and has since spread to both northern and southern hemispheres. The first European record was from The Netherlands in 1994. Since then it has spread within the North Sea and later to the west coast of Scotland and to Ireland. C. mutica is frequently associated with man-made structures and is found in abundance on boat hulls, navigation/ offshore buoys, floating pontoons and aquaculture infrastructure. It is highly likely that its dispersal is associated with vessel movements whilst attached to hull fouling. This species is expected to colonise the west coasts of France and Spain and offshore islands in the north-east Atlantic.


Introduction
The caprellid amphipod Caprella mutica Schurin 1935 (Figure 1) is indigenous to sub-boreal waters of north-east Asia (Peter the Great Bay, Vladivostok, Russia) and was subsequently identified in the neighbouring Possjet Bay, Japan (Vassilenko 1967) and Akkeshi Bay, Japan (Arimoto 1976).The first reports of C. mutica outside its native habitat were from the Pacific and Atlantic coasts o f North America in the 1970s (Carlton 1979) and 1980s (Marelli 1981, Cohen and Carlton 1995) and a recent review of its global distribution has shown that within 40 years this species has spread throughout the northern hemisphere and it has recently been found for the first time in New Zealand (Ashton et al. 2007a).
C. mutica is one of the largest caprellid amphipods, mature males attain body lengths of up to 50 mm (Nishimura 1995).Females are highly fecund, producing their first brood approximately 53 days post-hatching at an average body length of 8.5 mm and at a seawater temperature of 13-14°C (Cook et al. 2007).Each female has an average of two sequential broods released at approximately 20 day intervals.The maximum number of recorded hatchlings produced by a single female at a seawater temperature of 13.0±0.5°C is 82.Juveniles typically emerge from the brood pouch at a body length of approximately 1.3 mm (Cook et al. 2007).C. mutica is able to survive for up to 20 days without additional food under laboratory conditions (Cook et al. 2007) and tolerates temperatures of < 2°C to 28°C and salinities down to 19 psu over a short (48 h) exposure period (Ashton et al. 2007b).C. mutica is an aggressive species, out-competing the native European caprellid Caprella linearis for space, even at low densities (Shucksmith in press).In the native range, this species is typically associated with either attached or drifting macro algae, including Sargassum spp. or aquaculture structures, such as the ropes used for the culture o f the macroalga Undaria spp. in Otsuchi Bay (Kawashima et al. 1999).In regions outside its native range, it has been found associated with areas of anthropogenic activity, such as harbours, marinas, navigation buoys and aqua culture sites (W illis et al. 2004, Àshton 2006, K erckhof et al. 2007).
Carlton (1979) suggested that C. mutica arrived on the Pacific and Atlantic coasts of North America either as a result of numerous independent cross-oceanic introductions with oyster spat, or from small scale transport following its first introduction (Carlton 1996).Direct sequencing of mitochondrial DNA indicates that C. mutica was introduced to Europe either directly from Asia or from the Atlantic coast o f North America (Ashton 2006).Opportunities for the spread of non-native species to Europe across the Atlantic have existed for more than 500 years with early exploration and the subsequent establishment of shipping routes (Stoner et al. 2002).For a little more than a century ships' ballast water has C. mutica was first identified in European waters in 1994 in a harbour at Neeltje Jans in The Netherlands (M.Faasse, pers.obs.).In a review by Ashton et al. (2007a) its general occurrence in Europe is described.In this account, we report all known localities for this species in European waters and discuss the likely dispersal mechanisms involved in its further spread.

Methods and Materials
Published records and unpublished reports were consulted for verifiable material.Researchers w ith recorded sightings o f C. mutica were contacted for further information and if possible, specimens were obtained for confirmation of identification using the taxonomic key by Arimoto (1976).

Results
One hundred and twenty-one records of Caprella mutica were found for European waters (Annex), including eleven new localities for 2007.Confirmed records for C. mutica are from the North Sea, English Channel, Irish Sea, the west coast o f Scotland and Ireland (Figure 2) and range from 49°29'N to 62°22'N and 10°04'W to 8°26'E.While C. mutica was not found at all localities surveyed within this range, the region comprising the greatest number of records was the south-western North Sea.There are presently no records for the Baltic Sea, the Iberian Peninsula or the M editerranean Sea.
The majority of the European records occur in areas with human activity, such as marinas, ports and shipping routes.In Norway and the west coast of Scotland, C. mutica is associated with aquaculture activity, principally fish cage netting and mussel lines.This species has also been found on natural substrata within the sub-littoral zone on the macroalga Plocamium spp.(K.Boos, pers. obs.) and attached to drifting surface accumulations of macroalgae (Ashton 2006).

Dispersal of Caprella mutica within Europe has been rapid
and represents -1,200 km range extension to the west coast of Norway and -1 ,000 km to the west coast of Ireland from where it was first recorded in The Netherlands.C. mutica has been found on boat hulls, fish cage netting, marina pontoons, navigation buoys, harbour structures and to attached floating macroalgae.Its abundance on artificial structures is notable and may explain its ability to spread rapidly.C. mutica lacks a planktonic stage, the young hatch onto the substrate in the form of small adults, and their long-range distribution most probably depends on the movement of floating artificial structures, such as vessels, whilst attachment to floating marine algae may account for more localised movements.
A genetic study indicates two likely routes for the introduction of this species to Europe, including cross-oceanic introductions either directly from Asia or via the Atlantic coasts of the United States (Ashton 2006).Shipping has been identified as an important pathway for the transoceanic introduction of non-native species (Drake and Lodge 2004).Many of the areas in Europe where C. mutica has been introduced are close to busy ports suggesting that ballast water transport and/ or hull fouling could be involved.Living Caprella spp.have been found in ships' ballast tanks (Carlton 1985) and in sea-chests in a study in New Zealand (Courts et al. 2003).
W ithin its native environment, C. mutica may be found attached to the macroalgae Ulva spp.and the filamentous Cladophora spp.and these are regularly found attached to ships hulls (Mineur et al. 2007).It has also been seen associated with other algae at high densities on recreational boat hulls (M inchin and Holmes 2006, G Ashton, pers. obs. and R Shucksmith, pers. comm.) and in the Adriatic Sea Caprella scaura is thought to have been spread on the hulls o f leisure craft (Sconfietti et al. 2005).
Stock movements of cultured species have also been identified as one means of globally spreading non-native species (Ruiz andHewitt 2002, M inchin 2007a).Introduction of C. mutica to the United States has been potentially linked to the importation of the Pacific Oyster, C. gigas for culture purposes (Carlton 1987).Elsewhere there are several examples of species being inadvertently spread with oysters that include algae (Scagel 1956, Druehl 1973, Critchley 1983), molluscs (Cole 1942), bryozoa (De Blauwe and Faasse 2004) and crustaceans (Gruet et al. 1976).The Oosterschelde region in The Netherlands has received extensive shellfish imports and these movements may have been responsible for the introduction of C. mutica to Europe (W olff 2005).However, this region was regularly sampled between 1990-1995 and C. mutica was not found (M.Faasse, pers.obs.).This suggests that the introduction to Europe of C. mutica is more likely to be via commercial shipping rather than stock movements of cultured species.
Dispersal of C. mutica within Europe has been rapid.It is likely, therefore, that commercial and recreational vessels will continue to spread this species to unoccupied areas within its present range, as well as, to localities beyond where it presently occurs particularly in the summer months, when there is the greatest leisure vessel activity and highest densities of C. mutica.On the west coast of Scotland, their abundance can reach 300,000 individuals m"2 and fish farm cages (Ashton 2006) and other structures can be dominated by this species between July and August (Cook et al. 2006) (Figure 3).It is possible though, that the rapid range expansion to fish farm installations in Scotland (W illis et al. 2004), Ireland (Tierney et al. 2004) and in Norway (A.Jelmert, pers.comm.) and navigation buoys in Belgium and The Netherlands (F.Kerchkof, pers.obs.) may be with movements of service craft.In California, USA, the appearance of C. mutica on oil platforms offshore is thought to be due to transmissions with service craft from harbours (C. Culver, pers. comm.).Such expansion to offshore facilities may create a 'stepping-stone' effect, thereby enhancing opportunities for further range extensions.Spread could also be aided by attachment to drift algae but it is unclear how far C. mutica could be dispersed in this way, although algal rafts are known to persist for long durations (Ingolfsson 1995).
The present records of C. mutica all occur within the current global range of this species.Its tolerance to a wide range of temperatures and capability of surviving in marine to brackish water (Ashton et al. 2007b) would indicate that it is likely to expand its range further within Europe.It is unlikely to survive in the central and eastern Baltic Sea due to low salinities (FIMR 2006), and based on current knowledge it is not expected to become established in the Mediterranean Sea on account of the high summer seawater temperatures (Cook et al. 2006).The abundance of C. mutica on artificial substrata would indicate that conditions on such structures are in some way particularly suited for their survival and development, such as the lack of benthic predators.Should hull fouling be important in its range expansion it may be expected that their northward expansion in Norway will be slow, when compared with the north and west coasts of France and the Iberian Peninsula where there is a higher level of leisure craft and shipping activity.Other additional factors, that might limit their range expansion and/ or establishment in natural habitats include substrate features (Caine 1978), wave exposure (Takeuchi et al. 1987, Guerra-García 2001), high levels of predation (Guerra-García and Garcia-Gómez 2001) or port toxicity (Ohji et al. 2003).

Conclusions
Caprella mutica has become established in the North Sea, west coasts of Scotland and Ireland, in the Irish Sea and English Channel in less than 14 years.Since this species has a tolerance for a wide range of temperature and salinity, it is likely that it will expand its current range further north in Norway, to several Atlantic islands, the Bay of Biscay and the Iberian Peninsula; but it may not become established in the M editerra nean Sea or in the eastern Baltic Sea, where salinities fall below 19 ppt.C. mutica is thought to expand its range rapidly either by attachment to vessels or with drifting algae.It out-competes native caprellids under laboratory conditions and it is likely to behave in the same way in the field where it attains high densities.W hilst the wider environmental implications of C. mutica have not yet been confirmed, it is likely that it has an important impact on benthic communities.

F
ig u r e 1. M ale (to p ) an d fem ale (b o tto m ) C a p re lla m u tica (P hoto: T. N ick eli) transm itted many different crustacean taxa, including caprellids (Coutts et al. 2003) and in the last half-century ocean barges and oil platforms (or sim ilar structures) have been moved across oceans (Rodriguez and Suaréz 2001, Ruiz and Hewitt 2002) and may have introduced C. mutica to Europe.The im portation of different species of half-grown oysters as deck cargo since ~1870s (Loosanoff 1975) and of Pacific oysters (Crassostrea gigas) from British Columbia in the 1960 s and later directly from Japan in the 1970s into Europe, may also have provided opportunities for introduction (W olff 2005).C. mutica lacks a free-swimming plankto nic larval stage and secondary movements are also likely to involve human activities, such as shipping, aquaculture activities and recreational boating or may otherwise be associated with drifting macroalgae (Ashton 2006).

F
ig u r e 2. E u ro p ean d istrib u tio n o f C a p rella m utica.S olid c irc le s show co n firm ed sig h tin g s (in c lu d in g dates f o r firs t re c o rd in th e c o u n try ) an d d o tte d circ le s show re g io n s w h ere C. m u tica h as n o t b e e n re c o rd e d to date

F
ig u r e 3. E x p erim en tal fram e d ep lo y ed w est o f Z eeb ru g g e , B e lg iu m in 2 0 0 7 sh o w in g dense ag g re g a tio n s o f C a p rella m u tica a fte r 12 w eek s im m ersio n (P hoto: F. K erck h o f) A renas F, B ishop JD D, C arlton JT, D yrynda PJ, F arnham WF, G onzalez DJ, Jacobs M W , L am bert C, L am bert G, N ielsen SE, P ederson JA, P orter JS, W ard S and W ood C A (2006) A lien species and o ther notable records from a rap id assessm ent survey o f m arinas on the south coast o f England.Journal o f the M arine B iological A sso ciatio n o f th e U nited K ingdom 86: 1329 -1337 A rim oto I (1976) T axonom ic studies o f caprellids (C rustacea, A m phipoda, C aprellidae) found in the Japanese adjacent w aters.S pecial publications from th e Seto M arine B io lo g ical L aboratory Series III, N ippon P rinting & P u b lish in g Co., Ltd, O saka, Japan, 111 p A shelby CW (2005) The occurrence and d istrib u tio n o f no n nativ e fau n a in H arw ich H arbour and the S tour and O rw ell estuaries, including new records o f C aprella m utica Schurin 1935 and B u g u la stolonifera R yland 1960.E ssex N atu ralist 22: 103-116 A shton GV (2006) D istribution and dispersal o f the n o n n ative cap rellid am phipod, C aprella m utica Schurin, 1935.PhD T hesis, A berdeen, 192 p A shton GV, Boos K, S hucksm ith R and C ook E J (2006) R apid assessm en t o f the distribution o f m arine non-native species in m arinas in S cotland.A quatic Invasions 4: 209-213 A shton GV, W illis K J and C ook E J (2007a) G lobal D istribution o f the Japanese S keleton Shrim p, C aprella m utica (C rustacea, A m phipoda, C aprellidae) w ith a detailed account o f the d istrib u tio n in S cotland, U.K. H y drobiologia 590: 31-41 A shton GV, W illis K, B urrow s M and C ook E J (2007b) E nvironm ental tolerance o f C aprella m u tica : im plications for its d istribution as a non-native species.M arine E nvironm ental R esearch 64: 305-312 B uschbaum C and G utow L (2005) M ass occurrence o f an introduced crustacean {C aprella cf.m u tica ) in the sou th eastern N orth Sea.H elgoland M arine R esearch 59: 252-253 C aine EA (1978) H abitat adaptations o f N orth A m erican caprellid A m phipoda (C rustacea).B iological B ulletin 155: 288-296 C arlton JT (1979) H istory, biogeography, and ecology o f the introduced m arine and estuarine invertebrates o f the P acific C oast o f N orth A m erica.PhD T hesis, U niversity o f C alifornia.C arlton JT (1985) T ransoceanic and interoceanic dispersal o f coastal m arine organism s: the bio lo g y o f ballast w ater.O ceanogr M ar Biol.A n A nnual R eview 23: 313-371 C arlton JT (1987) P atterns o f tran so cean ic m arine biological invasions in the Pacific ocean.B ulletin M arine Science 41: 452-465 C arlton JT (1996) B iological Invasions and C ryptogenic Species.E cology 77: 1653-1655 C ohen AN and C arlton JT (1995) N onindigenous aquatic species in an U nited S tates E stuary: A case study o f the b io lo g ical invasions o f th e San F rancisco B ay and D elta.A R eport for th e U nited S tates fish and w ildlife service, W ashington D.C. and The national sea grant college p rogram C onnecticut sea grant.A vailable online: h ttp ://w w w .anstask fo rce.g o v /sfin v ad e.h tm , 246 p C ole H A (1942) The A m erican w h elk tingle, U rosalpinx cinerea (Say), on B ritish oyster beds.Journal o f the M arine B iological A ssociation o f the U n ited K ingdom 25: 477-508 C ook EJ, B lack KD, Sayer M D J, C rom ey C J, A ngel DL, S panier E, T sem el A, K atz T, E den N, K arakassis I, Y T sapakis M, A postolaki ET and M alej A (2006) The influence o f caged m ariculture on the early developm ent o f sublittoral fouling com m unities: a pan-E uropean study.ICES Journal o f M arine Science 63: 637-649 C ook EJ, W illis K J and L ozano-F em andez M (2007) Survivorship, G row th and R eproduction o f th e N on-N ative C aprella m utica Schurin (C rustacea: A m phipoda).H y drobiologia 590: 55-64 C outts ADM , M oore KM and H ew itt CL (2003) Ships' seachests: an overlooked tran sfer m echanism fo r n o n indigenous m arine species?M arine P ollution B ulletin 4 6 :1 5 0 4 -1 5 1 5 C ritchley A T (1983) Sargassum m u ticu m : a taxonom ic histo ry including w orld-w ide and w estern Pacific distributions.Journal o f th e M arine B iological A ssociation o f the U nited K ingdom 63: 617-625 De B lauw e H and F aasse M A (2004) S m itto id ea p ro lifica O sburn, 1952 (B ryozoa, C heilostom atida), a Pacific bryozoan introduced to The N etherlands (N ortheast A tlantic).B ulletin van h e t K oninklijk B elgisch Instituut voor N atu urw etenschappen, B iologie 74: 33-39 D rake JM and L odge DM (2004) G lobal h ot spots o f biological invasions: evaluating options fo r ballast-w ater m anagem ent.Proceedings o f the R oyal S ociety L ondon B 271: 575-580 D ruehl L (1973) M arine tran sp lan tatio n s.Science 179: 12 FIM R (2006) F IM R m o nitoring o f the B altic Sea environm ent -A nnual R eport 2006.F innish Institute for M arine R esearch, H elsinki G ruet Y, H eral M and R obert J-M (1976) P rem ières observ atio ns sur l'introduction de la faune associée au n ), im porté sur la côte A tlantique Française.C ahiers de B iologie M arine 17: 173-184 G u erra-G arcía JM (2001) H abitat use o f the C aprellidea (C ru stacea : A m phipoda) from C euta, N orth A frica.O p h elia 55: 27-38 G u erra-G arcía JM and G arcía-G óm ez J (2001) The spatial distrib u tio n o f C aprellidae (C rustacea: A m phipoda): a stress b io in d icato r in C eu ta (N orth A frica, G ibraltar A rea).M arine E cology-P ubblicazioni D ella S tazione Z o o lo g ica Di N apoli 22: 357-367 H eilsch er S (2000) S ustainability o f the brow n seaw eed L a m in a ria saccharina fo r cultivation in th e effluents o f an A tlan tic salm on ongrow th farm .A field study in S o u th eastern N orw ay, In stitu t fü r B iologie, F reiburg im B reisgau H éral M (1990) T raditional oyster culture in France.In: B arnabé (ed) A quaculture, pp 342-387, E llis-H orw ood, L ondon In g o lfsso n A (1995) F loating clum ps o f seaw eed around Icelan d -n atu ral m icrocosm s and a m eans o f dispersal fo r shore fauna.M arine B iology 122: 13-21 K aw ash im a H, T akeuchi I and O hnishi M (1999) F atty acid com positions in fo u r o f caprellid am phipod species (C rustacea) from O tsuchi and M utsu bays in northern Japan.Journal o f Japanese O il C hem istry S ociety 48: 595-599 K erck h o f F, H aelters J and G ollasch S (2007) A lien species in the m arine and brackish ecosystem : th e situation in B elgian w aters.A quatic Invasions 2(3): 243-257 L o o san o ff V L (1975) Introduction o f C odium to N ew E ngland w aters.F isheries B ulletin 73: 215-218 M arelli D C (1981) N ew records for C aprellidae in C alifornia, and notes on a m orphological v arian t o f C aprella verrucosa B oeck, 1871.Proceedings o f th e B iological Society W ashington 94: 654-662 M inchin D (2007a) A quaculture and tran sp o rt in a changing environm ent: O verlap and links in th e spread o f alien biota.M arine P ollution B ulletin 55: 302-313 M inchin D (2007b) R apid coastal survey fo r targ eted alien species associated w ith flo atin g pontoons in Ireland.A quatic Invasions 2: 63-70 M inchin D and H olm es JM C (2006) The first record o f C aprella m utica Schurin 1935 (C rustacea: A m phipoda) from the east C oast o f Ireland.Irish N atu ralists' Journal 28: 321-323 M ineur F, B elsh er T, Johnson MP, M aggs C A and V erlaque M (2007) E xperim ental assessm ent o f oyster transfers as a v ecto r fo r m acroalgal introductions.B iological C onserv ation 137: 237-247 N ish im u ra S (1995) G uide to the S eashore A nim als o f Japan w ith C o lo u r P ictures and K eys.Vol.II.H oikusha, Japan O 'R eilly M (2007) The Japanese M acho S keleton Shrim p {C aprella m u tica ) in the C M arine P ollution B ulletin 46: 1263-1272 P latvoet D, de B ruyne RH and G m elig M eyling AW (1995) D escription o f a new Caprella-spQciQS from the N etherlands: C aprella m acho nov.spec.(C rustacea, A m phipoda, C aprellidae).B ulletin o f the Z oological M useum , U n iv ersity o f A m sterdam 15: 1-4 R odriguez G and Suaréz H (2001) A nthropogenic dispersal o f decapod crustaceans in aquatic environm ents.In tercien c ia 26 282 Ruiz GM and H ew itt CL (2002) T ow ard understand in g patterns o f coastal m arine invasions: a prospectus.In: L eppâkoski E, G ollasch S and O lenin S (eds) Invasive aquatic species o f Europe.D istribution, im pacts and m anagem ent, K luw er A cadem ic P ublishers, D ordrecht, The N etherlands Scagel RF (1956) Intro d u ctio n o f a Japanese alga, Sargassum m uticum into the n o rth east P acific.F isheries R esearch Papers.D epartm ent o f F isheries, State o f W ashington 1C aprella m utica in der D eutschen B ucht und seine p o ten tielle A nsiedlung in natürlich en H abitaten.D iplom a T hesis, R ostock U niversity S churin A (1935) Z ur F auna der C aprelliden der B ucht Peter der G rossen (Japanisches M eer).Z oologischer A nzeiger 122: 198-203 S confietti R, M angili F, Savini D and O cchipinti-A m brog i A (2005) D iffusion o f the alien species C aprella scaura T em pleton, 1836 (A m phipoda:C aprellidae) in the N orthern A driatic Sea.B iología M arina M editerran ea 12: 335-337 Shucksm ith R (in press) B iological Invasions: The role o f b io d iv ersity in d eterm ining com m unity su scep tib ility to invasion PhD T hesis, A berdeen S toner D, B en-S hlom o R, R inkevich B and W eissm an I (2002) G enetic v ariab ility o f B o tryllu s schlosseri invasions to the east and w est coasts o f the U SA. M arine E cology P rogress Series 243: 93-100 T akeuchi I, K uw abara R, H irano R and Y am akaw a H (1987) Species com positions o f the C aprellidae (C rustacea: A m phipoda) o f the Sargassum zone on the P acific coast o f Japan.B ulletin o f M arine Science 41: 253-267 T ierney TD, K ane F, N aughton O, K ennedy S, O 'D onohoe P, C opley L and Jackson D (2004) O n the occurrence o f the caprellid am phipod, C aprella m utica S churin 1935, in Ireland.Irish N atu ralists' Journal 27: 437-439 V assilenko SV (1967) F auna o f C aprellidae (A m phipoda) o f the P ossjet B ay (S ea o f Japan) and som e data on th eir ecology.Issledovanija Fauny M orei (E xplorations o f the fauna o f th e seas o f th e U S S R ), B iotzenozy Z alik a P ossjet Japanskovo M orja 5: 196-229 W G ITM O (2003) R eport o f th e ICES W orking G roup on Introductions and T ransfers o f M arine O rganism s, V ancouver, C anada, 158 p W illis KJ, C ook EJ, L ozano-F ernandez M and T akeuchi I (2004) F irst record o f the alien caprellid am phipod, C aprella m utica, for th e UK.Journal o f th e M arine B iological A ssociation o f the U nited K ingdom 84: 1027-1028 W o lff W J (2005) N on-indigenous m arine and estuarine species in The N etherlands.Z oologische M ededelingen L eiden 79: 1-116 AnnexE uropean d istrib ution records o f C aprella m utica including location, latitude and longitude, date o f rep o rtin g and site d escription (if know n).C o n firm ed n on-sightings are also included.