JOURNAL OF BIOLOGY, 22(1): 184Ð189, 2002

A NEW ALIEN IN EUROPE: SANGUINEUS (: BRACHYURA: GRAPSIDAE)

Gérard Breton, Marco Faasse, Pierre Noël, and Thierry Vincent

(GB, TV) Muséum d’histoire naturelle, Place du vieux marché, F-76600 Le Havre, France (e-mail: [email protected]); (MF) Schorerstraat 14, NL-4341 GN Arnemuiden, Nederland (e-mail: [email protected]); (PN) Biologie des invertébrés marins (ESA CNRS 8044), Muséum National d’Histoire Naturelle, 55 rue Buffon, F-75005 Paris, France (e-mail: [email protected])

ABSTRACT The Asian shore crab Hemigrapsus sanguineus is recorded for the first time in two European lo- calities, Le Havre in France and the former estuary “Oosterschelde” in the Netherlands. While breed- ing populations occur in the former, only two male specimens were found in the latter. In both places, this alien species was mixed with the common shore crab Carcinus maenas.

Species of the genus Hemigrapsus had Perophora japonica Oka, 1927 (Vincent, been confined to the Pacific Ocean until 1999; Vincent and Breton, 1999). They are Hemigrapsus sanguineus (de Haan, 1835) new migrants to the French coast of the Eng- was introduced to the eastern coast of North lish Channel over the last four decades. All America (Williams and McDermott, 1990; came from northwestern Pacific Ocean, and McDermott, 1991). This invasive Asian shore some of them transited via the eastern Ameri- crab was first discovered in New in can or British coasts. For approximately six- September 1988 and by 1990 a breeding teen alien species recorded in the area (the so- population was established. Recently Hemi- called cryptogenic species sensu Eno et al., grapsus sanguineus has also been found on 1997, excluded), Le Havre Harbour is often European coasts, in Le Havre, France, and the the first or the only observation site (Breton former estuary “Oosterschelde” in the Nether- and Vincent, 1999), with several ecological lands. studies using SCUBA-diving (Breton, 1981; Its congener H. penicillatus (de Haan, Breton et al., 1995). 1835), also an alien species to Europe, was Alien species in the southwestern Delta discovered in La Rochelle, on the Atlantic area in the Netherlands, originating from the coast of France, in March 1994 (Noël et al., northwestern Pacific Ocean, include the algae 1997). By December 1996, it had spread Sargassum muticum and Undaria pinnatifida, southward to northeastern Spain and north- the anthozoan Haliplanella lineata (Verrill, ward to Fromentine, covering a distribution 1869), the Eriocheir sinensis H. range of some 800 km. It was recorded sub- Milne Edwards, 1854, and Caprella acan- sequently in Le Havre (Vincent and Breton, thogaster Mayer, 1890 (= C. macho Platvoet, 1999) and recently in Nederland (Nijland and De Bruyne, and Gmelig Meyling, 1995), and Beekman, 2000). Its ultimate distribution is the ascidian Styela clava. likely to extend from western Norway to Mo- rocco (Noël et al., 1997). The southwestern MATERIALS AND METHODS Delta area in the Netherlands would also pro- Le Havre Harbour (Fig. 1) is located at 49°29′N, vide suitable habitats (d’Udekem d’Acoz, 0°07′E close to the estuary of the River Seine, on the Nor- 1998). man coast of the . Le Havre basins fall into two main categories: 1) the basins in direct com- Alien species found in the docks of Le munication with the sea, with 32Ð34 ppt salinity and same Havre Harbour include the algae Sargassum tidal range as in the open sea (= “bassins de marée”); 2) muticum (Yendo) Fensholt and Undaria pin- the basins isolated from the sea by locks, with weak (1.5 natifida (Harvey) Suringar in Okamura, the m) to very weak (0.3 m) water-level range and with salin- ity decreasing irregularly eastwards (= “bassins à flot”). polychaete Hydroides ezoensis Okuda, 1934, More details on the ecological characteristics of the basins the crab Hemigrapsus penicillatus, and the are provided by Breton et al. (1995). Specimens were col- ascidians Styela clava Herdman, 1882, and lected mainly at two sites of the Harbour named Môle

184 BRETON ET AL.: HEMIGRAPSUS SANGUINEUS IN EUROPE 185

Central and Roro 4, respectively by lifting boulders at the Anthony Brière, on 29th August 1999, in a water edge during low tide, and by SCUBA diving. tidal basin, at the Môle Central. Several spec- Several apparently suitable localities for Hemigrap- sus spp. in the Netherlands were visited during the pre- imens were then collected under stones, dur- sent survey (AprilÐOctober, 1999). The Delta area of the ing low tide, at the water edge. The Môle rivers Rhine, Meuse, and Scheldt is situated in the Nether- Central is located at about 700 m downstream lands, some 200 km northeast of the English Channel, of a power station release, which is more or along the southern Bight of the . In the Delta area suitable habitats for Hemigrapsus were expected to less canalized. The substrate is a muddy be found in the estuary “Westerschelde”, and the former shelly sand. At the power station release estuary “Oosterschelde” (Fig. 1). The sites Bath, Walso- point, according to the season and the power orden, Borssele, Vlissingen, and Zoutelande along the for- station activity, the temperature increase is mer and the sites Anna Frisopolder, Westbout, Burghsluis, 2Ð11°C compared to the sea. At the Môle Schelphoek, and Strijenham along the latter were vis- ited. All sites were investigated by lifting boulders in the Central, it is far less, but still appreciable, littoral zone during low tide. A few, i.e., Zoutelande and especially at low tide. By lifting boulders at all sites in the Oosterschelde, were investigated during the water edge for approximately one hour high tide as well, by SCUBA-diving whenever the un- at low tide, Anthony Brière on 31.08.1999 derwater visibility permitted. Each site was investigated for at least one hour. and one of us (GB) on 01.09.1999 observed several dozens of adult . In addition to RESULTS the two specimens now housed in the Identification Muséum National d’Histoire Naturelle, Paris, On the sea-shore, crabs of the genus Hem- fifteen specimens were collected in this sur- igrapsus can be distinguished from the abun- vey and are in the collections of the Muséum dant shore crabs, Carcinus maenas (Linnaeus, d’Histoire Naturelle du Havre. [MH 1758) by the shape of the carapace and the D/068.001.009: 6 males, 21Ð31.5-mm CW, pigment pattern. Careful examination re- and 3 nonovigerous females, 20Ð24-mm CW, vealed that the morphological characteristics 31.08.99.—MH D/068.010.015: 6 males, of the specimens collected agree quite well 23Ð30-mm CW, 01.09.99]. with the description and color illustrations of The ovigerous females were left or released Hemigrapsus sanguineus (de Haan, 1835; in situ, one of them had a 19-mm CW. Most Sakai, 1965, 1976; McDermott, 1998a, b): the females found in the beginning of Septem- carapace is square, with three teeth on each ber 1999 were ovigerous. The crabs were side and mottled color, greenish to red-brown abundant (one per 4Ð5 stones, i.e., an ap- or dark-purple. Purple-red spots are present proximate maximum density at low tide of on the dorsal part of chelipeds; other 0.2Ð0.5 individual per m2), but shallow sub- pereiopods display a distinctive pattern of al- tidal zones were not explored. ternating light and dark transverse stripes. At the Môle Central, the following species Males have a fleshy vesicle at the base of the of decapod crustaceans were found with cheliped dactylus which is absent in females; Hemigrapsus sanguineus: Palaemon serratus a hair patch is present at the same place in (Pennant, 1777)[common], Athanas nitescens H. penicillatus (Fig. 2). The infraorbital ridge (Leach, 1814)[one], Carcinus maenas [abun- is also different in H. sanguineus and H. peni- dant, some specimens mating], Polybius cillatus (Fig. 3). Two H. sanguineus from Le (Necora) puber (Linnaeus, 1767)[one juve- Havre (one small male ~23-mm CW and one nile], Hemigrapsus penicillatus [abundant], larger male ~29-mm CW) deposited in the Porcellana platycheles (Pennant, 1777)[abun- collections of the Muséum National d’His- dant], Pilumnus hirtellus (Linnaeus, 1761)[a toire Naturelle (coll. no MNHN-B 27366) few specimens], Inachus phalangium (Fabri- were compared with reference specimens of cius, 1775)[one]. Males of H. sanguineus Hemigrapsus sanguineus (de Haan, 1835) were more abundant than females. This may kept in MNHN [male 29 mm CW, from not indicate an abnormal sex-ratio, but may Japan, 58-1897; coll. no MNHN-B 12841, E.- be due to a collecting bias. L. Bouvier det.] and found conspecific. Hemigrapsus sanguineus was also found on 24 October 1999 in a basin 6 km from the Populations of Hemigrapsus sanguineus in Môle Central, with a very weak tidal range Le Havre and a salinity of 30 ppt at the so-called Roro Hemigrapsus sanguineus, new to the En- 4, on the south bank of the Canal Central glish Channel fauna, was first found by Mr. Maritime. Young males and adult females 186 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 1, 2002

Fig. 1. Location of first sites of Hemigrapsus sanguineus in Europe.

(20Ð25-mm CW) were found but were much tuary “Oosterschelde.” One male (RMNH less abundant than H. penicillatus (ratio 1:10 D48570), 21 mm in CW, was found on to 1:20) and Carcinus maenas. The crabs in- 21.08.99 during high tide and another male habited the cavities of a mussel colony of (RMNH D48273), 20 mm in CW, on 23.08.99 Mytilus edulis Linnaeus, 1758, at 1- to 4-m during low tide. Both specimens lived ap- depth. For the moment, this species is only proximately at 1 m below high water level, known at these two sites in Le Havre harbour. between boulders lying on the slope of a man- made basalt seadyke. The crabs seemed to be Specimens in Former Oosterschelde Estuary more active during high tide. The littoral Two specimens of H. sanguineus were dis- habitat was rather barren, the only other crus- covered at one site in the Delta area. The site, taceans noted being barnacles Elminius modes- called “Schelphoek” [~51°41′N, 03°49′E], is tus Darwin, 1854 [abundant], and common situated near the entrance of the former es- shore crabs Carcinus maenas [abundant]. BRETON ET AL.: HEMIGRAPSUS SANGUINEUS IN EUROPE 187

Fig. 3. Semidiagrammatic representation of cephalotho- rax in frontolateral view showing the suborbital stridu- lating organ (A) a finely striated crest in Hemigrapsus Fig. 2. External view of male left cheliped showing be- sanguineus and (B) a more or less smooth crest divided tween the fingers (A) the pulvinus (= fleshy vesicle or into three parts of unequal length in Hemigrapsus peni- membranous swelling) in Hemigrapsus sanguineus and cillatus [same specimens as in Fig. 2]. Scale bar = 5 mm. (B) the tuft of hair in Hemigrapsus penicillatus [H. san- guineus specimen n¡ = MNHN B.27429; H. penicillatus = an 18-mm CW male, collected in St. Georges de Di- donne, France, 9.05.1996]. Scale bar = 5 mm. sels, barnacles, and small crustaceans (Mc- Dermott, 1999). D’Udekem d’Acoz (1999; p. 253) thought that, from the U.S.A., it might Subsequent thorough investigations on the reach the European coasts by way of ship bal- site did not yield any more specimens of H. last waters. sanguineus. Can we now predict the colonization of the eastern Atlantic by Hemigrapsus sanguineus DISCUSSION in the future? On the European coasts, the Hemigrapsus sanguineus was likely to species meets ecological conditions similar to have settled in Le Havre Harbour in or before those of the northern Pacific Ocean (Lohrer 1998, because the 1999 population is adult et al., 2000) and of the east coast of North and breeding (including ovigerous females), America (Lohrer and Whitlach, 1997; Mc- but the settlement went unnoticed until August Dermott, 1995, 1998a); it is therefore proba- 1999. This species, native to the northwestern bly able to invade many places. Because lab- Pacific Ocean, was first reported outside its oratory observations showed that adults of H. original area near Cape May, , sanguineus survived salinity reductions down U.S.A., in 1988 and colonized subsequently to 10 ppt (McDermott, 1995, 1998a), the the northeast coast of the U.S.A. (McDermott, species may invade the Baltic Sea or similar 1998a). It covered more than 650 kilometres places with low salinity as well. In fact, the of coasts between 1988 and 1995, ranging majority of successful of from Cape Cod, Massachusetts, in the north north-west European coastal waters are more to Oregon Inlet, North Carolina, in the south; or less euryhaline. Wolff (1999) suggested the it feeds there primarily on algae, blue mus- availability of many empty niches in north- 188 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 1, 2002 west European brackish waters plays a prime and points out the importance of continuing role in the success of invasive species. investigations. In Le Havre Harbour, H. sanguineus lives in the same environment as two other crabs, ACKNOWLEDGEMENTS Carcinus maenas, which is of a larger size, We are endebted to the following persons/colleagues. and Hemigrapsus penicillatus, another alien Anthony Brière (Le Havre) made the first observations of the species in the harbour of Le Havre. Th. Hollem (Rot- species, which is smaller. Will there be any terdam) provided assistance during the SCUBA-dive near competition between this last immigrant and Schelphoek. F. Kerckhof (Oostende, Belgium) drew at- the other species? We have the experience of tention to the article of Gollasch. C. d’Udekem d’Acoz some places in Le Havre Harbour where (Braine-l’Alleud, Belgium) identified the Dutch speci- Hemigrapsus penicillatus have competed mens of H. sanguineus. D. Guinot made available refer- ence specimens from the Muséum National d’Histoire Na- since their settlement in 1997 with juveniles turelle for confirmation of the identification of specimens of Carcinus maenas of approximately the from Le Havre and helped in literature search. Finally, same size; after a couple of years, the devel- we also thank referees for their valuable criticisms and opment of both populations is well-balanced. suggestions in improving the manuscript. At the fall 1999, H. sanguineus seemed rare in The Netherlands, and no ovigerous females LITERATURE CITED have been reported. Its rarity may be only Breton, G. 1981. Observations sur l’écologie et les pe- temporary, the colonization having just begun. uplements des bassins du port du Havre (France).— The origin of the colonizing individuals is un- Bulletin Trimestriel de la Société Géologique de Nor- mandie et des Amis du Muséum du Havre 68: 45–58. known. The “Oosterschelde” is an important ———, A. Girard, and J.-P. Lagardère [avec la collabora- center of shellfish culture. Several alien tion de: Monniot F., Monniot C., Noël P., Vincent T.] species are believed to have been introduced 1995. Espèces animales benthiques des bassins du port to the Netherlands and neighbouring countries du Havre (Normandie, France) rares, peu connues ou nouvelles pour la région.—Bulletin Trimestriel de la with imported shellfish (Vaas, 1975). In times Société Géologique de Normandie et des Amis du of shortage, importation of living shellfish Muséum du Havre 82: 7–28. from other countries occurs, among them the ———, and T. Vincent. 1999. Invasion du port du Havre U.S.A., but this does not happen regularly. (France, Manche) par Hydroides ezoensis (Polycheta, There is no international harbour in the “Oost- Serpulidae), espèce d’origine japonaise.—Bulletin Trimestriel de la Société Géologique de Normandie et erschelde”, all local harbours are for yacht- des Amis du Muséum du Havre 82: 33–43. ing or small-scale fisheries and shellfish cul- de Haan, W. 1835. Crustacea. In P. F. de Siebold, Fauna ture. Introduction of adults in fouling or lar- Japonica sive descriptio animalium, quae in itinere per vae with ballast water cannot be ruled out, Japoniam, jussu et auspiciis superiorum, qui summum in India Batava Imperium tentent, suscepto, annis however, the distance from the international 1823Ð1830 collegit, notis, observationibus et adum- seaports of Antwerp and Rotterdam being only brationibus illustra. Leiden: IÐXVII, IÐXXXI, 1Ð244, some 100 km. It is well known that grapsid pl. 1Ð55, AÐQ. crabs, among which the Pacific species Hem- Eno, N. C., R. A. Clark, and W. G. Sanderson, eds. 1997. igrapsus penicillatus, occur in fouling com- Non Native Marine Species in British Waters: A Re- view and Directory.—Joint Nature Conservation Com- munities on ship hulls; in Europe one case was mittee, Peterborough, U.K. 152 pp. reported in the harbour of Bremerhaven, Ger- Gollasch, S. 1999. The Asian decapod Hemigrapsus many (Gollasch, 1999). Another possibility is penicillatus (de Haan, 1835) (Grapsidae, Decapoda) in- a settlement of larvae originating from France, troduced in European waters: status quo and future per- spective.—Helgoländer Meeresuntersuchungen 52: where a breeding population lives, or else- 359Ð366. where along the Channel coast. Residual cur- Lohrer, A. M., Y. Fukui, K. Wada, and R. B. Whitlatch. rents are in the right direction. Similar colo- 2000. Structural complexity and vertical zonation of nization of the coast of The Netherlands by intertidal crabs, with focus on habitat requirements of other immigrant species with pelagic larvae the invasive Asian shore crab, Hemigrapsus sanguineus (de Haan).—Journal of Experimental Marine Biology has been suggested by Vaas (1975). and Ecology 244: 203Ð217. With the data available at present, it is im- ———, and R. B. Whitlatch. 1997. Ecological studies on possible to make predictions about the future the recently introduced Japanese shore crab (Hemi- development of Dutch and French popula- grapsus sanguineus), in Eastern Long Island Sound. Pp. 49Ð60 in N. Balcom, ed. Proceedings of the Sec- tions of H. sanguineus. However, the spec- ond Northeast Conference on Nonindigenous Aquatic tacular spread of its congener H. penicillatus Nuisance Species 1997. in France and Spain should make us cautious McDermott, J. J. 1991. A breeding population of the west- BRETON ET AL.: HEMIGRAPSUS SANGUINEUS IN EUROPE 189

ern Pacific crab Hemigrapsus sanguineus (Crustacea: grapsus penicillatus (de Haan, 1835).—De Strandvlo Decapoda: Grapsidae) established on the Atlantic coast 18: 45Ð48. of North America.—Biological Bulletin 181: 195–198. ——— . 1999. Inventaire et distribution des crustacés dé- ——— . 1995. Geographical distribution of a western Pa- capodes de l’Atlantique nord-oriental, de la Méditer- cific brachyuran crab Hemigrapsus sanguineus, along ranée et des eaux continentales adjacentes au nord de the east coast of the United States.—Chesapeake Re- 25°N.—Collection Patrimoines Naturels, Service du search Consortium Publication, No 149: 708. [Abstract.] patrimoine naturel, MNHN Paris: 40: iÐx + 383 pp. ——— . 1998a. The western Pacific brachyuran (Hemi- Vaas, K. F. 1975. Immigrants among the of the grapsus sanguineus: Grapsidae), in its new habitat Delta area of the SW Netherlands.—Hydrobiological along the Atlantic coast of the United States: geo- Bulletin 9: 114Ð119. graphic distribution and ecology.—ICES Journal of Vincent, T. 1999. Undaria pinnatifida (Harvey) Suringar, Marine Science 55: 289Ð298. algue laminaire allochtone: une confirmation de son im- ——— . 1998b. The western Pacific brachyuran Hemi- plantation et de sa progression en plusieurs points du grapsus sanguineus (Grapsidae) in its new habitat along littoral normand.—Bulletin Trimestriel de la Société the Atlantic coast of the United States: reproduction.— Géologique de Normandie et des Amis du Muséum du Journal of Crustacean Biology 18: 308Ð316. Havre 86: 35Ð37. ——— . 1999. The western Pacific brachyuran Hemi- ———, and G. Breton. 1999. Présence du crabe Hemi- grapsus sanguineus (Grapsidae) in its new habitat along grapsus penicillatus (de Haan, 1835) dans les bassins the Atlantic coast of the United States: feeding, che- du port du Havre (Normandie, France).—Bulletin liped morphology and growth.—Proceedings of the Trimestriel de la Société Géologique de Normandie et IVth International Crustacean Congress, Amsterdam, des Amis du Muséum du Havre 86: 19–23. July 20Ð24 1998, volume 1, Koninklijke Brill NV, Lei- Williams, A. B., and J. J. McDermott. 1990. An eastern den: 425Ð444. United States record for the western Indo-Pacific crab, Nijland, R., and J. Beekman. 2000. Hemigrapsus peni- Hemigrapsus sanguineus (Crustacea: Decapoda: Grap- cillatus de Haan 1835 waargendmen in Nederland.— sidae).—Proceedings of the Biological Society of Het Zeepaard 60: 169Ð171. Washington 103: 108, 109. Noël, P. Y., E. Tardy, and C. d’Udekem d’Acoz. 1997. Wolff, W. J. 1999. Exotic invaders of the meso-oligo- Will the crab Hemigrapsus penicillatus invade the haline zone of estuaries in the Netherlands: why are coasts of Europe?—Comptes Rendus de l’Académie there so many?—Helgoländer Meeresuntersuchungen des Sciences de Paris, Sciences de la vie 320: 741Ð745. 52: 393Ð400. Sakai, T. 1965. The Crabs of Sagami Bay.—Maruzen Co. Ltd., Tokyo: 1Ð206 + pls. 1Ð100 + 1Ð92 + 1Ð32, Note: Order for authors is alphabetical. Contribution of 1Ð206 + pls. 1Ð100 + 1Ð92 + 1Ð32 + 1 map. G.B. and T.V. is mainly for Le Havre data, that of M.F. ——— . 1976. Crabs of Japan and the Adjacent Seas. Ko- is mainly for Nederland data, and P.N. for coordination. dansha Ltd., Tokyo (3 vols.): iÐxxix + 1Ð773 + pls. 1Ð251 + 1Ð461. Udekem d’Acoz, C. d’. 1998. Kolonisatie van de Eu- RECEIVED: 10 May 2000. ropees-Atlantische kusten door de borselkrab Hemi- ACCEPTED: 20 June 2001.