First record of Grandiderella japonica Stephensen, 1938 (Amphipoda: Aoridae) from mainland Europe

Abstract

The non-native amphipod Grandidierella japonica Stephensen, 1938 is reported for the first time on the Atlantic coast of mainland Europe, specifically from Marennes-Oléron Bay, France. Likely vectors for this introduction include commercial shellfish transplants and ballast waters. A native of Japan, this species had previously only been reported twice outside the Pacific region; in both cases from coastal waters
of England. Adults of both sexes, females carrying eggs, and juveniles were collected in Marennes-Oléron Bay, which suggests the species has become established.

Full text

BioInvasions Records (2013) Volume 2, Issue 1: 51–55
doi: http://dx.doi.org/10.3391/bir.2013.2.1.09
© 2013 The Author(s). Journal compilation © 2013 REABIC
Open Access
51
Short Communication
First record of Grandidierella japonica Stephensen, 1938 (Amphipoda: Aoridae)
from mainland Europe
Jérôme Jourde
1, 2
*, Pierre-Guy Sauriau
2
, Stéphane Guenneteau
3
and Emmanuel Caillot
4
1 OBIONE (Observatoire de la Biodiversité Faune Flore des Pertuis Charentais), CNRS, Université de La Rochelle, 2 rue Olympe
de Gouges, 17000 La Rochelle, France
2 LIENSs (Littoral Environnement et Sociétés), CNRS, Université de La Rochelle, 2 rue Olympe de Gouges, 17000 La Rochelle,
France
3 Réserve Naturelle Nationale de Moëze-Oléron, Grange à NOUREAU, 17780 Saint Froult, France
4 Réserves Naturelles de France (RNF), 6bis rue de la Gouge CS 60100, 21803, Quétigny, France
E-mail: jjourde@univ-lr.fr (JJ), pierre-guy.sauriau@univ-lr.fr (PGS), stephane.guenneteau@lpo.fr (SG),
emmanuel.caillot@espaces-naturels.fr (EC)
*Corresponding author
Received: 29 October 2012 / Accepted: 18 December 2012 / Published online: 10 January 2013
Handling editor: Philippe Goulletquer
Abstract
The non-native amphipod Grandidierella japonica Stephensen, 1938 is reported for the first time on the Atlantic coast of mainland Europe,
specifically from Marennes-Oléron Bay, France. Likely vectors for this introduction include commercial shellfish transplants and ballast
waters. A native of Japan, this species had previously only been reported twice outside the Pacific region; in both cases from coastal waters
of England. Adults of both sexes, females carrying eggs, and juveniles were collected in Marennes-Oléron Bay, which suggests the species
has become established.
Key words: alien species; Japan; shellfish farming activities; ballast water; Marennes-Oléron Bay; France
Introduction
Grandidierella japonica Stephensen, 1938 is an
aorid amphipod species (Crustacea: Amphipoda:
Aoridae) native to the Japanese archipelago
(Chapman and Dorman 1975). Until recently, the
species occurred exclusively in the Pacific
region. Outside its native area, it was first
reported in San Francisco Bay in 1966 (Chapman
and Dorman 1975) but is now found in intertidal
and subtidal sediments of bays and estuaries of
the western coast of North America from Mexico
to British Columbia, Canada (Greenstein and
Tiefenthaler 1997; Okolodkov et al. 2007). It has
also been reported from Hawaii (Coles et al.
1999) and New South Wales, Australia (Myers
1981). Outside the Pacific region, the only
known reports of this species are from
Southampton (1997) and the Orwell Estuary
(2007), south eastern England (Smith et al. 1999;
Ashelby 2006; Noël 2011). The species is not
listed in recent checklists available at the
national scale for France (Dauvin and Bellan-
Santini 2002), at the regional scale of the
Southern Bay of Biscay (Bachelet et al. 2003), or
anywhere on the coast of mainland Europe
(Goulletquer et al. 2002; Wolff 2005; DAISIE
2009; Preisler et al. 2009; Haydar and Wolff
2011). To the best of our knowledge, this study
represents the first report of Grandidierella
japonica, a reproducing population, in coastal
waters of mainland Europe.
Methods
As part of a national benthic survey to monitor
intertidal macrofauna species available in early
autumn to wintering shorebirds (RNF “Littoral
Shorebirds and Benthic Macrofauna” observa-

J. Jourde et al.
52
Figure 1. Location of the 13 stations (crosses) sampled in the Pertuis Charentais Sea within the framework of the RNF “Littoral
Shorebirds and Benthic Macrofauna” observatory in 2009, 2010 and 2011. Blue crosses show the stations where Grandidierella
japonica was found (Bellevue and Ostrea). Gray shading indicates the areas of intense bivalve aquaculture.
tory), 13 stations have been sampled within the
Pertuis Charentais Sea every autumn since 2009
(Figure 1). Specimens of Grandidierella japoni-
ca have only been collected from two stations:
Bellevue (45°56'20.40"N, 01°13'04.80"W) and
Ostrea (45°54'53.60"N, 01°12'56.60"W).
Located along the Eastern coast of Oléron Island
(Figure 1), these stations lie on sheltered muddy
and sandy shores. They are located in the
vicinity of large shellfish farming areas where
Pacific oysters (Crassostrea gigas Thunberg,
1793) are reared in bags on metal trestles
(Goulletquer and Héral 1997; Gosling 2004), and
blue mussels (Mytilus edulis Linnaeus, 1758) are
reared on bouchots (Goulletquer and Héral 1997;
Prou and Goulletquer 2002; Gosling 2004).
During analysis of samples collected at
Bellevue and Ostrea on 8 November 2010, we
found two possible specimens of amphipods of
the genus Grandidierella Coutière, 1904. Our
preliminary identification was based on keys in
Ruffo (1982) and Barnard and Karaman (1991).
This aorid amphipod genus is, however, close to
both the genera Microdeutopus Costa, 1853 and
Unciolella Chevreux, 1911. It differs from the
former mainly by the uniramous uropods 3
(Figure 2). It differs from the latter by: 1) the
length of the uropod 3 rami, which is more than
twice the length of the peduncle (Figure 2); 2)
the third article of antenna 1, which is much less
than half the length of the first article (Figure
3A); and 3) the carpochelate gnathopods 1 of the
male (Figure 3A, 4A). However, our identifica-
tion remained tentative due to the poor condition
of the female collected at Bellevue and the sub-
adult male collected at Ostrea.

First record of Grandidierella japonica from mainland Europe
53
Figure 2. Grandidierella japonica, urosome showing uniramous
uropods 3 (arrows). Alcohol preserved specimen collected at the
Bellevue station on 20 August 2012. Photo by Jérôme Jourde.
Figure 3. Grandidierella japonica, male (A) and brooding female
(B). Arrows show articles 1 and 3 of the male antenna 1. Alcohol
preserved specimens collected at the Bellevue station on 20
August 2012. Note: the eggs were greenish in colour before
alcohol preservation. Photo by Jérôme Jourde.
Figure 4. Grandidierella japonica, male gnathopod 1 left, inner
surface (A), detail of anterior margin of the gnathopod 1 carpus,
arrows show the transverse ridges (B), three teeth (arrows) on
carpus distal part (C). Alcohol preserved specimen collected at
the Bellevue station on 20 August 2012. Photo by Jérôme Jourde.
Four additional specimens (females) were found
in samples collected at the Bellevue station on
30 November 2011. Although the specimens
were in good condition, identifying female aorid
amphipods to species is difficult; mature males
are generally required. To confirm the species
identity, additional qualitative benthic samples
were made at the Bellevue station on 20 August
2012.
Results
From samples collected at the Bellevue station
on 20 August 2012, we obtained 70 specimens in
good condition: 21 mature males (Figure 3A); 31
females including 8 brooding females (Figure
3B); and 18 undifferentiated juveniles.
Diagnosis: The mature males had transverse
ridges on the carpus anterior margin of the
gnathopods 1 (figure 4B). In the genus Grandi-
dierella, only five species have such ridges:
namely G. japonica, G. perlata Schellenberg,
1938, G. taihuensis Morino and Dai, 1990, G.
vietnamica Dang, 1968 (Ariyama 1996) and G.
chaohuensis Hou and Li, 2002 (Hou and Li
2002). However, the specimens can be identified
as G. japonica, because only G. japonica has
three teeth on the carpus of the male gnathopod 1
(Figure 4C). In addition, morphological
characters of the specimens agree well with the
descriptions and figures of G. japonica provided
by Stephensen (1938), Chapman and Dorman
(1975), Hirayama (1984) and Ariyama (1996).

J. Jourde et al.
54
Discussion
In the case of Grandidierella japonica
introduction into Californian waters, the most
likely hypothesis is commercial transplant of
Crassostrea gigas spat from Japan (Chapman
and Dorman 1975). The same vector may apply
here because the Marennes-Oléron Bay is the
most important area for shellfish farming along
the French coast (Goulletquer and Héral 1997).
Oyster culture in this sheltered bay has been
characterized by a series of flourishing and
declining periods of activity, particularly over
the last century when a complete collapse of the
Portuguese oyster Crassostrea angulata industry
occurred [C. angulata (Lamarck, 1819) is now
considered as a junior synonym of C. gigas
(WoRMS 2012)]. Large quantities of C. gigas
were imported from British Columbia and Japan
during the late 1960s and 1970s to counter both
the disappearance of C. angulata populations and
the decline in native flat oyster stocks (Ostrea
edulis Linnaeus, 1758) due to disease and
parasite outbreaks (Grizel and Héral 1991;
Goulletquer and Héral 1997). It is now well
established that the movement of C. gigas
between countries has led to establishment of
numerous alien species into Northern Europe
(Goulletquer et al. 2002; Wolff and Reise 2002).
Indeed, the oyster industry appears to be the
main vector of introduction for more than 25%
of the 104 alien species recorded along the
French Atlantic coast (Goulletquer et al. (2002).
However, other vectors of introduction such as
ballast waters and ship fouling cannot be
excluded because G. japonica has become
established in vicinity of major ports involved in
international cargo transport (Coles et al. 1999;
Smith et al. 1999; Ashelby 2006). In the context
of this study, there are two major seaports
handling international cargo nearby: Port
Atlantique La Rochelle, which is located North
of Marennes-Oléron Bay; and the Port of
Rochefort located 25 km upstream of the
Charente estuary mouth (Figure 1). A 1993–1995
study analysing ships’ traffic and ballast water
estimated total annual ballast for both ports to be
1.2 million metric tons (Masson 2003).
The timing of introduction of G. japonica into
Marennes-Oléron Bay is difficult to establish.
For three decades, there have been no official
commercial transplants of C. gigas because
oyster imports from the Pacific ended by 1982
due to parasite infestation (Grizel and Héral
1991; Wolff and Reise 2002). The species may
have been present but not identified because the
genus Grandidierella can be easily confused
with other aorid genera, especially Micro-
deutopus. Moreover, neither the species nor the
genus was described in the taxonomic works
most commonly used for amphipod identification
in French Atlantic waters (Chevreux and Fage
1925; Lincoln 1979). As already noted by
Ashelby (2006), this may have led to the species
being overlooked during the last decades. Even
so, introduction of G. japonica into Marennes-
Oléron Bay prior to the 1980s would seem
unlikely because there were large scale benthic
surveys of both intertidal and subtidal areas
within Marennes-Oléron Bay during the 1980s
and 1990s with no records of the genus
(Montaudouin and Sauriau 2000). An alternative
hypothesis is that this is a recent introduction
similar to that in English waters (Smith et al.
1999; Ashelby 2006).
The current extent of the geographic range of
G. japonica along the French Atlantic coast is
unknown. For now, this appears to be an isolated
occurrence because there is no evidence of its
presence anywhere else in the Pertuis Charentais
area or anywhere on coast of mainland Europe.
As the presence of brooding females suggests a
self-sustaining population exists in Marennes-
Oléron Bay and, given the difficulty in
identifying the species, it may well be present
elsewhere in European waters. Now that a
reproducing population of the species has been
confirmed, special attention during all benthic
monitoring programs would seem to be warran-
ted to better define the species’ geographic range
in European waters. This would also allow an
evaluation of species’ invasiveness potential in
European waters and permit measurement of
significant effects on native fauna.
Acknowledgements
The authors are grateful to the League for Protection of Birds staff
(LPO), especially S. Travichon, for funding this research through
FEDER. The LPO staff performed the RNF sampling program. L.
Jomat’s help was particularly appreciated during the 2012
sampling session. Thanks are due to C. Curti for preparing the
map and T. Worsfold for supplying some papers (Smith et al.
1999 and Ashelby 2006). JJ was financially supported by the
Région Poitou-Charentes through CPER funding, the Université
de La Rochelle and CNRS. This study complied with the Moëze-
Oléron nature reserve regulations and was supervised by Ph.
Delapporte. Authors gratefully thank the three anonymous
reviewers and Dr J.M. Hanson (Ed.) for their valuable comments
that helped improve this short communication.

First record of Grandidierella japonica from mainland Europe
55
References
Ariyama H (1996) Four species of the genus Grandidierella
(Crustacea: Amphipoda: Aoridae) from Osaka Bay and the
northern part of the Kii Channel, central Japan. Publications
of the Seto Marine Biological Laboratory 37: 167–191
Ashelby C (2006) Record of the introduced amphipod Grandi-
dierella japonica Stephensen 1938 (Crustacea: Amphipoda:
Gammaridea: Aoridae) from the Orwell estuary, Suffolk.
Transactions of the Suffolk Natural History 42: 48–54
Bachelet G, Dauvin JC, Sorbe JC (2003) An updated checklist of
marine and brackish water Amphipoda (Crustacea:
Peracarida) of the southern Bay of Biscay (NE Atlantic).
Cahiers de Biologie Marine 44: 121–151
Barnard JL, Karaman GS (1991) The families and genera of
marine gammaridean Amphipoda (except marine
gammaroids). Records of the Australian Museum,
Supplement 13 (Part 1 and 2): 1–866
Chapman JW, Dorman JA (1975) Diagnosis, systematics, and
notes on Grandidierella japonica (Amphipoda: Gammaridea)
and its introduction to the Pacific coast of the United States.
Bulletin of the Southern California Academy of Sciences 74:
104–108
Chevreux E, Fage L (1925) Amphipodes. Volume 9. Office
Central de Faunistique, Librairie de la Faculté des Sciences,
Paris, 488 pp
Coles SL, DeFelice RC, Eldredge LG, Carlton JT (1999)
Historical and recent introductions of non-indigenous marine
species into Pearl Harbor, Oahu, Hawaiian Islands. Marine
Biology 135: 147–158,
http://dx.doi.org/10.1007/s002270050612
DAISIE (Delivering Alien Invasive Species Inventories for
Europe) (2009 onwards) Handbook of alien species in
Europe, Springer, Dordrecht.
http://www.europe-aliens.org
(Accessed 1st October 2012)
Dauvin JC, Bellan-Santini D (2002) Les Crustacés Amphipodes
des côtes françaises métropolitaines: bilan des connais-
sances. Crustaceana 75: 299–340,
http://dx.doi.org/10.1163/156
854002760095408
Gosling E (2004) Bivalve molluscs. Biology, ecology and culture.
Blackwell Publishing Ltd., Oxford, 443 pp
Goulletquer P, Héral M (1997) Marine molluscan production
trends in France: from fisheries to aquaculture. In:
MacKenzie CL, Burrell VG, Rosenfield AWH (eds), The
history, present condition, and future of the Molluscan
fisheries of North America and Europe. NOAA Technical
Report NMFS 129, Department of Commerce, Seattle,
Washington, pp 137–164
Goulletquer P, Bachelet G, Sauriau PG, Noël P (2002) Open
Atlantic coast of Europe - A century of introduced species
into French waters. In: Leppäkoski E, Gollash S, Olenin S
(eds) Invasive aquatic species of Europe. Distribution,
impacts and management. Kluwer Academic Publishers,
Dordrecht, The Netherlands, pp 276–290
Greenstein DJ, Tiefenthaler LL (1997) Reproduction and
population dynamics of a population of Grandidierella
japonica (Stephensen) (Crustacea: Amphipoda) in upper
Newport Bay. California. Bulletin of the Southern California
Academy of Sciences 96: 34–42
Grizel H, Héral M (1991) Introduction into France of the
Japanese oyster (Crassostrea gigas). Journal du Conseil
International pour l'Exploration de la Mer 47: 399–403
Haydar D, Wolff WJ (2011) Predicting invasion patterns in
coastal ecosystems: relationship between vector strength and
vector tempo. Marine Ecology Progress Series 431: 1–10,
http://dx.doi.org/10.3354/meps09170
Hirayama A (1984) Taxonomic studies on the shallow water
gammaridean Amphipoda of west Kyushu, Japan. II.
Corophiidae. Publications of the Seto Marine Biological
Laboratory 29: 1–92
Hou ZE, Li SQ (2002) A new species of the genus Grandidierella
from Lake Chaohu, China. Acta Zootaxonomica Sinica 27:
225–234
Lincoln RJ (1979) British marine amphipoda: Gammaridea.
British Museum (Natural History), London, 658 pp
Masson D (2003) Les eaux de ballast des navires, sources
d'introduction d'organismes nuisibles. La Revue Maritime
464: 224–229
Montaudouin X (de), Sauriau P-G (2000) Contribution to a
synopsis of marine richness in the Pertuis Charentais Sea
with new insights in soft-bottom macrofauna of the
Marennes-Oleron Bay. Cahiers de Biologie Marine 41: 181–
222
Myers AA (1981) Taxonomic studies on the genus Grandidierella
Coutière (Crustacea, Amphipoda). III. Fijian, Australian and
Saudi Arabian species. Bulletin du Museum National
d’Histoire Naturelle, Paris, 4e série, 3, section A:1, pp 213–
226
Noël P (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, Berlin, pp 345–
375,
http://dx.doi.org/10.1007/978-94-007-0591-3_12
Okolodkov YB, Bastida-Zavala R, Ibáñez AL, Chapman JW,
Suárez-Morales E, Pedroche F, Gutiérrez-Mendieta FJ (2007)
Especies acuáticas no indígenas en México. Ciencia y Mar
11: 29–67
Preisler RK, Wasson K, Wolff WJ, Tyrrell MC (2009) Invasions
of Estuaries vs the Adjacent Open Coast: A Global
Perspective. In: Rilov G, Crooks JA (eds), Biological
Invasions in Marine Ecosystems. Springer, Berlin, pp 587–
617,
http://dx.doi.org/10.1007/978-3-540-79236-9_33
Prou J, Goulletquer P (2002) The French mussel industry: present
status and perspectives. Bulletin of the Aquaculture
Association of Canada 102-103: 17–23
Ruffo S (Ed) (1982) The Amphipoda of the Mediterranean (Part
1) Gammaridea (Acanthonotozomatidae to Gammaridae).
Musée Océanographique de Monaco, Monaco, 364 pp
Smith P, Perrett J, Garwood P, Moore G (1999) Two additions to
the UK marine fauna: Desdemona ornata Banse, 1957
(Polychaeta, Sabellidae) and Grandidierella japonica
Stephensen, 1938 (Amphipoda, Gammaridea). Newsletter of
the Porcupine Marine Natural History Society 2: 8–11
Stephensen K (1938) Grandidierella japonica n. sp., a new
amphipod with stridulating (?) organs from brackish
water in Japan. Annotationes Zoologicae Japonenses 17:
179–184
Wolff WJ (2005) Non-indigenous marine and estuarine species in
The Netherlands. Zoologische Mededelingen 79(1): 3–116
Wolff WJ, Reise K (2002) Oyster imports as a vector for the
introduction of alien species into northern and western
European coastal waters. In: Leppäkoski E, Gollasch S,
Olenin S (eds), Invasive aquatic species of Europe
Distribution, impacts and management. Kluwer Academic
Publishers, Dordrecht, The Netherlands, pp 193–205
WoRMS (2012) Crassostrea angulata (Lamarck, 1819). World
Register of Marine Species at
http://www.marinespecies.org/
aphia.php?p=taxdetails&id=146900
(Accessed on 1st October
2012