First record of the invasive oriental shrimp Palaemon macrodactylus Rathbun , 1902 in France ( Gironde Estuary )

During summer 2006, the first specimens of the oriental shrimp Palaemon macrodactylus Rathbun, 1902 were identified in the Gironde Estuary (France). These specimens, which included ovigerous females, are confirmed present throughout a large part of the estuary, in large numbers compared to the local resident shrimp Palaemon longirostris Milne Edwards, 1837. Native to Asia, P. macrodactylus was first introduced in California (USA) in the 1950s, before being detected recently within several European estuaries, e.g. the Guadalquivir Estuary (Spain) and the Orwell Estuary (England). According to these records, P. macrodactylus appears to be a strong invader, able to colonise a wide geographical range.


Introduction
The oriental shrimp Palaemon macrodactylus Rathbun, 1902 is native to Japan, Korea andChina (Kubo 1942, Rathbun 1902).In the 1950s, this shrimp was first recorded in San Francisco Bay, California (Newman 1963) where it is now a common and well-established species (Central Valley Bay Delta Branch 2006).It has also been found in Australia (Poore 2004).Since the end of the 1990s, P.macrodactylus has been found in several European waters: in Spain (Guadalquivir and Guadalete Estuaries, Salado River, San Pedro River) (Cuesta et al. 2004), in England (Orwell Estuary, Suffolk) (Ashelby et al. 2004) and in the Southern Bight of the North Sea (d'Udekem d'Acoz 2005).During the same period, a first specimen was recorded in southern Atlantic waters in Mar del Plata Harbor (Argentina) (Spivak et al. 2006).According to all these studies, P. macrodactylus appears to be a very successful invader, able to colonise a wide geographical range.
In this short communication, we report for the first time the presence of P. macrodactylus in French waters, specifically in the Gironde Estuary.

Study area, Materials and Methods
The Gironde Estuary (45°20'N, 0°45'W), with an area of 635 km², is the largest estuary in Western Europe (Figure 1).About 20 species of Decapoda have been inventoried in this estuary (Mauvais and Guillaud 1994) and the genus Palaemon is well represented with four species.Among these, the white shrimp Palaemon longirostris Milne Edwards, 1837, a resident species, represents large population throughout the estuary (Aurousseau 1984, Girardin et al. 2005, Sorbe 1983) and supports a traditional fishing industry.
Since 1979, a large part of the estuary (Figure 1) within a 20 km area around the nuclear power plant had been sampled monthly for fauna survey (mainly fishes and crustaceans) (Girardin et al. 2005).The water surface was sampled using two pushnets located on either side of the boat (section 4m x 1m, stretched mesh of 2.8mm at the end).The bottom was sampled using an Agassiz trawl consisting of a metal frame 2m x 1.2m kept at 0.2m from the bottom by skates with similar mesh size.Samplings were carried out only in daytime between the mid-flow and the slack period of the high tide.Each tow lasted about seven minutes.
The first specimens of P. macrodactylus were identified during the summer 2006.They were initially recognised by their colour pattern, especially their orange/pink coloration, which is not observed in P. longirostris in this estuary, and by the presence of a whitish longitudinal dorsal stripe running all along the back, which is absent in European native Palaemonidae (d'Udekem d'Acoz et al 2005).A microscopic examination enabled us to confirm the finding.Indeed, P.macrodactylus can be identified with their rostrum which has 9 to 15 dorsal teeth and ventral margin with a double row of setae, with the shorter ramus of antennular flagellum fused for a quarter of its length to longer ramus and with the absence of protuberance above spine of the posterolateral margin of the sixth abdominal segment (Ashelby et al. 2004, Gonzalez-Ortegon andCuesta 2006).
Additional samples collected during summer 1992, 1996, 1997, 1998, 1999 and 2002 in the same conditions have been examined in order to look for P. macrodactylus.

Results and Discussion
Specimens of P. macrodactylus were first recorded in the Gironde Estuary during summer 2006 (Annex).Their presence was confirmed in all sampling stations, surface and bottom water, within a salinity range from 8 to 20 psu and representing 8 to 71% of the collected shrimps (P.macrodactylus and P. longirostris).Similarly to P. longirostris, P. macrodactylus was more abundant in the bottom samples.
Therefore, according to these first observations, it appears that P. macrodactylus already make up a major proportion of the estuarine shrimp population during summer 2006.Several ovigerous females were identified in the August samples (Figures 2 and 3), indicating that the population of P. macrodactylus might be established in the area, with reproducing specimens.
Due to their similar morphologies, it is not easy to distinguish between the exotic species (P.macrodactylus) and the local species P. longirostris.The coloration criterion, which helps for initial identification, is useless within the Gironde Estuary due to the high turbidity (1g/l to 10g/l, exceptionally 400g/l) (Sottolichio and Castaing 1999) which tends to enhance a loss of coloration in all organisms (Figures 2 and  3).The specimens observed had almost no coloration compared with specimens found in the Netherlands for example.This might explain the fact that P. macrodactylus has not previously been identified.
The examination of several samples from 1992, 1996 and 1997 revealed no P. macrodactylus specimens.One specimen was found in a sample from 1998, followed by several in 1999 and 2000 samples, suggesting the presence of P. macrodactylus in the Gironde Estuary since at least 1998.Since it cannot be excluded that the  species was already present, further anterior samples will have to be examined.
We found several specimens in the Adour Estuary in September 2006 (Annex).No P. macrodactylus specimens were found in samples from the Loire (2004 and 2006 samples) and Seine estuaries (2004 samples).More samples must be examined to determine whether this species has already invaded these estuaries.
The most probable cause of introduction may be the accidental transport of pelagic larvae in the ballast water of ships, as shown in previous cases (e.g.Carlton 1985).Inter-regional traffic is indeed well developed in the Gironde Estuary (Allain et al. 2006).
P. macrodactylus is very similar to the resident species P. longirostris.Both are strong osmoregulators (Born 1968, Campbell andJones 1989) and are typical estuarine species with similar diets, consisting mainly of mysids and copepods (Siegfried 1982, Sitts and Knight 1979, Sorbe 1983).We can assume that food competition will take place between the two species and even with another common species, Crangon crangon Linnaeus, 1758.There is also evidence of cannibalism when individuals are kept in crowded laboratory conditions (Newman 1963), so the species could prey on other carideans in the estuaries.Moreover, each age group of P. macrodactylus produces at least two cohorts compared with only one or two for P. longirostris (Aurousseau 1984, Omori andChida 1988).
We can assume that interactions between the two species could be considerable and could perhaps lead to a decrease in the native shrimp population abundance.In California, Ricketts et al. (1968) observed that P. macrodactylus was responsible for the disappearance of the native Crangon spp.Furthermore, Gil-Turnes et al (1989) found fungi associated with P. macrodactylus which, if confirmed in the Gironde, raises the possibility of new diseases being introduced that may affect the native shrimps.
We can assume that interactions between the two species could be considerable and could perhaps lead to a decrease in the native shrimp population abundance.In California, Ricketts et al. (1968) observed that P. macrodactylus was responsible for the disappearance of the native Crangon spp.Furthermore, Gil-Turnes et al. (1989) found fungi associated with P. macrodactylus which, if confirmed in the Gironde, raises the possibility of new diseases being introduced that may affect the native shrimps.
In the Gironde Estuary, shrimps are an important food resource for many fish species (Pasquaud 2006) and form the basis of fish richness (Lobry 2004, Lobry et al. 2006).Thus, by representing a new or an additional resource for fish species, the spread of the P. macrodactylus population could also result in disturbance estuarine functioning.
In order to study the effect of this invasive species, we are currently sampling the estuary once a month (poly-to oligohaline zone).We focus particularly on the interaction between P. macrodactylus and the resident species P. longirostris, which is traditionally fished in the Gironde Estuary.Samples collected between 1992 and 1998 will be examined to specify its apparition period and to detail the invasion in the Gironde Estuary.We also plan an extensive survey of the entire tidal estuary to determine its spatial distribution.

Figure 1 .
Figure 1.The Gironde Estuary and the sampling area (between dotted lines).