A bomb set to drop: parthenogenetic Marmorkrebs for sale in Ireland, a European location without non-indigenous crayfish

Ireland is one of the few locations in Europe where non-indigenous North American crayfish species have not been introduced, and is a refuge for endangered white-clawed crayfish, Austropotamobius pallipes (Lereboullet, 1858). The parthenogenetic crayfish species Marmorkrebs, Procambarus fallax f. virginalis (Hagen, 1870), is sold in the pet trade in Ireland within the recorded range of A. pallipes. Marmorkrebs risk being introduced into Irish waters, where they could threaten A. pallipes populations, particularly as a vector for crayfish plague.


Introduction
Non-indigenous crayfish threaten native European crayfish (Holdich et al. 2009;Kouba et al. 2014) through competition and acting as vectors for crayfish plague Aphanomyces astaci Schikora, 1906(Unestam 1965Unestam 1966;Unestam 1969), a disease for which European crayfish have no resistance (Unestam 1972;Alderman et al. 1984;Reynolds 1988;Matthews and Reynolds 1992;Diéguez-Uribeondo 2009;Grandjean et al. 2014). Ireland is unusual in Europe because it has no non-indigenous crayfish in its waters (Reynolds 1997;Kouba et al. 2014). Consequently, the whiteclawed crayfish, Austropotamobius pallipes (Lereboullet, 1858), is more abundant in Ireland than mainland Europe (Lucey and McGarrigle 1987;Holdich and Rogers 1997;Reynolds et al. 2002;Demers et al. 2005;Füreder et al. 2010). Ireland could provide A. pallipes stock to repopulate other regions in Europe if North American crayfish species can be controlled. Import of crayfish into Ireland is banned (Holdich and Rogers 1997;Peay 2009), and the Irish National Parks and Wildlife Service has produced a pamphlet to promote public awareness of crayfish conservation, and the threat posed by introduced crayfish (Reynolds and O'Keeffe 2010).
Marmorkrebs, Procambarus fallax f. virginalis (Hagen, 1870), create grave concerns as a nonindigenous crayfish. First, a single individual can establish a population because they are parthenogenetic (Scholtz et al. 2003). Second, they have high propagule pressure because they are widely distributed in the pet trade (Faulkes 2010;Chucholl 2013;Faulkes 2013), resulting in releases in multiple European countries (reviewed in Chucholl et al. 2012;Kouba et al. 2014). Monitoring the online pet trade can provide insights into the risk of release of non-indigenous species (Duggan et al. 2006;Kikillus et al. 2012;Martin et al. 2012;Chucholl 2013;Papavlasopoulou et al. 2014). Here, I report on recent advertisements confirming that Marmorkrebs are being kept and sold in Ireland within the range of A. pallipes.

Methods
Custom searches in Google Alerts (http://www. google.com/alerts) scan the Internet for the terms "Marmorkrebs" and "marbled crayfish" on English language websites. Results of these searches are

Results
Advertisements for "marble crayfish" were placed on sales websites on 11 April 2014 (http://www. adverts.ie, which advertises itself as, "Ireland's trusted marketplace"; Figure 1) and 15 July 2014 (http://www.donedeal.ie, which describes itself as, "Ireland's biggest classifieds site"). The sellers were located in Mullagh, Cavan, and Mallow, Co. Cork, Ireland, both of which are within the recorded distribution of A. pallipes ( Figure 2). The April seller wrote, "these crayfish are all female they do not need males to breed", which, combined with the commonly used name for P. fallax f. virginalis, "marble crayfish", suggests the buyer believed these were Marmorkrebs. A large individual was priced at 20€ (about US$27) and smaller ones at 5€ (about US$6.9); the latter is the typical price for Marmorkrebs in Europe (Chucholl 2013) and close to the North American mode price of US$5 (Faulkes 2013). Comments on the ad indicated that there was at least one potential buyer. The July ad indicated the seller had about a dozen crayfish, but gave no price details. I informed the National Parks and Wildlife Service (Ireland) of both advertisements by email. A representative of that agency replied on 14 April 2014 that a local conservation ranger had been informed of the ad. The April ad was withdrawn from the website on 17 April 2014. The July ad was removed 17 July 2014.
While this paper was initially being reviewed, Reynolds (2014) reported Marmorkrebs were available for sale online in Cork, Ireland. This is not within the known range of A. pallipes, however (Figure 2).

Discussion
The sale of Marmorkrebs in the Irish pet trade (this report; Reynolds 2014) is of great concern for the conservation of white-clawed crayfish, A. pallipes. Some quantitative species distribution models suggest that Ireland contains suitable habitat for Marmorkrebs ( Figure 3D in Feria and Faulkes 2011). Marmorkrebs can carry crayfish plague (Steyskall et al. 2013), which wiped out one A. pallipes population in Ireland, even in the absence of any North American crayfish species (Reynolds 1988;Matthews and Reynolds 1992). Aphanomyces astaci can be spread from dead crayfish or fish feces (Oidtmann et al. 2002), so even if Marmorkrebs are contained in aquaria while alive, their presence increases the risk of crayfish plague if their cadavers come into contact with natural waters. Further, Marmorkrebs could affect A. pallipes populations by direct competition. A. pallipes can be outcompeted by other decapod crustaceans (Barbaresi and Gherardi 1997), and Marmorkrebs can compete with Procambarus clarkii (Girard, 1852) in fights (Jimenez and Faulkes 2011). This risk may be mitigated if Marmorkrebs and A. pallipes use different habitats: Marmorkrebs populations commonly occur in lentic ponds and lakes (Chucholl et al. 2012), while A. pallipes populations occur in lotic riparian streams and rivers (Smith et al. 1996;Naura and Robinson 1998;Broquet et al. 2002;Demers et al. 2003).
Even in the unlikely event that the crayfish for sale were not Marmorkrebs, the sale of any crayfish species in the Irish pet trade is a concern. The online sale of illegal crayfish as ostensibly benign pets suggests that the Irish pet trade be more closely scrutinized for compliance with laws prohibiting import of crayfish into Ireland, and that the laws be more highly visible to the general public. While there is considerable discussion among the crayfish research community concerning expanding and strengthening laws on the import and sale of crayfish (Peay 2009), the sale of Marmorkrebs in Ireland, where import of crayfish is already illegal, highlights the difficulty of enforcing even existing laws concerning crayfish. Vendors (DiStefano et al. 2009) and pet owners (Faulkes 2013) are often non-compliant with local laws, often through simple ignorance. Enforcement of existing laws is also typically low in many jurisdictions (Peay 2009), and aimed at end users rather than vendors (Stebbing et al. 2014), which may reduce the effectiveness of such laws. Education is often mentioned as an important component in controlling introductions of non-indigenous crayfish (Peay 2009;Stebbing et al. 2014). Systematic studies on the effectiveness of educational campaigns aimed at the general public (such as Reynolds and O'Keeffe 2010) or changes in enforcement would be valuable. Diéguez-Uribeondo J (2009)