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All issues No 418 (2017) Knowl. Manag. Aquat. Ecosyst., 418 (2017) 40 Full HTML
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Knowl. Manag. Aquat. Ecosyst.
Number 418, 2017
Topical issue on Crayfish
Article Number 40
Number of page(s) 5
DOI https://doi.org/10.1051/kmae/2017029
Published online 05 September 2017

© B. Lipták et al., Published by EDP Sciences 2017

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (http://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

1 Introduction

Biological invasions have devastating consequences on the native biota, which is particularly apparent in freshwater ecosystems (Richman et al., 2015). Introduced non-indigenous crayfish species affect the invaded biotopes, with negative community-level impacts (Moorhouse et al., 2014; Roukonen et al., 2016). Among alien crayfish, the marbled crayfish Procambarus fallax f. virginalis is an emerging threat, particularly in Europe. It is the only known crayfish reproducing via obligate apomictic parthenogenesis, producing genetically uniform offspring (Martin et al., 2010). This species is characterised by early maturation (Seitz et al., 2005), reproduces throughout the whole year under favourable conditions (Vogt et al., 2004; Seitz et al., 2005), and its high competitiveness for food and shelters has been documented (Jimenez and Faulkes, 2011). Its survival under low temperatures was proven both in the laboratory and the field (Veselý et al., 2015; Lipták et al., 2016). The marbled crayfish was first discovered in the German aquarium trade in the mid-1990s, from where it further dispersed (Scholtz et al., 2003). Its availability at the pet markets is usually high (e.g. Kotovska et al., 2016; Vodovsky et al., 2017). At the beginning of the new millennium, reports on occurrence of single specimens from the wild appeared, followed by confirmation of established populations in Germany and Slovakia in 2010; since then, the number of invaded European countries has steadily increased (see Patoka et al., 2016 and references cited therein), and the ability of marbled crayfish to carry the crayfish plague pathogen has been confirmed both in aquarium trade (Mrugała et al., 2015) and in the field (Keller et al., 2014). Due to all these characteristics, the marbled crayfish became listed among the invasive alien species of European Union concern according to recent legislation (EU Regulation No. 1143/2014 and Commission Implementing Regulation No. 2016/1141). Here we report an established marbled crayfish population in Bratislava, Slovakia, which has presumably initiated the colonisation of the Danube.

2 Material and methods

The marbled crayfish was discovered by a chance during research focused on the ecology of another alien species, the yellow-bellied slider Trachemys scripta scripta and the red-eared slider T. s. elegans, both native to North America. Two marbled crayfish were caught in turtle traps on August 25, 2016, in front of the pumping station in the Chorvátske rameno in Bratislava. Chorvátske rameno is a dead-end artificial canal within the town district Petržalka, which ends at a pumping station (48.0996 N, 17.1306 E) next to a side arm of the Danube (Jarovecké rameno) directly connected to the river (Fig. 1A, B). The canal is approx. 5 km long and 20 m wide with a depth of 2–3 m in its centre. Submerged macrophytes are present in some sections of the canal, and its banks are usually lined with emergent macrophytes. The canal bed is formed by fine gravel mixed with organic detritus.

Two installed pumps at the station in Chorvátske rameno have a capacity of 260 l·s−1 and are activated mainly during elevated flow rates (floods) in the Danube and during extensive rainfalls in the area in order to regulate ground waters in this highly populated town district. They are also occasionally activated when being checked for functionality. The pumping activity will transfer any biota in the immediate vicinity of the station into the side arm of the Danube, with no further barriers to dispersal to the river itself.

After accidental finding of marbled crayfish, two additional field samplings followed, the first on September 11, and the second on October 24, 2016. Both samplings focused on the areas just above and below the pumping station, i.e., places where the presumed chance of successful capture of crayfish was highest. The first survey of the Chorvátske rameno canal was performed by a single researcher, who explored 2 m long stony section of the shore for 30 min. The second survey was performed by three researchers on a 10 m stretch. The sampling lasted for 40 min. Thanks to the high abundance of the marbled crayfish and easy access to the site, no crayfish trapping was needed. The Jarovecké rameno side arm is stabilised by heavy stones forming several layers. Thus manual search (ineffective in such conditions) was combined with trapping, using six baited traps exposed overnight during the first survey and 25 traps in the second survey.

Carapace length of sampled crayfish was measured to the nearest 0.1 mm. The eggs and juveniles in the first two developmental stages were counted if present. Juveniles in the third developmental stage become gradually independent and their quantification would be inaccurate. All captured crayfish individuals were preserved in 96% ethanol. Screening of the presence of the crayfish plague pathogen Aphanomyces astaci, using the quantitative PCR-based methods of Vrålstad et al. (2009), was conducted on all adult crayfish captured at both investigated sites (Chorvátske rameno and Jarovecké rameno). Details of the laboratory protocols are described in Mrugała et al. (2015) and Lipták et al. (2016).

thumbnail Fig. 1

Map showing the marbled crayfish Procambarus fallax f. virginalis occurrence in Bratislava, Slovakia – general view (A) and detailed location (B). Asterisk refers to the pumping station, while 1 and 2 to the locations in the Chorvátske rameno canal and the Jarovecke rameno side arm where marbled crayfish and spiny-cheek crayfish Orconectes limosus were found, respectively. Fecundity of marbled crayfish females (C) expressed as the number of eggs (circles), stage 1 (triangles) and stage 2 juveniles (squares), respectively, and the relationship between female carapace size and the number of offspring (exponential regression, with all three age categories pooled). The basis for the maps is available under the Open Database License (www.openstreetmap.org).

3 Results

During the two field sampling events, altogether 39 adult marbled crayfish (11 + 28 females) and 9 spiny-cheek crayfish Orconectes limosus (7 + 2 individuals of both sexes) were captured. All marbled crayfish were caught above the pumping station in the Chorvátske rameno canal, while all spiny-cheek crayfish individuals were caught into traps below the pumping station in the Jarovecké rameno side arm (Fig. 1B).

The carapace length (totalling ca. 50% of the body size) of marbled crayfish specimens ranged from 21.8 to 48.1 mm, with a mean of 39.2 mm (Fig. 1C). In total, 27 marbled crayfish (69% of the catch) carried eggs or juveniles. The quantity of the offspring ranged between 147 and 647 (on average 420) eggs or juveniles per female, with a positive correlation with the size of the mother (Fig. 1C). Altogether, the 27 captured berried females carried 11 348 offspring. No trace of A. astaci DNA was detected in any analysed marbled crayfish.

Of the spiny-cheek crayfish (6 males, 3 females, carapace length 25.0–52.1 mm, mean 42.6 mm), one specimen was confirmed as being infected with A. astaci (agent level A3, according to the method of Vrålstad et al., 2009).

4 Discussion

Due to irresponsible or uninformed hobby breeders, marbled crayfish are intentionally released into the wild and become established, as documented across Europe (Chucholl et al., 2012; Kouba et al., 2014). Most of the sites with well-documented established populations are lentic habitats relatively isolated from the main watercourses. However, records from some sizeable rivers (e.g. the Rhine in Germany or the Po delta in Italy) were also reported, although their recent population status remains unclear (Chucholl et al., 2012; Vojkovská et al., 2014; Patoka et al., 2016 and literature cited therein). Weiperth et al. (2015) refer to several specimens of various sizes detected in thermal ponds and their outflows including adjacent Danube in Budapest, Hungary. Evaluation of the population status in the river is an issue of on going research (Weiperth A., pers. comm., 2017).

The newest discovered site with the marbled crayfish in Bratislava, Slovakia, also occurs in the immediate vicinity of the Danube, separated only by a pumping station that occasionally releases its waters to one of the river arms. This section of the Danube is already colonised by the non-indigenous spiny-cheek crayfish which invaded this river section in the last two decades and, recently, also by signal crayfish Pacifastacus leniusculus (Lipták and Vitázková, 2014). We have not confirmed syntopic occurrence of marbled crayfish with these species yet, but we consider that confirmation of marbled crayfish in the side arm of the Danube is just a matter of time and search effort. Water pumping, intentional translocation of marbled crayfish by humans, or active migrations of marbled crayfish, are factors that can transfer (or may have already transferred) the species into the Danube (Chucholl et al., 2012; Lipták et al., 2016).

The conditions in the side arm of the Danube, Jarovecké rameno, are favourable for crayfish, as indicated by the locally present spiny-cheek crayfish population. The documented presence of A. astaci in that species corresponds to its infection status elsewhere in the Danube (Kozubíková et al., 2010; Pârvulescu et al., 2012). Upon contact of marbled crayfish with infected spiny-cheek crayfish, we may expect a horizontal transmission of A. astaci between the two host species (see James et al., 2017). This means that thereafter the marbled crayfish expansion in the Danube catchment will be very likely accompanied by the expansion of the crayfish plague pathogen, which causes mass mortalities of indigenous crayfish stocks in Europe (Holdich et al., 2009).

Any attempts to eradicate this marbled crayfish population are likely to be ineffective because of its obligate parthenogenetic reproduction mode, when even a single survivor may re-establish the whole population. Its remarkable reproductive capacity and extremely high fecundity, low-temperature tolerance and high competitiveness (Vodovsky et al., 2017 and literature cited therein) all suggest that the marbled crayfish will become a permanent part of the Danube ecosystem, with great potential for an extension of its range, with largely unknown consequences so far. Some of its life history characteristics (e.g. higher fecundity, earlier maturation, supposedly faster growth and more reproduction events per year) provide significant advantages, even compared to other non-indigenous crayfish species already present in this section of the Danube, the spiny-cheek crayfish and the signal crayfish (Lipták and Vitázková, 2014).

To conclude, we expect that marbled crayfish might be already present in a side arm of the Danube, where horizontal infection with crayfish plague pathogen originating from spiny-cheek crayfish will occur. We presume that the marbled crayfish will spread actively further (mainly downstream), but its range extension may be accelerated by the occasional floods where successful reproduction of even single dispersed specimens is not limited. A competition with this new invader might have severe consequences for remaining stocks of the indigenous narrow-clawed crayfish Astacus leptodactylus, already under pressure of spiny-cheek crayfish (cf. Pârvulescu et al., 2012, 2015). Successful competition of marbled crayfish with other non-indigenous crayfish species already present in the Danube may also be expected. However, given the role of crayfish in ecosystems in general and characteristics of marbled crayfish in particular, the spread of marbled crayfish has the potential for significant consequences for much broader range of taxa. This is a serious issue since the Danube possesses habitats for diverse biota, being a unique ecosystem of European importance. Future monitoring of marbled crayfish in the Danube is warranted, but at early phases of establishment may be methodologically challenging in such large river course. Utilisation of eDNA methods might be an useful tool in this regard.

Acknowledgments

This study was supported by the Ministry of Education, Youth and Sports of the Czech Republic – projects “CENAKVA” (No. CZ.1.05/2.1.00/01.0024) and “CENAKVA II” (No. LO1205 under the NPU I program) and the Grant Agency of the University of South Bohemia (012/2016/Z). We acknowledge Boris Kováč (Slovak Water Management Company, state enterprise) for technical details on Chorvátske rameno canal, and Agata Mrugała for indispensable support in the lab. We appreciate constructive comments of two anonymous referees.

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Cite this article as: Lipták B, Mojžišová M, Gruľa D, Christophoryová J, Jablonski D, Bláha M, Petrusek A, Kouba A. 2017. Slovak section of the Danube has its well-established breeding ground of marbled crayfish Procambarus fallax f. virginalis. Knowl. Manag. Aquat. Ecosyst., 418, 40.

All Figures

thumbnail Fig. 1

Map showing the marbled crayfish Procambarus fallax f. virginalis occurrence in Bratislava, Slovakia – general view (A) and detailed location (B). Asterisk refers to the pumping station, while 1 and 2 to the locations in the Chorvátske rameno canal and the Jarovecke rameno side arm where marbled crayfish and spiny-cheek crayfish Orconectes limosus were found, respectively. Fecundity of marbled crayfish females (C) expressed as the number of eggs (circles), stage 1 (triangles) and stage 2 juveniles (squares), respectively, and the relationship between female carapace size and the number of offspring (exponential regression, with all three age categories pooled). The basis for the maps is available under the Open Database License (www.openstreetmap.org).
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