Issue
Knowl. Manag. Aquat. Ecosyst.
Number 418, 2017
Topical issue on Crayfish
Article Number 30
Number of page(s) 7
DOI https://doi.org/10.1051/kmae/2017018
Published online 23 June 2017

© T. Uderbayev et al., Published by EDP Sciences 2017

Licence Creative Commons
This 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

The international pet industry encompasses numerous freshwater and marine species (Tlusty et al., 2013). In contrast to the long history of trade and keeping of tremendously popular freshwater fish and molluscs, the pet trade with freshwater ornamental decapod crustaceans including crayfish, shrimps and crabs has started rather late, in the mid-1990s (Scholtz et al., 2003; Chucholl, 2013; Patoka et al., 2016a).

Globally, we can found numerous examples of human-mediated introductions of non-native ornamental decapod crustaceans (Magalhães et al., 2005; Kawai et al., 2009; Klotz et al., 2013; Vojkovská et al., 2014; Lipták et al., 2016; Patoka et al., 2016d). Negative consequences such as out-competition with native species, disease spread, food web and habitat alternation, and incidental fauna introduction are widely discussed (Duggan, 2010; Gherardi et al., 2011; Chucholl and Wendler, 2016; Patoka et al., 2016a; Souty-Grosset et al., 2016). Although pet trade has been considered one of the most important sources of non-native species (Padilla and Williams, 2004; Duggan, 2010), risk assessment of decapod crustaceans introduced via this pathway had been marginalized for a long time. The situation began to change in recent years (see Soes and Koese, 2010; Chucholl, 2013; Faulkes, 2014; Papavlasopoulou et al., 2014; Patoka et al., 2014a; Mazza et al., 2015; Kotovska et al., 2016). Since mitigation and eradication are difficult and mostly impossible when non-native species become established (Aquiloni et al., 2009), the importance of prevention is obvious (Souty-Grosset et al., 2016). In this regards, the climatic modelling and risk assessment are processed by various tools to high-risk species identification.

Pet-traded freshwater animals and ornamental plants are not kept exclusively in indoor tanks, but they are also frequently released into the garden and urban ponds (Hassall, 2014; Patoka et al., 2016b, c). Despite the unexceptional illegality of this act, it is also true for freshwater decapod crustaceans (Peay, 2009; Patoka et al., 2014b; Novitsky and Son, 2016). Leading markets with ornamental freshwater decapod crustaceans globally are the Czech Republic (Patoka et al., 2015), Germany (Chucholl, 2013; Chucholl and Wendler, 2016) and the USA (Faulkes, 2015b), followed by several other countries such Brazil (Magalhães et al., 2005), Greece (Papavlasopoulou et al., 2014), Russia (Vodovsky et al., 2017), Slovakia (Lipták and Vitázková, 2015), Turkey (Turkmen and Karadal, 2012) and Ukraine (Kotovska et al., 2016).

Within the meaning of pet trade, Central Asia is not perceived as an important market with freshwater decapod crustaceans. The economically dominant country of this region is the Republic of Kazakhstan (further referred as Kazakhstan) (Takenov et al., 2004; Pomfret, 2006). With 2.72 million km2 of land it is the world's largest landlocked country and its territory forms eight internal-drainage basins, none of which have a direct outflow into an ocean (Takenov et al., 2004).

Especially crayfish are perceived as animals with great and not fully exploited potential in aquaculture production in Kazakhstan. Although the taxonomy of Eastern European and Central Asian crayfish taxa are to a certain degree still non-settled, the usually accepted state is that native Kazakhstan decapods are represented by two crayfish species occurring in western part of the country: Astacus leptodactylus and Astacus pachypus (Malinovskaia, 1984; Kirichenko et al., 2013; Kouba et al., 2014). Even if data from the eastern part of the country are almost lacking, some fragmentary information appears to indicate that crayfish also live here, at least in Balkhash Lake where are preyed by invasive fish species (Mamilov, 2015). No relevant information about the origin of these animals are available, but local people are convinced that the crayfish were introduced from Russia (Isaev and Karpova, 1989).

Furthermore, there are known two non-native decapod species currently occurring in Kazakhstan waterbodies: shrimps Palaemon modestus and Macrobrachium nipponense. Freshwater shrimp P. modestus native to eastern Asia was found established in the Ili River, flowing to Balkhash Lake, Almaty region, south-eastern Kazakhstan (De Grave and Mann, 2012). In this species, larval development is shortened as an adaptation to freshwater environment and thus there is no barrier to its spreading within landlocked regions (Kwon and Uno, 1968). The occurrence of M. nipponense native to China, Japan, Korea, Myanmar, Taiwan and Vietnam (De Grave and Ghane, 2006) was recorded in the Kapchagay Reservoir, a main dam on the Ili River (Alekhnovich and Kulesh, 2001). This species is highly adaptable under different environmental conditions and it can survive in freshwater for its entire life cycle (Mashiko, 1990). Although the introduction pathways related with both species in Kazakhstan remain rather unclear, De Grave and Ghane (2006), Mirabdullaev and Niyazov (2005) and De Grave and Mann (2012) suggested as the most probable the intentional introduction for consumption purposes or accidental escapes from aquaculture or ornamental stocks.

Although nothing is known about pet industry development in Kazakhstan, based on the aforementioned note, we hypothesised that the overlooked pet trade with decapod crustaceans exists in the country. Hence the objectives of the present study are: (i) the survey of market and compilation of the list of pet-traded decapods, and (ii) identification of potentially invasive species and assessment of related environmental risks.

2 Material and methods

2.1 Data collection

Information about pet-traded species of decapod crustaceans and their availability on Kazakhstan market were obtained over a period of May and October 2016. Altogether, we interviewed four wholesalers, five pet shop owners, two online shops and two local crayfish breeders. Two local pet bazaars (places where people can sell or change pets) were also visited. Collected records were subsequently clarified during personal visits and/or provided photo-documentation and misnomers as well as alternative trade names were eliminated.

2.2 Availability on market

Availability on market was evaluated for each species according to Chucholl (2013) using the following criteria: (i) “very rare” species available only for a short period and in low quantities; (ii) “rare” species available occasionally in low quantities; (iii) “common” species available frequently in low quantities; and (iv) “very common” species always available in high quantities. Even if this method is to a certain degree heuristic, it is useful for a rough estimate of species availability on market (Kotovska et al., 2016).

2.3 Climate match

Climatic conditions used for analysis of probability of survival were represented in our analysis by temperature during the coldest quarter of the year as a variable. The climate match between source and target area was compared using the Climatch tool (v.1.0; Invasive Animals Cooperative Research Centre, Bureau of Rural Sciences, http://data.daff.gov.au:8080/Climatch/climatch.jsp); we opted Euclidean algorithm. This tool was used in previous studies focusing decapod crustaceans (e.g. Chucholl, 2013; Patoka et al., 2014a; Kotovska et al., 2016). We used region of the native geographic range of evaluated species as the source area; in the case of marbled crayfish Procambarus fallax f. virginalis, which native occurrence is not yet known, the source region was taken in accordance with Chucholl (2014) as validated European localities with its established populations. The target area was defined as the territory of Kazakhstan containing 341 climatic stations from the database of the WorldClim (Hijmans et al., 2005). Where the climate match between the source area and the climatic station in the target area reached score ≥7.0, this was interpreted as there is no environmental barrier to the survival of evaluated species.

2.4 Risk assessment

To assess a potential invasiveness degree of decapod crustaceans traded in Kazakhstan, we utilised the Freshwater Invertebrate Invasiveness Scoring Kit produced by the UK Centre for Environment, Fisheries and Aquaculture Science (FI-ISK, v.1.19, https://www.cefas.co.uk/services; Tricarico et al., 2010). Based on computed FI-ISK score, each evaluated species was subsequently classified as: (i) low (score <1); (ii) medium (score ≥1 but <16); and (iii) high (score ≥16) from risk in target area perspective.

3 Results

In total, we recorded at least 16 species of decapod crustaceans pet-traded in Kazakhstan. This set contains 11 shrimp (8 from family Atyidae and 3 from family Palaemonidae), four crayfish (two from family Cambaridae and 2 from family Parastacidae), and one crab species (family Potamidae). The complete list of species and their current availability on market are given in Table 1. Since species identifications of some shrimps according to morphology were not clear, these taxa were not evaluated in risk assessment. Three species were found very common on the market accompanied by three common, five rare and two very rare species.

Climatic data showed the highest probability of establishment in two shrimps M. nipponense and P. modestus (score ≥8 on entire target area) followed by shrimps Neocaridina heteropoda and Caridina multidentata, crab Potamon potamios and crayfish Procambarus clarkii (wild and white morph) and P. fallax f. virginalis.

The FI-ISK score ranged between values of −2 and 30. Two shrimp species were assessed as low-risk, seven shrimp species, one crayfish and the crab were classified as medium-risk, and three crayfish were classified in high-risk category (Tab. 1). The probability of establishment of the high-risk species, crayfish C. destructor, P. clarkii, and P. fallax f. virginalis, within Kazakhstan territory is shown in Figure 1.

Table 1

List of pet-traded species of decapod crustaceans and their families, availability on market (VC, very common; C, common; R, rare; VR, very rare), potential invasiveness (FI-ISK score), risk category (FI-ISK category), nursery environment required for larval or juvenile development, environment for adult individuals (B, brackish water; F, freshwater), and native distribution (AF, Africa; AU, Australia; EA, East Asia; J, Japanese Archipelago; NA, North America; NG, New Guinea; SEA, South-eastern Asia).

thumbnail Fig. 1

Climate match map of Kazakhstan showing colour-coded regions with a different probability of establishment of the most hazardous from all evaluated species: (a) marbled crayfish (Procambarus fallax f. virginalis), (b) red swamp crayfish (Procambarus clarkii), and (c) yabby (Cherax destructor); scores of ≥7.0 are interpreted as there is no environmental barrier to survival.

4 Discussion

All ornamental decapod crustaceans found pet-traded in Kazakhstan are non-native in this landlocked country. Since we recorded collection of at least 16 species (Tab. 1), it is obvious that the pet trade with these animals is probably well-developed and popular in more countries than were previously overlooked in this regard.

The majority of found pet-traded species are adapted to the freshwater environment within their entire life cycle (Tropea et al., 2015). However shrimp C. multidentata and two fan shrimps, Atya gabonensis and Atyopsis moluccensis, live in freshwaters in adulthood only and their free-living larvae require brackish water for successful development (Page et al., 2008) (Tab. 1). Although Kazakhstan has no connection with ocean, larvae of M. nipponense can tolerate brackish conditions in the Caspian Sea with salinity circa 10–13 g/L (De Grave and Ghane, 2006). Hence we assume that, in the case of mentioned shrimp species, there is no barrier to their larval development and survival in Kazakhstan in this regard.

Probably the most important climatic factor affecting the survival of decapod crustaceans is temperature (Hartnoll, 2001). Aforementioned fan shrimps are not capable of acclimating to climatic conditions in Kazakhstan. Based on evaluated climatic matching, we identified as species with the highest probability of establishment two shrimps M. nipponense and P. modestus, both species previously introduced in Kazakhstan (De Grave and Ghane, 2006; De Grave and Mann, 2012). These species are followed to a lesser extent shrimps N. heteropoda and C. multidentata, crab P. potamios, and crayfish P. fallax f. virginalis (Fig. 1a) and P. clarkii (Fig. 1b). The climatic matching of the rest of recorded species was very low. From these species, two shrimps, C. multidentata and N. heteropoda, are very common on the market following by common crayfish P. fallax f. virginalis. Availability on market is highly comparable with the situation in other countries (Faulkes, 2015b; Lipták and Vitázková, 2015; Patoka et al., 2015). The origin of traded decapods in Kazakhstan is unclear. Nevertheless, the market is probably saturated by exports from Russia similarly as could be in Ukraine (Kotovska et al., 2016), but imports from China and South-Eastern Asia are also expected. Domestic production of some easily bred species such shrimp N. heteropoda and crayfish P. fallax f. virginalis is also possible.

In comparison with previously analysed markets in European countries (e.g. Chucholl, 2013; Patoka et al., 2015; Kotovska et al., 2016) and in the USA (Faulkes, 2015b), no crayfish species from genera Cambarellus were found traded in Kazakhstan. Since some of these species such as Cambarellus patzcuarensis are very common on mentioned markets, their absence in Kazakhstan suggests that the pet trade with crayfish is still developing with a probable increase in the number of traded species in near future. Also other colour morphs of P. clarkii such as full red, blue, orange and ghost are prospective in this regard.

Faulkes (2015a) mentioned two major threats for native decapods caused by pet trade: the potential for overexploitation of native species and negative consequences related to non-native species releases and escapes. Currently, no native species has been found pet-traded in Kazakhstan, but expected a further increase in the number of traded species and growing popularity of their keeping may result into the exploiting of native crayfish as well. Considering risk assessment, the origin of particular species, their availability on the market, the probability of establishment and further aspects, we identified crayfish P. clarkii and P. fallax f. virginalis being the seriously hazardous taxa with high invasive potential within Kazakhstan territory. The origin of the latter was exclusively derived from aquarium-bred individuals since native populations of this species are not yet known (Martin et al., 2016). This crayfish reproduces exclusively unisexually (parthenogenetically) and thus a single female can theoretically establish a viable population that might outcompete native crayfish (Scholtz et al., 2003). Moreover, both mentioned species were confirmed to serve as a host and vector of the crayfish plague, the disease caused by the oomycete Aphanomyces astaci, which is almost lethal for both Kazakhstan native crayfish species (Keller et al., 2014; Mrugała et al., 2015; Svoboda et al., 2017). The adaptability to environmental changes like precipitation (Kouba et al., 2016) together with the low-temperature tolerance (Veselý et al., 2015), and extremely fast growth and reproduction features (Vogt et al., 2004; Souty-Grosset et al., 2016) make these crayfish species to be “perfect invaders”. This assumption has been confirmed by numerous examples of introduction and establishment in natural habitats. P. clarkii has been successfully introduced in all continents except Australia and Antarctica, e.g. it is recorded currently in 16 European countries (summarized in Gherardi, 2006; Souty-Grosset et al., 2016); and P. fallax f. virginalis established wild populations particularly in Germany (Chucholl et al., 2012), but it was also reported from Croatia (Samardžić et al., 2014), the Czech Republic (Patoka et al., 2016e), Hungary (Weiperth et al., 2015; Lőkkös et al., 2016), Italy (Nonnis Marzano et al., 2009; Vojkovská et al., 2014), the Netherlands (Koese, 2008), Slovakia (Janský and Mutkovič, 2010; Lipták et al., 2016), Sweden (Bohman et al., 2013), Ukraine (Novitsky and Son, 2016), and outside of Europe in Madagascar (Jones et al., 2009; Kawai et al., 2009). Though salinity tolerance in P. fallax f. virginalis seems to be low, it is much higher in P. clarkii (Veselý et al., 2017 and references therein). This opens an issue of direct interactions even with stocks of native crayfish A. leptodactylus and A. pachypus in the Caspian Sea, the more that this region fulfil temperature requirements of both non-native crayfish (Vodovsky et al., 2017). Aforementioned facts have caused concern among local as well as international authorities which were consequently reflected in certain legislative restrictions such as the list of Invasive Alien Species of European Union Concern (EU Regulation No. 1143/2014; Commission Implementing Regulation No. 2016/1141). In case of found pet-traded Cherax species, C. quadricarinatus is not able to successfully overwinter under climatic conditions in Kazakhstan; and even if C. destructor can be perceived as hazardous species, its probability of establishment in the territory of Kazakhstan is also very limited (Fig. 1c).

Therefore, we highlight as necessary and crucial a further survey of lentic habitats near conurbations at least in Kazakhstan regions identified as threatened by the potential establishment of both P. clarkii and P. fallax f. virginalis. The attention should be focused especially on popular secondary habitats, such as gravel pit lakes, garden and park ponds where these crayfish are particularly released by hobbyists in other countries (e.g. Chucholl et al., 2012; Novitsky and Son, 2016; Souty-Grosset et al., 2016). If these crayfish will be found, stakeholders are strongly encouraged to initiate their eradication. To prevent new introductions, similarly as in the case of European Union, we recommend the total ban of import, trade and keeping of these high-risk taxa within Kazakhstan and adjoining countries in Central Asia.

Acknowledgements

This study was supported by the Internal Grant Agency of the Czech University of Life Sciences Prague “CIGA” (No. 20152007), and 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).

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Cite this article as: Uderbayev T, Patoka J, Beisembayev R, Petrtýl M, Bláha M, Kouba A. 2017. Risk assessment of pet-traded decapod crustaceans in the Republic of Kazakhstan, the leading country in Central Asia. Knowl. Manag. Aquat. Ecosyst., 418, 30.

All Tables

Table 1

List of pet-traded species of decapod crustaceans and their families, availability on market (VC, very common; C, common; R, rare; VR, very rare), potential invasiveness (FI-ISK score), risk category (FI-ISK category), nursery environment required for larval or juvenile development, environment for adult individuals (B, brackish water; F, freshwater), and native distribution (AF, Africa; AU, Australia; EA, East Asia; J, Japanese Archipelago; NA, North America; NG, New Guinea; SEA, South-eastern Asia).

All Figures

thumbnail Fig. 1

Climate match map of Kazakhstan showing colour-coded regions with a different probability of establishment of the most hazardous from all evaluated species: (a) marbled crayfish (Procambarus fallax f. virginalis), (b) red swamp crayfish (Procambarus clarkii), and (c) yabby (Cherax destructor); scores of ≥7.0 are interpreted as there is no environmental barrier to survival.

In the text

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