Knowl. Manag. Aquat. Ecosyst.
Number 418, 2017
Topical issue on Crayfish
|Number of page(s)||7|
|Published online||12 May 2017|
Salinity tolerance of marbled crayfish Procambarus fallax f. virginalis
Tolérance à la salinité de l'écrevisse marbrée Procambarus fallax f. virginalis
University of South Bohemia in České Budějovice, Faculty of Fishery and Protection of Waters, South Bohemian Research Centre of Aquaculture and Biodiversity of Hydrocenoses,
Vodňany, Czech Republic
2 CBMA − Centre of Molecular and Environmental Biology, Department of Biology, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal
⁎ Corresponding author: firstname.lastname@example.org
Eastern Europe comprises a significant part of the native ranges for indigenous crayfish species (ICS) belonging to the genus Astacus. This region has been largely overlooked by astacologists and considered relatively immune to the impacts of non-indigenous crayfish species (NICS). The recent discovery of two marbled crayfish Procambarus fallax f. virginalis populations in Ukraine has changed this view. Increased propagule pressure (mainly due to pet trade) has raised concerns of NICS which may negatively impair the ecosystems of Azov, Black and Caspian Seas and their tributaries inhabited by ICS. In this study, we provide the first insight into salinity tolerance of marbled crayfish. We performed a 155-day experiment using 5 different salinities (6, 9, 12, 15, and 18 ppt) and a freshwater control. Evaluation of survival, growth and reproduction suggests that marbled crayfish have a lower salinity tolerance than other crayfish species, which may limit their invasive potential in brackish environments. However, its ability to survive for more than 80 days at 18 ppt opens up the possibility of gradual dispersion and adaptation to brackish conditions. Our study highlights the need for further studies elucidating the potential for marbled crayfish to negatively impair these ecosystems.
L'Europe de l'Est comprend une partie importante des régions abritant des espèces indigènes d'écrevisses (ICS) appartenant au genre Astacus. Cette région a été largement ignorée par les astacologues et considérée comme relativement protégée des impacts des espèces d'écrevisses non indigènes (NICS). La découverte récente de deux populations d'écrevisses marbrées Procambarus fallax f. virginalis en Ukraine ont changé cette vision. Le potentiel d'augmentation de la pression des propagules (principalement en raison du commerce des animaux de compagnie) a soulevé des préoccupations concernant les NICS qui pourraient nuire aux écosystèmes des mers d'Azov, Noire et Caspienne et à leurs affluents habités par des ICS. Dans cette étude, nous fournissons le premier aperçu de la tolérance à la salinité des écrevisses marbrées. Nous avons effectué une expérience de 155 jours en utilisant 5 salinités différentes (6, 9, 12, 15, 18 ppt) et un contrôle d'eau douce. L'évaluation de la survie, de la croissance et de la reproduction suggère que les écrevisses marbrées ont une tolérance à la salinité plus faible que les autres espèces d'écrevisses, ce qui peut limiter leur potentiel invasif dans les milieux saumâtres. Cependant, sa capacité à survivre pendant plus de 80 jours à 18 ppt ouvre la possibilité d'une dispersion progressive et d'une adaptation aux conditions saumâtres. Notre étude souligne la nécessité de poursuivre les études permettant d'éclaircir le potentiel de l'écrevisse marbrée à nuire négativement à ces écosystèmes.
Key words: brackish environment / growth / reproduction / moult / survival
Mots clés : environnement saumâtre / croissance / reproduction / mue / survie
© L. Veselý et al., Published by EDP Sciences 2017
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Salinity is an important abiotic factor influencing crucial processes of animals such as feeding, growth, and reproduction, which determines their long-term survival, distribution and success in ecosystems (Snell, 1986; Ball, 1998; Sousa et al., 2006, 2007, 2008; Costa-Dias et al., 2010). Species are generally divided into euryhaline and stenohaline organisms, which specify their ability to adapt to a wide or narrow range of salinities, respectively (Croghan, 1976). Basically, freshwater species do not invade marine environments. However, species with marine ancestry may tolerate a wide range of salinities, while this pattern strongly varies across and within taxa (Hart et al., 1991). Despite physiological changes and potential detrimental effects of elevated salinities to freshwater organisms (Heugens et al., 2001; Nielsen et al., 2003), they can migrate through saline ecosystems (van Ginneken and Maes, 2005; Jaszczołt and Szaniawska, 2011; Kornis et al., 2012). However, this window of opportunity is often limited, and related to a specific part of their life cycle (juvenile stages and reproduction are usually vulnerable to higher salinity) due to physiological constrains (Holdich et al., 1997; Anger, 2003). Thus salinity is of paramount importance for the spread of freshwater animals into new areas (Croghan, 1976; Leppäkoski and Olenin, 2000) due to, for example, possible dispersion to new watersheds through different estuaries. Also, the ionic composition of water, i.e., the ratio of cations to anions together with the pH, strongly affects the magnitude of saline toxicity to freshwater organisms (Frey, 1993; Bailey and James, 2000). Therefore, life history features together with general ecological information (e.g., distribution, abundance and population structure) should be taken into account when evaluating the effects of salinity.
Biological invasions are a significant threat to native biodiversity worldwide, with important ecological and economic impacts (Simberloff et al., 2013; Seebens et al., 2017). These impacts are particularly important in freshwater ecosystems (Strayer, 2010; Sousa et al., 2014; Moorhouse and Macdonald, 2015). Conversely, estuaries and coastal areas have been overlooked in this regard within the last decades (Cohen and Carlton, 1998; Grosholz, 2002). Nowadays, these heavily invaded ecosystems are used as biological corridors for species that are able to withstand saline conditions (Grosholz, 2002). To our knowledge there are only a few studies dealing with invasion of freshwater species into saline environments (Leppäkoski and Olenin, 2000; Gonçalves et al., 2007). Interestingly, some of these few studies assess the colonization of brackish waters by red swamp crayfish Procambarus clarkii in Europe, e.g., Sousa et al. (2013) and Meineri et al. (2014). Considering biological invasions, the EU parliament and Council have listed some non-indigenous invasive species considered to be of high concern to European biodiversity (EU Regulation No. 1143/2014; Commission Implementing Regulation No. 2016/1141). It lists 23 animals of which freshwater crayfish form a remarkable group of five representatives. This clearly highlights the invasive potential, ecological and economic importance of at least some members in this animal group, as documented mainly in Europe and various parts of North America (Lodge et al., 2000; Holdich et al., 2009). Marbled crayfish Procambarus fallax f. virginalis is one of these listed animals. Its all-female stocks exclusively reproduce via apomictic parthenogenesis, thus producing clones that exhibit fast growth, early maturation, and high fecundity (Seitz et al., 2005; Martin et al., 2010). As presumed from its North American origin, it has also been proven to be a chronic carrier of crayfish plague Aphanomyces astaci pathogen (Keller et al., 2014; Mrugała et al., 2014). Marbled crayfish is a capable burrower (Kouba et al., 2016) with the ability to overwinter in the temperate zone (Veselý et al., 2015; Lipták et al., 2016). Marbled crayfish were first discovered in the German aquarist trade in the mid-1990s, from where it dispersed (Scholtz et al., 2003). The pet trade is an important pathway for the spread of non-indigenous taxa, and marbled crayfish are one of the most frequent and environmentally risky crayfish traded (Patoka et al., 2014). Due to irresponsible or uninformed hobbyists, it may intentionally or accidentally be introduced into the wild (Chucholl, 2013; Patoka et al., 2014). Indeed, reports on the presence of single specimens in the wild occurred at the beginning of the new millennium, followed by confirmed established populations in Germany and Slovakia in 2010. Since then, the number of invaded European countries has substantially increased (Patoka et al., 2016, and references cited therein).
Eastern Europe possesses the entire native ranges, or at least their significant parts, for indigenous crayfish species (ICS) belonging to the genus Astacus, especially thick-clawed crayfish Astacus pachypus (Kouba et al., 2014). This region has been largely overlooked by astacologists and considered relatively safe from the adverse impacts of gradually expanding non-indigenous crayfish species (NICS) (Perdikaris et al., 2012). Discovery of two distant marbled crayfish Procambarus fallax f. virginalis populations in Dnipropetrovsk and Odessa, Ukraine in 2015 drastically changed this view (Novitsky and Son, 2016). Pet trade surveys provide extended lists of NICS, often of North American origin, both in the Ukraine (Kotovska et al., 2016) and Lower Volga region of the Russian Federation (Vodovsky et al., 2017). This has raised concerns of NICS potential to negatively impact the unique ecosystems of Azov, Black and Caspian Seas as well as their tributaries that are inhabited by ICS. Therefore, our goal was to investigate survival, growth, and reproduction of marbled crayfish in a range of salinities. This information will be important for implementation of possible management measures regarding the spread of this species in Eastern Europe, but also in estuaries elsewhere.
We conducted a 155-day experiment, lasting from the second half of May to the second half of October 2016, on salinity tolerance in marbled crayfish Procambarus fallax f. virginalis. This time of year normally includes a seasonal peak in reproduction (Vogt, 2015). The experiment was conducted at the Research Institute of Fish Culture and Hydrobiology in Vodňany, Czech Republic and we used animals from our own laboratory culture. Ten specimens (five in two replicates) for each of 6 experimental treatments, 60 animals in total, were used. The experiment was divided into two parts. Animals were first acclimated in a step-wise manner for 5 days to the target levels of salinity (final salinities of 6, 9, 12, 15, and 18 ppt, respectively). On the first day of acclimation crayfish were moved from fresh water to a saline environment of 6 ppt. Subsequently, salinities were gradually elevated by 3 ppt per day until the target levels were reached. During the acclimation period all crayfish were divided into 12 static aquaria (described below) with 5 specimens per aquarium (10 aquaria with saline conditions and two aquaria with fresh water serving as a control). The aquaria (36 × 29.5 × 54 cm) were always filled with 16 L of aged tap water with or without salt added depending on the treatment. For ion composition of source water, see Table 1. Aquaria were covered by a plastic lid to limit water evaporation and aerated. To minimize aggression, the shelters were provided. For this, two blocks of joined polypropylene tubes, each containing five tubes (length 10 cm, inner diameter 35 mm), were added to each aquarium. The base of each block was represented by three longitudinally joined tubes with a further two tubes positioned pyramidal in the second layer.
The second part of the experiment started immediately after acclimation. Crayfish were held in the same aquaria as in the acclimation period and individually marked with nail polish on specific places on the carapace (Buřič et al., 2008). Every day observations noting the number of individuals alive in each lot, the number of moulting and the presence of eggs were performed. After visual checking, impurities (e.g., faeces and unconsumed food) were gently siphoned. Offspring was counted at the second developmental stage. When crayfish moulted, the marking was renewed when the animal re-calcified their exoskeleton. To maintain water quality, all baths were changed twice per week (Tue and Fri). The light regime was 12L:12D. Water temperature was recorded hourly by means of a temperature sensor MINIKIN (Environmental measuring systems, Brno, Czech Republic) and kept at 20.6 ± 0.7 °C. Crayfish were fed daily in excess with commercial dry feed for aquarium fish enriched with algae (Sera Granugreen, Sera GmbH, Germany) and frozen chironomid Chironomus sp. larvae.
We decided to generalize our experimental design by adding common salt (NaCl p.a., Penta s.r.o., Czech Republic), considering that marine water has specific profiles of salts, and these ions represent the bulk of the compositions. The range of tested salinities was chosen based on specific conditions in the target region and by the continental context. Average salinities of 10–12, 12–13 and 17–18 ppt correspond to the Azov, Caspian and Black Seas, respectively (Berdnikov et al., 1999; Jazdzewski and Konopacka, 2002; Pourkazemi, 2006). Thus, salinity values tested in this experiment are relevant both for the mentioned Seas and estuaries elsewhere.
Prior to the experiment, crayfish were measured (digital calliper; Proma CZ Ltd., Mělčany, Czech Republic) and weighed (analytical balance; Kern & Sohn GmbH, Balingen, Germany) to the nearest 0.1 mm and 0.1 g, respectively. Mean ± SD carapace length (29.9 ± 2.3 mm) and weight (5.3 ± 1.5 g) of marbled crayfish did not differ among all experimental groups, i.e., saline and control groups (F5,54 = 0.39, p = 0.95 and F5,54 = 0.53, p = 0.87, respectively). Following re-calcification (usually 2–3 days after moulting), crayfish biometry was re-measured. For assessment of growth, the following indices were calculated: (1)
Firstly, we counted specific growth rate (SGR; Eq. (1)), where Wt is weight at time t, Wi is initial weight and T is time in days. (2)
Secondly, we counted absolute carapace length increment at moult (Lm; Eq. (2)), specifically for each moult separately. La is carapace length after moult and Lb is length before moult.
Ion composition of aged tap water used in experiment. Water analyses conducted in the accredited laboratory of the AGRO-LA, spol. s r.o., Jindřichův Hradec, Czech Republic.
Non-parametric survival analysis (Kaplan–Meier method) was performed for all groups, using survival package (Therneau and Grambsch, 2000). To confirm normality in data (Kolmogorov–Smirnov test) one-way ANOVA followed by Tukey's HSD test was performed to compare initial biometry, and absolute length increments and SGR values among groups if applicable. Relationships between initiated and successful moult as well as ovulation were evaluated by means of a Spearman-rank correlation. All analyses were conducted in R version 3.2.5 (R Core Team, 2016). The null hypothesis was rejected at α < 0.05 in all tests in this study.
Marbled crayfish survival rate differed among tested conditions (χ2 = 31.3, df = 5, p ≤ 0.001; Fig. 1). At the end of the experiment, survivors were found only in three experimental groups – control (n = 8), 9 and 12 ppt, each having a single specimen after 155 days. In other salinity conditions (6, 15, and 18 ppt) no crayfish survived but the last specimens died at different times (146, 87, and 91 days, respectively). When control was removed from survival analysis, we found no differences among salinity conditions (χ2 = 7, df = 4, p = 0.13). Additionally, neither carapace length (F5,54 = 1.03, p = 0.31) nor weight (F5,54 = 0.66, p = 0.41) significantly influenced marbled crayfish survival among salinity conditions.
Salinity negatively influenced physiological processes such as growth, moulting and reproduction of marbled crayfish (Tab. 2). Salinity significantly decreased all measures of moulting (number of initiated, number of successful; Spearman-rank correlation, p < 0.05), SGR (F1,30 = 10.74, p < 0.001), and Lm (F1,30 = 9.37, p < 0.001). Only in the control five specimens successfully moulted twice. Salinity negatively influenced ovulation rate and reproduction success of marbled crayfish (Spearman-rank correlation, p < 0.05). Females ovulated in all experimental groups, while successful reproduction (reaching 2nd developmental stage) was confirmed only in the control. One female reproduced twice. No apparent cannibalism was observed during the experiment.
Survival analysis plot of marbled crayfish Procambarus fallax f. virginalis kept under different salinities.
Growth and reproduction indices of marbled crayfish Procambarus fallax f. virginalis kept under different salinities. Growth indices presented as mean ± SD. Reproduction indices refer to number of specimens. Values with differing superscripts in given column are significantly different (one-way ANOVA, Tukey's HSD test, p < 0.05).
Growth and reproduction are the most important processes expressing fitness and adaptation of species (Guan and Wiles, 1999). Most crayfish are able to survive in saline environments from a few days to a few months, while the effects of salinity on physiological processes differ among crayfish species and families (Jones, 1989; Holdich et al., 1997; Alcorlo et al., 2008). According to Jaszczołt and Szaniawska (2011) spiny-cheek crayfish Orconectes limosus are able to successfully reproduce and grow at salinity up to 7 ppt, but growth could be limited in more saline conditions. These results are in line with Holdich et al. (1997) who assessed growth in signal crayfish Pacifastacus leniusculus and narrow-clawed crayfish Astacus leptodactylus sensu lato at salinity of 7 ppt. Nevertheless, salinity levels higher than 14 ppt were lethal for eggs in both species. According to Casellato and Masiero (2011), red swamp crayfish reproduce at salinities up to 25 ppt, but there is a negative correlation between salinity and the number of eggs (Alcorlo et al., 2008). Newsom and Davis (1994) suggest elevated salinity as a factor causing higher growth in red swamp crayfish, due to lower energy spent on osmoregulation, which concurs with Sharfstein and Chafin (1979) suggesting salinity of 3–9 ppt as possible for culture of this species. Similarly, Australian species belonging to Parastacidae show analogous patterns where they are generally capable of growth and reproduction under saline conditions (Jones, 1989). For example, Anson and Rouse (1994) found the hatching ability of redclaw Cherax quadricarinatus to be from 1 to 20 ppt but hatching rate reduces as salinity increases. Additionally, high salinity (up to 18 ppt) reduced growth and caused lethargy of tested redclaw specimens (Jones, 1989). In comparison to the above-mentioned studies, marbled crayfish exhibited lower survival, growth and no reproduction even in the lowest salinity (6 ppt). Furthermore, increasing salinity contributed to high direct mortality during moulting. It is likely that osmotic stress negatively influenced moulting for which Na+ and Cl− are particularly important (Wheatly and Gannon, 1995; Bissattini et al., 2015). The imbalance in ions composition, in particular, might have altered osmoregulation, resulting in a high mortality rate during moulting in our experiment. Nevertheless, it should be taken into account that all mentioned studies had different acclimation periods at each salinity level or used different methods of salt addition (gradual application vs. salt shock) and maintenance making possible comparisons among studies very difficult and highly context dependent.
Currently, marbled crayfish is considered a possible result of either hybridization between slough crayfish Procambarus fallax and other species of the genus Procambarus, or rather of autopolyploid origin (Martin et al., 2016). It is usually regarded as P. fallax (Hagen, 1870) f. virginalis (Martin et al., 2010). However, Vogt et al. (2015) suggest elevation of marbled crayfish to the species level. Slough crayfish and Everglades crayfish Procambarus alleni are North American species with a distribution centre in Florida, USA (Taylor et al., 2007). They are probably the closest relatives to marbled crayfish (Martin et al., 2016). Sometimes they live in sympatry in fresh waters (Hendrix and Loftus, 2000; Martin et al., 2010), but it seems that salinity is an important factor in the separation of these two species in brackish conditions (Hendrix and Loftus, 2000). Everglades crayfish can inhabit saline environments in a range of 0–18 ppt (Hendrix and Loftus, 2000), but we are not aware of any study evaluating salinity tolerance in slough crayfish. Considering the relationship of marbled crayfish with the later may partly explains its low salinity tolerance. We found no differences in survival among salinities. It seems that long-term establishment in saline environments such as estuaries or coastal areas are not possible for marbled crayfish. Nevertheless, the ability to withstand saline environments at least for more than 80 days suggests that the species might inhabit watersheds in the vicinity and gradually adapt to more saline conditions using brackish waters as a biological corridor. This might promote its spread to coastal areas and estuaries and then colonisation of different river basins. Also, different water compositions could either reduce or enhance physiological or survival conditions of marbled crayfish, depending on pH, and cations and anions composition (Frey, 1993; Bailey and James, 2000). Furthermore, the short generation time of marbled crayfish might promote its quick adaptation to local conditions. Nevertheless, taking our experimental design as a whole (duration of adaptation and own experiment, numbers and size class of crayfish and salinity values used, etc.), further research is needed since salinity stress and salinity fluctuations may be amplified by other environmental conditions such as temperature, oxygen, and pH (Gilles and Pequeux, 1983).
Marbled crayfish is a successful invader with high ecological plasticity, capable of colonizing new habitats (Martin, 2015). We provide first insights into salinity tolerance of marbled crayfish. To sum up, marbled crayfish are probably unable to invade saline ecosystems due to their low survival, reduced growth and prevented reproduction. However, acclimation to natural conditions might lead to higher salinity tolerance due to the broader range of ions which are regulated by different pathways. Even so, its long-term survival in saline conditions has been proved. This might enable its spread in saline ecosystems, which in addition to their short generation time, could potentially lead to its local adaptation in the future.
This study was supported by the Ministry of Education, Youth, and Sports of the Czech Republic (projects CENAKVA – CZ.1.05/2.1.00/01.0024 and CENAKVA II – LO1205 under the NPU I program) and the Grant Agency of the University of South Bohemia (012/2016/Z). We thank Ingrid Steenbergen for language editing. We appreciate constructive criticism of Zen Faulkes and a reviewer that stayed anonymous.
- Alcorlo P, Geiger W, Otero M. 2008. Reproductive biology and life cycle of the invasive crayfish Procambarus clarkii (Crustacea: Decapoda) in diverse aquatic habitats of South-Western Spain: implications for population control. Fundam Appl Limnol 173: 197–212. [CrossRef] [Google Scholar]
- Anger K. 2003. Salinity as a key parameter in the larval biology of decapod crustaceans. Invertebr Reprod Dev 43: 29–45. [CrossRef] [Google Scholar]
- Anson KJ, Rouse DB. 1994. Effects of salinity on hatching and post-hatch survival of the Australian red claw crayfish Cherax quadricarinatus. J World Aquacult Soc 25: 277–280. [CrossRef] [Google Scholar]
- Bailey PC, James K. 2000. Riverine & wetland salinity impacts − assessment of R&D needs. [Google Scholar]
- Ball M. 1998. Mangrove species richness in relation to salinity and waterlogging: a case study along the Adelaide River floodplain, Northern Australia. Glob Ecol Biogeogr Lett 7: 73–82. [CrossRef] [Google Scholar]
- Bissattini AM, Traversetti L, Bellavia G, Scalici, M. 2015. Tolerance of increasing water salinity in the red swamp crayfish Procambarus clarkii (Girard, 1852). J Crustacean Biol 35: 682–685. [CrossRef] [Google Scholar]
- Berdnikov S, Selyutin V, Vasilchenko V, Caddy J. 1999. Trophodynamic model of the Black and Azov Sea pelagic ecosystem: consequences of the comb jelly, Mnemiopsis leydei, invasion. Fish Res 42:261–289. [CrossRef] [Google Scholar]
- Buřič M, Kozák P, Vích P. 2008. Evaluation of different marking methods for spiny-cheek crayfish (Orconectes limosus). Knowl Manag Aquat Ecosyst 389: 02. [Google Scholar]
- Casellato S, Masiero L. 2011. Does Procambarus clarkii (Girard, 1852) represent a threat for estuarine brackish ecosystems of Northeastern Adriatic Coast (Italy)? Life Sci J 5: 549–554. [Google Scholar]
- Chucholl C. 2013. Feeding ecology and ecological impact of an alien ‘warm-water' omnivore in cold lakes. Limnologica 43: 219–229. [CrossRef] [Google Scholar]
- Cohen AN, Carlton JT. 1998. Accelerating invasion rate in a highly invaded estuary. Science 279: 555–558. [CrossRef] [PubMed] [Google Scholar]
- Costa-Dias S, Freitas V, Sousa R, Antunes C. 2010. Factors influencing epibenthic assemblages in the Minho estuary (NW Iberian Peninsula). Mar Pollut Bull 61: 240–246. [CrossRef] [PubMed] [Google Scholar]
- Croghan P. 1976. Ionic and osmotic regulation of aquatic animals. In: Bligh J, Cloudsley-Thompson JL, MacDonald AG, eds. Environmental physiology of animals. Oxford: Blackwell, pp. 59–94. [Google Scholar]
- Frey, DG. 1993. The penetration of cladocerans into saline waters. Hydrobiologia 267: 233–248. [CrossRef] [Google Scholar]
- Gilles R, Pequeux A. 1983. Interactions of chemical and osmotic regulation with the environment. In: Vemberg FJ, Vemberg WB, eds. The biology of the Crustacea: environmental adaptations. New York: Academic Press, pp. 109–177. [Google Scholar]
- Gonçalves A, Castro B, Pardal M, Gonçalves F. 2007. Salinity effects on survival and life history of two freshwater cladocerans (Daphnia magna and Daphnia longispina). Ann Limnol: Int J Lim 43: 13–20. [CrossRef] [EDP Sciences] [Google Scholar]
- Grosholz E. 2002. Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17: 22–27. [CrossRef] [Google Scholar]
- Guan R-Z, Wiles PR. 1999. Growth and reproduction of the introduced crayfish Pacifastacus leniusculus in a British lowland river. Fish Res 42: 245–259. [CrossRef] [Google Scholar]
- Hart BT, Bailey P, Edwards R, et al. 1991. A review of the salt sensitivity of the Australian freshwater biota. Hydrobiologia 210: 105–144. [CrossRef] [Google Scholar]
- Hendrix A, Loftus W. 2000. Distribution and relative abundance of the crayfishes Procambarus alleni (Faxon) and P. fallax (Hagen) in southern Florida. Wetlands 20: 194–199. [CrossRef] [Google Scholar]
- Heugens EH, Hendriks AJ, Dekker T, Straalen NMv, Admiraal W. 2001. A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Crit Rev Toxicol 31: 247–284. [CrossRef] [PubMed] [Google Scholar]
- Holdich D, Harlioğlu M, Firkins I. 1997. Salinity adaptations of crayfish in British waters with particular reference to Austropotamobius pallipes, Astacus leptodactylus and Pacifastacus leniusculus. Estuar Coast Shelf Sci 44: 147–154. [CrossRef] [Google Scholar]
- Holdich D, Reynolds J, Souty-Grosset C, Sibley P. 2009. A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowl Manag Aquat Ecosyst 394–395: 11. [CrossRef] [EDP Sciences] [Google Scholar]
- Jaszczołt J, Szaniawska A. 2011. The spiny-cheek crayfish Orconectes limosus (Rafinesque, 1817) as an inhabitant of the Baltic Sea — experimental evidences for its invasion of brackish waters. Oceanol Hydrobiol Stud 40: 52–60. [Google Scholar]
- Jazdzewski K, Konopacka A. 2002. Invasive Ponto-Caspian species in waters of the Vistula and Oder basins and the southern Baltic Sea. In: Leppäkoski E, Gollasch S, Olenin S, eds. Invasive aquatic species of Europe. Distribution, impacts and management. Berlin: Springer, pp. 384–398. [CrossRef] [Google Scholar]
- Jones CM. 1989. The biology and aquaculture potential of Cherax quadricarinatus. Final report submitted by the Queensland Department of Primary Industries to the Reserve Bank of Australia Rural Credits Development Project No. QDPI/8860, pp. 1–116. [Google Scholar]
- Keller N, Pfeiffer M, Roessink I, Schulz R, Schrimpf A. 2014. First evidence of crayfish plague agent in populations of the marbled crayfish (Procambarus fallax forma virginalis). Knowl Manag Aquat Ecosyst 414: 15. [CrossRef] [EDP Sciences] [Google Scholar]
- Kornis M, Mercado-Silva N, Vander Zanden M. 2012. Twenty years of invasion: a review of round goby Neogobius melanostomus biology, spread and ecological implications. J Fish Biol 80: 235–285. [CrossRef] [PubMed] [Google Scholar]
- Kotovska G, Khrystenko D, Patoka J, Kouba A. 2016. East European crayfish stocks at risk: arrival of non-indigenous crayfish species. Knowl Manag Aquat Ecosyst 417: 37. [CrossRef] [EDP Sciences] [Google Scholar]
- Kouba A, Petrusek A, Kozák P. 2014. Continental-wide distribution of crayfish species in Europe: update and maps. Knowl Manag Aquat Ecosyst 414: 05. [CrossRef] [EDP Sciences] [Google Scholar]
- Kouba A, Tíkal J, Císař P, et al. 2016. The significance of droughts for hyporheic dwellers: evidence from freshwater crayfish. Sci Rep 6: 26569. [CrossRef] [PubMed] [Google Scholar]
- Leppäkoski E, Olenin S. 2000. Non-native species and rates of spread: lessons from the brackish Baltic Sea. Biol Invasions 2: 151–163. [CrossRef] [Google Scholar]
- Lipták B, Mrugała A, Pekárik L, et al. 2016. Expansion of the marbled crayfish in Slovakia: beginning of an invasion in the Danube catchment? J Limnol 75: 305–312. [Google Scholar]
- Lodge DM, Taylor CA, Holdich DM, Skurdal J. 2000. Nonindigenous crayfishes threaten North American freshwater biodiversity: lessons from Europe. Fisheries 25: 7–20. [CrossRef] [Google Scholar]
- Martin P. 2015. Reproductive biology, parthenogenesis: mechanisms, evolution, and its relevance to the role of marbled crayfish as model organism and potential invader. In: Kawai T, Faulkes Z, Scholtz G, eds. Freshwater crayfish: a global overview. New York: CRC Press, pp. 63–82. [CrossRef] [Google Scholar]
- Martin P, Dorn NJ, Kawai T, van der Heiden C, Scholtz G. 2010. The enigmatic Marmorkrebs (marbled crayfish) is the parthenogenetic form of Procambarus fallax (Hagen, 1870). Contrib Zool 79: 107–118. [Google Scholar]
- Martin P, Thonagel S, Scholtz G. 2016. The parthenogenetic Marmorkrebs (Malacostraca: Decapoda: Cambaridae) is a triploid organism. J Zool Sys Evol Res 54: 13–21. [CrossRef] [Google Scholar]
- Meineri E, Rodriguez-Perez H, Hilaire S, Mesleard F. 2014. Distribution and reproduction of Procambarus clarkii in relation to water management, salinity and habitat type in the Camargue. Aquat Conserv 24: 312–323. [CrossRef] [Google Scholar]
- Moorhouse TP, Macdonald DW. 2015. Are invasives worse in freshwater than terrestrial ecosystems? Wiley Interdiscip Rev 2: 1–8. [CrossRef] [Google Scholar]
- Mrugała A, Kozubíková-Balcarová E, Chucholl C, et al. 2014. Trade of ornamental crayfish in Europe as a possible introduction pathway for important crustacean diseases: crayfish plague and white spot syndrome. Biol Invasions 17: 1–14. [Google Scholar]
- Newsom JE, Davis KB. 1994. Osmotic responses of haemolymph in red swamp crayfish (Procambarus clarkii) and white river crayfish (P. zonangulus) to changes in temperature and salinity. Aquaculture 126: 373–381. [CrossRef] [Google Scholar]
- Nielsen D, Brock M, Rees G, Baldwin DS. 2003. Effects of increasing salinity on freshwater ecosystems in Australia. Aust J Bot 51: 655–665. [CrossRef] [Google Scholar]
- Novitsky RA, Son MO. 2016. The first records of Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] (Crustacea, Decapoda, Cambaridae) in Ukraine. Ecol Mont 5: 44–46. [Google Scholar]
- Patoka J, Kalous L, Kopecký O. 2014. Risk assessment of the crayfish pet trade based on data from the Czech Republic. Biol Invasions 16: 2489–2494. [CrossRef] [Google Scholar]
- Patoka J, Buřič M, Kolář V, et al. 2016. Predictions of marbled crayfish establishment in conurbations fulfilled: evidences from the Czech Republic. Biologia 71: 1380–1385. [CrossRef] [Google Scholar]
- Perdikaris C, Kozák P, Kouba A, Konstantinidis E, Paschos I. 2012. Socio-economic drivers and non-indigenous freshwater crayfish species in Europe. Knowl Manag Aquat Ecosyst 404: 01. [CrossRef] [EDP Sciences] [Google Scholar]
- Pourkazemi M. 2006. Caspian Sea sturgeon conservation and fisheries: past present and future. J Appl Ichthyol 22: 12–16 [CrossRef] [Google Scholar]
- R Core Team. 2016. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. URL: https://www.R-project.org/. [Google Scholar]
- Scholtz G, Braband A, Tolley L, et al. 2003. Ecology: parthenogenesis in an outsider crayfish. Nature 421: 806. [CrossRef] [PubMed] [Google Scholar]
- Seebens H, Blackburn T, Dyer E, Genovesi P, Hulme P, Jeschke J. 2017. No saturation in the accumulation of alien species worldwide. Nat Commun 8: 14435. [CrossRef] [PubMed] [Google Scholar]
- Seitz R, Vilpoux K, Hopp U, Harzsch S, Maier G. 2005. Ontogeny of the Marmorkrebs (marbled crayfish): a parthenogenetic crayfish with unknown origin and phylogenetic position. J Exp Zool A Comp Exp Biol 303: 393–405. [CrossRef] [PubMed] [Google Scholar]
- Sharfstein BA, Chafin C. 1979. Red swamp crayfish: short-term effects of salinity on survival and growth. Prog Fish Cult 41: 156–157. [CrossRef] [Google Scholar]
- Simberloff D, Martin J-L, Genovesi P, et al. 2013. Impacts of biological invasions: what's what and the way forward. Trends Ecol Evol 28: 58–66. [CrossRef] [PubMed] [Google Scholar]
- Snell T. 1986. Effect of temperature, salinity and food level on sexual and asexual reproduction in Brachionus plicatilis (Rotifera). Mar Biol 92: 157–162. [CrossRef] [Google Scholar]
- Sousa R, Dias S, Antunes C. 2006. Spatial subtidal macrobenthic distribution in relation to abiotic conditions in the Lima estuary, NW of Portugal. Hydrobiologia 559: 135–148. [CrossRef] [Google Scholar]
- Sousa R, Dias S, Antunes C. 2007. Subtidal macrobenthic structure in the lower Lima estuary, NW of Iberian Peninsula. Ann Zool Fennici 44: 303–313. [Google Scholar]
- Sousa R, Dias S, Freitas V, Antunes C. 2008. Subtidal macrozoobenthic assemblages along the River Minho estuarine gradient (north-west Iberian Peninsula). Aquat Conserv 18: 1063–1077. [CrossRef] [Google Scholar]
- Sousa R, Freitas FEP, Mota M, Nogueira AJA, Antunes C. 2013. Invasive dynamics of the crayfish Procambarus clarkii (Girard, 1852) in the international section of the River Minho (NW of the Iberian Peninsula). Aquat Conserv 23: 656–666. [Google Scholar]
- Sousa R, Novais A, Costa R, Strayer D. 2014. Invasive bivalves in fresh waters: impacts from individuals to ecosystems and possible control strategies. Hydrobiologia 735: 233–251. [CrossRef] [Google Scholar]
- Strayer DL. 2010. Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshwater Biol 55: 152–174. [CrossRef] [Google Scholar]
- Taylor CA, Schuster GA, Cooper JE, et al. 2007. A reassessment of the conservation status of crayfishes of the United States and Canada after 10+ years of increased awareness. Fisheries 32: 372–389. [CrossRef] [Google Scholar]
- Therneau MT, Grambsch MP. 2000. Modeling survival data: extending the Cox model. New York: Springer Science & Business Media. [CrossRef] [Google Scholar]
- van Ginneken VJ, Maes GE. 2005. The European eel (Anguilla anguilla, Linnaeus), its lifecycle, evolution and reproduction: a literature review. Rev Fish Biol Fish 15: 367–398. [CrossRef] [Google Scholar]
- Veselý L, Buřič M, Kouba A. 2015. Hardy exotics species in temperate zone: can “warm water” crayfish invaders establish regardless of low temperatures? Sci Rep 5: 16340. [CrossRef] [MathSciNet] [PubMed] [Google Scholar]
- Vodovsky N, Patoka J, Kouba A. 2017. Ecosystem of Caspian Sea threatened by pet-traded non-indigenous crayfish. Biol Invasions. DOI:10.1007/s10530-017-1433-1. [PubMed] [Google Scholar]
- Vogt G. 2015. Bimodal annual reproduction pattern in laboratory-reared marbled crayfish. Invertebr Rep Dev 59: 218–223. [CrossRef] [Google Scholar]
- Vogt G, Falckenhayn C, Schrimpf A, et al. 2015. The marbled crayfish as a paradigm for saltational speciation by autopolyploidy and parthenogenesis in animals. Biol Open 4: 1583–1594. [CrossRef] [PubMed] [Google Scholar]
- Wheatly MG, Gannon AT. 1995. Ion regulation in crayfish: freshwater adaptations and the problem of molting. Amer Zool 35: 49–59. [CrossRef] [Google Scholar]
Cite this article as: Veselý L, Hrbek V, Kozák P, Buřič M, Sousa R, Kouba A. 2017. Salinity tolerance of marbled crayfish Procambarus fallax f. virginalis. Knowl. Manag. Aquat. Ecosyst., 418, 21.
Growth and reproduction indices of marbled crayfish Procambarus fallax f. virginalis kept under different salinities. Growth indices presented as mean ± SD. Reproduction indices refer to number of specimens. Values with differing superscripts in given column are significantly different (one-way ANOVA, Tukey's HSD test, p < 0.05).
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