Spiny-cheek crayfish Orconectes limosus carry a novel genotype of the crayfish plague pathogen Aphanomyces astaci

The oomycete Aphanomyces astaci causes mass mortalities of European crayfish. Different species of North American crayfish, original hosts of this parasite, seem to carry different strains of A. astaci. So far, four distinct genotype groups have been recognised using Random Amplification of Polymorphic DNA (RAPD-PCR). We succeeded in isolating A. astaci from the spiny-cheek crayfish Orconectes limosus, a widespread invader in Europe, and confirmed that this species carries a novel A. astaci genotype. Improving knowledge on the diversity of this parasite may facilitate identification of genotypes in mass mortalities of European crayfish, thus tracing the sources of infection.     

The crayfish plague pathogen can infect freshwater‐inhabiting crabs

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Prevalence of the Crayfish Plague Pathogen Aphanomyces astaci in Populations of the Signal Crayfish Pacifastacus leniusculus in France: Evaluating the Threat to Native Crayfish

Aphanomyces astaci, the crayfish plague pathogen, first appeared in Europe in the mid-19^th century and is still responsible for mass mortalities of native European crayfish. The spread of this parasite across the continent is especially facilitated by invasive North American crayfish species that serve as its reservoir. In France, multiple cases of native crayfish mortalities have been suggested to be connected with the presence of the signal crayfish Pacifastacus leniusculus, which is highly abundant in the country. It shares similar habitats as the native white-clawed crayfish Austropotamobius pallipes and, when infected, the signal crayfish might therefore easily transmit the pathogen to the native species. We investigated the prevalence of A. astaci in French signal crayfish populations to evaluate the danger they represent to local populations of native crayfish. Over 500 individuals of Pacifastacus leniusculus from 45 French populations were analysed, plus several additional individuals of other non-indigenous crayfish species Orconectes limosus, O. immunis and Procambarus clarkii. Altogether, 20% of analysed signal crayfish tested positive for Aphanomyces astaci, and the pathogen was detected in more than half of the studied populations. Local prevalence varied significantly, ranging from 0% up to 80%, but wide confidence intervals suggest that the number of populations infected by A. astaci may be even higher than our results show. Analysis of several individuals of other introduced species revealed infections among two of these, O. immunis and P. clarkii. Our results confirm that the widespread signal crayfish serves as a key reservoir of Aphanomyces astaci in France and therefore represents a serious danger to native crayfish species, especially the white-clawed crayfish. The prevalence in other non-indigenous crayfish should also be investigated as they likely contribute to pathogen transmission in the country.     

The North American crayfish <Emphasis Type="Italic">Procambarus clarkii</Emphasis> is the carrier of the oomycete <Emphasis Type="Italic">Aphanomyces astaci</Emphasis> in Italy

Aphanomyces astaci (Saprolegniales, Oomycetes) is classified among the 100 world’s worst invasive species. This species is endemic to North America and has been introduced into Europe by imports of their hosts, the North American crayfish species. As a consequence, extensive mass mortalities involved several populations of the European crayfish. Here, we checked its occurrence in four Italian populations of Procambarus clarkii, the most widespread alien crayfish in Italy. Digital image analyses and image processing techniques were used to select micro-melanized areas in the subabdominal cuticle of 2–10 crayfish per population. All the selected areas tested positive for A. astaci ITS nrDNA specific primers; moreover, the obtained sequences clearly corresponded to A. astaci, thus revealing that P. clarkii is an active carrier of this oomycete in Italy. Decisions are to be urgently made to control the spread of both P. clarkii and A. astaci for the conservation of the indigenous crayfish biodiversity.     

First records of the non-indigenous signal crayfish (<Emphasis Type="Italic">Pacifastacus leniusculus</Emphasis>) and its threat to noble crayfish (<Emphasis Type="Italic">Astacus astacus</Emphasis>) populations in Estonia

This study gives an overview of status and distribution of signal crayfish (Pacifastacus leniusculus), the first NICS in Estonia and its influence on native noble crayfish (Astacus astacus) populations. The first specimen of signal crayfish was caught during the monitoring of noble crayfish in North Estonia in 2008. The signal crayfish has since been found in three additional sites. Test fishing has indicated that the abundance of signal crayfish has been fluctuating between years and among localities. It has had strong negative impact on abundance of one noble crayfish population. The disconnected distribution of signal crayfish strongly suggests that these populations are the result of human-assisted introductions. Real-time PCR analyses proved that signal crayfish carry the causative agent of the crayfish plague, an oomycete Aphanomyces astaci, thus contributing to its spread. Mortalities in noble crayfish populations had been caused by A. astaci strains from A, B and E genotype group.     

Phylogeography of noble crayfish (Astacus astacus) reveals multiple refugia

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Identification of two GH18 chitinase family genes and their use as targets for detection of the crayfish-plague oomycete Aphanomyces astaci

Background  

The oomycete Aphanomyces astaci is regarded as the causative agent of crayfish plague and represents an evident hazard for European crayfish species. Native crayfish populations infected with this pathogen suffer up to 100% mortality. The existence of multiple transmission paths necessitates the development of a reliable, robust and efficient test to detect the pathogen. Currently, A. astaci is diagnosed by a PCR-based assay that suffers from cross-reactivity to other species. We developed an alternative closed-tube assay for A. astaci, which achieves robustness through simultaneous amplification of multiple functionally constrained genes.     

Threat of non-native crayfish introductions into Turkey: global lessons

Introductions of crayfish species from their home range to new environments have been carried out in many parts of the world. The most important introduced crayfish species are Procambarus clarkii, Pacifastacus leniusculus, Cherax destructor, C. quadricarinatus, Orconectes limosus, O. rusticus and Astacus leptodactylus. The environmental impact of crayfish introductions can be positive, negative or neutral. However, native crayfish populations in Europe have been negatively affected by introductions of non-indigenous crayfish species from America. Negative effects of non-native crayfish introductions included displacement of native crayfish species, transfer of disease (crayfish plague), consumption of fish eggs, reduction of fish stocks, consumption of large amounts of macrophytes, indirect and direct effects on other invertebrates and upsetting production in rice fields. As a result of non-native crayfish introductions, the natural harvest and crayfish industry in Europe have been severely affected. Large quantities of Turkish A. leptodactylus were harvested (approximately 7,000 tonnes annually) and exported to Europe before the crayfish plague was observed in these populations. The total harvest of A. leptodactylus in Turkey reduced dramatically to 320 in 1991 after the plague. Therefore, although Turkey currently has no known non-native crayfish species, there is a threat of non-native crayfish introduction in order to increase crayfish productions and subsequent harvest. The North American spiny-cheek crayfish, O. limosus, has been spreading quickly down the River Danube and could soon reach neighboring countries including Turkey. The North American signal crayfish, P. leniusculus is known from Greece and could be a threat to native stocks if it is introduced into Turkey for aquaculture. Additional threats may come from the release of other North American species, which are widely available through the aquarium trade. We conclude that the spread of non-native crayfish introductions throughout Turkey will increase local problems, because introductions of non-native crayfish in many parts of the world have been known to have caused important reductions in population density and numbers of native crayfish species. Furthermore, freshwater ecosystems may be altered by such introductions and the economic viability of native crayfish species fisheries could be severely reduced in Turkey.     

AFLP-PCR and RAPD-PCR evidences of the transmission of the pathogen Aphanomyces astaci (Oomycetes) to wild populations of European crayfish from the invasive crayfish species, Procambarus clarkii

Aphanomyces astaci (Oomycetes) is responsible for the crayfish plague disease. This species is endemic of North America and five genotypes have been described using RAPD-PCR. The red swamp crayfish, Procambarus clarkii, is one of the most widely spread North American species and invasive in the world. However, no outbreaks on its specific genotype, i.e., genotype D, have ever been described in nature. We investigated three major series of crayfish plague outbreaks in indigenous crayfish populations of Austropotamobius pallipes, located in the areas of influence of P. clarkii. All samples collected tested positive for A. astaci using a rnDNA ITS-PCR test. We also performed an AFLP-PCR analysis on 19 isolates, and found that all isolates belong to genotype D. These isolates exhibited similar properties, i.e., adaptation to warm temperatures. We demonstrate, for the first time, the transmission of A. astaci genotype D to indigenous European populations of crayfish, and confirm that the properties of adaptation to warm water temperatures seem to be a specific character of genotype D. The results of this work emphasize once more the need of controlling invasive species and its trade, since they can carry harmful pathogens with specific adaptations or increased virulence in new environments.     

Non-indigenous signal crayfish <Emphasis Type="Italic">Pacifastacus leniusculus</Emphasis> are now common in Danish streams: preliminary status for national distribution and protective actions

North American signal crayfish (Pacifastacus leniusculus) are invasive in Europe and pose a serious threat to indigenous European crayfish such as the noble crayfish (Astacus astacus). This is mainly because signal crayfish is the carrier of crayfish plague agent, Aphanomyces astaci, which freshwater crayfish from all other continents are highly susceptible to. Until recently, the distribution of signal crayfish in Danish streams has been considered local and restricted to a small geographical area. Here we present data demonstrating that signal crayfish are now widespread in Denmark, including the largest Danish river, River Gudenå. For one of the rivers where co-existing signal crayfish and indigenous noble crayfish were documented, sensitive molecular tests could not detect the crayfish plague agent Aphanomyces astaci in either species. Hence, it seems that not all signal crayfish are chronic carriers of the disease. For the remaining freshwater systems with the introduced signal crayfish, the infection status is presently unknown. Large areas of the freshwater systems in Denmark also remain unexplored with respect to presence/absence of signal crayfish and noble crayfish. Nevertheless, our preliminary data that covers about 14% of the Danish rivers, strongly suggests that signal crayfish should be considered as a common invader that poses an increased threat to the biota in Danish streams, in particular for the indigenous noble crayfish.     

An invasive species may be better than none: invasive signal and native noble crayfish have similar community effects

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The introduced signal crayfish and native noble crayfish have different effects on sublittoral macroinvertebrate assemblages in boreal lakes

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Associations between stream habitat characteristics and native and alien crayfish occurrence

Human mediated introductions of non-indigenous crayfish species (NICS) are responsible for their rapid colonisation of European freshwaters. The introduction of North American crayfish is furthermore linked to the spread of crayfish plague and the decline of indigenous crayfish species (ICS). As the management of ICS and NICS have become necessary, a detailed knowledge on their distribution and ecological requirements is needed. We studied the current range of native noble crayfish Astacus astacus and stone crayfish Austropotamobius torrentium, as well as alien signal crayfish Pacifastacus leniusculus in Carinthia (Austria) and evaluated environmental and physical habitat features in streams with and without crayfish. Meanwhile, the loss of many ICS populations was recorded and alien P. leniusculus was found to be widespread in this region. Most of the habitat features of streams having crayfish differed significantly from sites lacking crayfish for at least one investigated native or alien species. Furthermore, multivariate and regression analyses showed specific differences in the habitat use of the investigated crayfish. Our results showed that the presence of alien P. leniusculus was associated with larger and smoother sloped lowland rivers, while the occurrence of the two native species was confined to smaller streams either at higher altitudes and with distinct physical habitat conditions (A. torrentium) or with moderate water temperatures (A. astacus). This study helps to identify potential refuge areas for the endangered native species and to predict the further spread of the most common non-native crayfish species in European streams.     

The first record of the non-indigenous signal crayfish <Emphasis Type="Italic">Pasifastacus leniusculus</Emphasis> in Norway

The non-indigenous signal crayfish Pasifastacus leniusculus was registered for the first time in Norway in October 2006. The location represents an isolated pond about 100 km in air line from the nearest known signal crayfish population in the neighbouring country Sweden without any connecting watercourses. The occurrence is therefore undoubtedly caused by human introduction. Molecular analyses confirmed that tested individuals from the signal crayfish population were carriers of the crayfish plague agent Aphanomyces astaci. Disease carrying signal crayfish represents a severe threat to the indigenous and endangered noble crayfish Astacus astacus. Norwegian authorities are currently considering actions for the eradication of the signal crayfish population.     

Population collapses in introduced non-indigenous crayfish

Invasive species often have instable population dynamics and are known to collapse or oscillate heavily after passing through the initial lag/growth phases. Long-term data-series documenting these fluctuations are however rare. We use long-term (starting in the early 1960s), semi-quantitative data on the invasive signal crayfish (Pacifastacus leniusculus), capturing its population development after introduction in 44 Swedish lakes. In total 18 (41 %) of these populations had experienced a collapse. A stepwise discriminant function analysis including 20 different ecological or physicochemical characteristics identified three variables explaining collapses in the following order: stocking year, population age and mean air temperature. Populations stocked in the 1980s were more likely to collapse than populations stocked in the 1970s. Lakes with collapses were located in areas with 0.4 °C higher yearly mean air temperatures than the still viable populations. Collapses also depended on the time phase of the population and started to occur 12 years after stocking and were most frequent in the interval 16–20 years after stocking and after 11–15 years duration of the established phase with harvestable densities. An analysis of prevalence and pathogen load of Aphanomyces astaci was conducted in eight of the studied populations. A. astaci was present in all populations but neither the level of prevalence nor the pathogen load in infested specimens differed significantly between lakes with collapses and lakes without. Our results highlight the potential sensitivity and instability of introduced crayfish. The importance of density-dependence and temperature suggest that both climate variability and/or fisheries can influence these processes.     

The diversity of oomycetes on crayfish: Morphological vs. molecular identification of cultures obtained while isolating the crayfish plague pathogen

Numerous oomycetes colonise the crayfish cuticle, the best known being the crayfish plague pathogen Aphanomyces astaci. Although other oomycetes associated with crayfish complicate the isolation and molecular detection of A. astaci, their diversity is little known. To improve this knowledge, we analysed 95 oomycete isolates obtained during attempts to isolate A. astaci from crayfish presumably infected by this pathogen. We characterized the isolates morphologically and by sequencing of the nuclear internal transcribed spacer (ITS) region. We identified 13 taxa by molecular analysis. Ten of them were assigned to five genera; the remaining three were affiliated with the order Saprolegniales but could not be reliably assigned to any genus. Morphological identification to species level was only possible for 15 % of isolates; all corresponded to Saprolegnia ferax, which was confirmed by ITS sequencing. The most frequently isolated species were S. ferax and Saprolegnia australis. Only seven isolates of A. astaci were obtained, all from one disease outbreak. We show that oomycete cultures obtained as by-products of parasite isolation are valuable for oomycete diversity studies, but morphological identification may uncover only a fraction of their diversity. Further, we show that crayfish may be frequently associated with potentially serious parasites of other organisms.     

Species-specific differences in dynamics of agonistic interactions may contribute to the competitive advantage of the invasive signal crayfish (Pacifastacus leniusculus) over the native narrow-clawed crayfish (Astacus leptodactylus)

Species-specific differences in dynamics of agonistic interactions may influence the outcome of interspecific competition and potentially contribute to competitive advantage of one species over another. In this study, we compared the dynamics of agonistic interactions of one of the most successful crayfish invaders of European freshwater ecosystems, the signal crayfish (Pacifastacus leniusculus) and the widespread native European species currently undergoing range expansion in Croatia and Europe, the narrow-clawed crayfish (Astacus leptodactylus). Comparisons between P. leniusculus pairs and the A. leptodactylus pairs demonstrated significant differences in frequency and duration of agonistic encounters: P. leniusculus dyads engaged in fewer fights, but their duration was significantly longer. In staged interactions between size-matched interspecific pairs, agonistic behaviour of P. leniusculus individuals translated into dominance over their A. leptodactylus counterparts. This indicates that the success of P. leniusculus in agonistic encounters with the native competitor might stem from its readiness to continue fighting for a longer time period, and could lead to ecological advantages during niche competition even when facing a successful native crayfish species.     

Reprint of: The diversity of oomycetes on crayfish: Morphological vs. molecular identification of cultures obtained while isolating the crayfish plague pathogen

Numerous oomycetes colonise the crayfish cuticle, the best known being the crayfish plague pathogen Aphanomyces astaci. Although other oomycetes associated with crayfish complicate the isolation and molecular detection of A. astaci, their diversity is little known. To improve this knowledge, we analysed 95 oomycete isolates obtained during attempts to isolate A. astaci from crayfish presumably infected by this pathogen. We characterized the isolates morphologically and by sequencing of the nuclear internal transcribed spacer (ITS) region. We identified 13 taxa by molecular analysis. Ten of them were assigned to five genera; the remaining three were affiliated with the order Saprolegniales but could not be reliably assigned to any genus. Morphological identification to species level was only possible for 15 % of isolates; all corresponded to Saprolegnia ferax, which was confirmed by ITS sequencing. The most frequently isolated species were S. ferax and Saprolegnia australis. Only seven isolates of A. astaci were obtained, all from one disease outbreak. We show that oomycete cultures obtained as by-products of parasite isolation are valuable for oomycete diversity studies, but morphological identification may uncover only a fraction of their diversity. Further, we show that crayfish may be frequently associated with potentially serious parasites of other organisms.     

Non‐lethal predator effects on the performance of a native and an exotic crayfish species

1. I tested the hypothesis that the potential for non‐lethal effects of predators are more important for overall performance of the fast‐growing exotic signal crayfish (Pacifastacus leniusculus Dana) than for the slower growing native noble crayfish (Astacus astacus L.). I further tested if omnivorous crayfish switched to feed on less risky food sources in the presence of predators, a behaviour that could reduce the feeding costs associated with predator avoidance. 2. In a 2 month long outdoor pool experiment, I measured behaviour, survival, cheliped loss, growth, and food consumption in juvenile noble or signal crayfish in pools with either a caged predatory dragonfly larvae (Aeshna sp.), a planktivorous fish that do not feed on crayfish (sunbleak, Leucaspius delineatus Heckel), or predator‐free controls. Crayfish had access to multiple food sources: live zooplankton, detritus and periphyton. Frozen chironomid larvae were also supplied ad libitum outside crayfish refuges, simulating food in a risky habitat. 3. Crayfish were mainly active during hours of darkness, with signal crayfish spending significantly more time outside refuges than noble crayfish. The proportion of crayfish outside refuges varied between crayfish species, time and predator treatment, with signal crayfish spending more time in refuges at night in the presence of fish. 4. Survival in noble crayfish was higher than in signal crayfish, and signal crayfish had a higher frequency of lost chelipeds, indicating a high level of intraspecific interactions. Crayfish survival was not affected by the presence of predators. 5. Gut‐contents analysis and stable isotope values of carbon (δ¹³C) and nitrogen (δ¹⁵N) indicated that the two crayfish species had similar food preferences, and that crayfish received most of their energy from feeding on invertebrates (e.g. chironomid larvae), although detritus was the most frequent food item in their guts. Signal crayfish guts were more full than those of noble crayfish, but signal crayfish in pools with fish contained significantly less food and fewer had consumed chironomids compared with predator‐free controls. Length increase of signal crayfish (35%) was significantly higher than of noble crayfish (20%), but signal crayfish in pools with fish grew less than in control pools. 6. This short‐term study indicates that fish species that do not pose a lethal threat to an organism may indirectly cause reductions in growth by affecting behaviour and feeding. This may occur even though prey are omnivorous and have access to and consume multiple food sources. These non‐lethal effects of predators are expected to be particularly important in exotic crayfish species that show a general response to fish, have high individual growth rates, and when their feeding on the most profitable food source is reduced.     

Invasive crayfish and crayfish plague on the move: first detection of the plague agent Aphanomyces astaci in the Romanian Danube

Native European crayfish, such as Astacus leptodactylus, are threatened, among other factors, by the crayfish plague agent Aphanomyces astaci, dispersed by invasive North American crayfish. Two of these invaders, Pacifastacus leniusculus and Orconectes limosus, have extended their distribution in the River Danube catchment; the latter was detected for the first time in Romania in 2008. We monitored, at monthly intervals for over 2 yr, occurrence of native A. leptodactylus and invasive O. limosus at 6 sites on the Romanian Danube and checked for the invasive species in 4 of its tributaries. Between January 2009 and March 2011, the relative abundances of O. limosus steadily increased with time, while the native A. leptodactylus dramatically decreased in abundance. O. limosus expanded downstream at a rate of ca. 15 km yr-1; in August 2011, it was already present in the upper 105 km of the Romanian Danube. An agent-specific real-time PCR analyses demonstrated the presence of A. astaci DNA in at least 32% of the analysed invasive (n = 71) and 41% of the native (n = 49) crayfish coexisting in the Danube. Furthermore, A. astaci was also detected in A. leptodactylus captured about 70 km downstream of the O. limosus invasion front (at the time of sampling). Assuming a steady rate of expansion, O. limosus may invade the sensitive Danube delta area in the mid-2060s, even without long-distance dispersal. The crayfish plague agent, however, may reach the delta substantially earlier, through dispersal downstream among populations of native crayfish.