Competition and parasitism in the native White Clawed Crayfish Austropotamobius pallipes and the invasive Signal Crayfish Pacifastacus leniusculus in the UK

Many crayfish species have been introduced to novel habitats worldwide, often threatening extinction of native species. Here we investigate competitive interactions and parasite infections in the native Austropotamobius pallipes and the invasive Pacifastacus leniusculus from single and mixed species populations in the UK. We found A. pallipes individuals to be significantly smaller in mixed compared to single species populations; conversely P. leniusculus individuals were larger in mixed than in single species populations. Our data provide no support for reproductive interference as a mechanism of competitive displacement and instead suggest competitive exclusion of A. pallipes from refuges by P. leniusculus leading to differential predation. We screened 52 P. leniusculus and 12 A. pallipes for microsporidian infection using PCR. We present the first molecular confirmation of Thelohania contejeani in the native A. pallipes; in addition, we provide the first evidence for T. contejeani in the invasive P. leniusculus. Three novel parasite sequences were also isolated from P. leniusculus with an overall prevalence of microsporidian infection of 38% within this species; we discuss the identity of and the similarity between these three novel sequences. We also screened a subset of fifteen P. leniusculus and three A. pallipes for Aphanomyces astaci, the causative agent of crayfish plague and for the protistan crayfish parasite Psorospermium haeckeli. We found no evidence for infection by either agent in any of the crayfish screened. The high prevalence of microsporidian parasites and occurrence of shared T. contejeani infection lead us to propose that future studies should consider the impact of these parasites on native and invasive host fitness and their potential effects upon the dynamics of native-invader systems.     

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.     

Diatoms prefer strangers: non-indigenous crayfish host completely different epizoic algal diatom communities from sympatric native species

Despite their wide distribution and ecological importance, almost no information is available about the role of freshwater crayfish as basibiont for epizoic algae. Moreover, studies on epizoic freshwater diatoms have been largely neglected. In this study, we examined the occurrence of diatoms on two sympatric species, the native white-clawed crayfish Austropotamobius pallipes and the non-indigenous signal crayfish Pacifastacus leniusculus, coexisting in the same stream in NW Italy. We detected that signal crayfish showed a far more productive epizoic algal community than white-clawed crayfish. Microscopical analysis confirmed that non-indigenous crayfish hosted rich and diversified diatom communities while virtually no diatom was found on the native. After analyzing different hypotheses, we suggested that this significant difference can be the result of diverse crayfish behavioral habits. Because of the lack of studies investigating epibiontic diatoms on freshwater crayfish, we performed a detailed characterization on the epizoic flora, including comparisons with natural epilithic communities. The exponential diffusion of non-indigenous freshwater crayfish is a subject of greatest interest. Increasing our knowledge on their role as basibionts is definitely necessary to better understand their ecological role, also considering their influence on primary producer community and their role as vectors of algal species of concern, such as Didymosphenia geminata.     

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.     

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.     

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.     

Invasive American crayfish <Emphasis Type="Italic">Pacifastacus leniusculus</Emphasis> (Decapoda: Astacidae) in the Morava River (Slovakia)

The signal crayfish, Pacifastacus leniusculus (Dana, 1852), was recorded in the Slovak-Austrian stretch of the Morava (March) River in the Záhorie region in August 2006. This is the first confirmed record of a non-indigenous crayfish species of American origin in Slovakia. Most likely, signal crayfish were intentionally released to the river by Austrian fishermen, or invaded from adjacent water bodies in Austria. As this species has a substantial invasive capability and is a potential vector of the crayfish plague pathogen, it represents a threat to the native crayfish species and its spread should be monitored. Its invasion upstream to the territory of the Czech Republic is not unlikely in near future.     

Muddied waters: suspended sediment impacts on gill structure and aerobic scope in an endangered native and an invasive freshwater crayfish

Suspended sediment (SS) loadings in freshwater habitats have increased over the past century and SS is now a significant environmental stressor. Greater tolerance to environmental stressors has been proposed as a factor in the success of aquatic invasive species. Further, parasites may interact with environmental stressors to increase host susceptibility to loss of fitness and mortality. We compared the effects of SS exposure on the gill structure and aerobic scope of the endangered white-clawed crayfish (Austropotamobius pallipes), and the invasive signal crayfish (Pacifastacus leniusculus), and assessed impacts in relation to parasite burden. SS caused gill fouling and reduction in aerobic scope in both species, though A. pallipes was more susceptible than invasive P. leniusculus. The parasite Branchiobdella astaci, a crayfish worm that infests the gills, interacted with the sediment to affect gill structure whereas infection with the microsporidian parasite Thelohania contejeani had no effect on crayfish response to SS. Juvenile P. lenisuculus had a higher standard metabolic rate than A. pallipes, which may be linked to competitive advantages such as higher growth rate and behavioural dominance. Conservation of A. pallipes often involves relocation of threatened populations to isolated stillwaters; our findings suggest that SS levels should be assessed before relocation.     

Phoma glomerata, a potential new threat to Italian inland waters

Non-indigenous crayfish species, carrier of the oomycete Aphanomyces astaci, are the most important threats to European crayfish species. However, other ectoparasite species have been reported to be the pathogen of aquatic organisms. As little is known about other potential pathogens carried by the red swamp crayfish Procambarus clarkii, a total of 86 individuals of this species was collected in Lake Trasimeno from June 2007 to 2008. Phoma glomerata, never recorded in Italy, colonised more than 65% of the captured crayfish. No significant differences in prevalence were recorded between sexes, among life stages and between soft- and hard-shelled crayfish. This Coelomycetes is the causal agent of many diseases in plants, animals and humans. These results may contribute to a better understanding of the implications of epibiontic microfungi on the invasive crayfish P. clarkii, for both ecological and sanitary purposes.     

Absence of the crayfish plague pathogen (Aphanomyces astaci) facilitates coexistence of European and American crayfish in central Europe

1. Most European crayfish species are strongly threatened, mainly as a result of the introduced pathogen, Aphanomyces astaci, transmitted by invasive North American crayfish. Long‐term coexistence of American and European crayfish species is therefore regarded as almost impossible, even though some coexisting populations have been observed. 2. In this study, crayfish were collected from presently coexisting populations of the introduced spiny‐cheek crayfish (Orconectes limosus) and the native noble crayfish (Astacus astacus) from nine standing waters in central Europe. Our aim was to resolve whether the coexistence resulted from reduced virulence in local strains of A. astaci, increased immunity in the native crayfish or an absence of the pathogen in these populations. We used highly sensitive A. astaci‐specific real‐time PCR to evaluate the crayfish latent carrier status, combined with transmission experiments to further validate the molecular results. 3. From the total of 523 crayfish tested (490 spiny‐cheek crayfish, 33 noble crayfish), none positive for A. astaci was detected. Transmission experiments confirmed these results: No abnormal mortality or behavioural changes were seen in noble crayfish kept together with American crayfish from the coexisting populations. If we assume a very low prevalence of A. astaci of 10% in a carrier population, there is a 98% probability of disease being absent in five of the nine coexisting populations tested. Hence, a consistent absence, or an extremely low prevalence, of A. astaci seems to allow the coexistence of European and American crayfish in these central European populations. 4. The results are important for native crayfish conservation and management and demonstrate that disease transmission risk may vary substantially between the different populations of spiny‐cheek crayfish in central Europe.     

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.     

Crayfish invading Europe: the case study of Procambarus clarkii

The red swamp crayfish, Procambarus clarkii, native to northeastern Mexico and southcentral USA, is today the dominant macroinvertebrate in several European countries. While the first introduction of this species into Spain is well-documented, little is known about its pathways of invasion and the reason for its rapid spread in several European countries. Study of the biology of the species has revealed a number of properties that makes this crayfish a successful invader. Procambarus clarkii exhibits properties characteristic of an r-selected species, including early maturity at small body size, rapid growth rates, large numbers of offspring at a given parental size, and relatively short life spans. It is also plastic in its life cycle, able to disperse widely in the habitat and to tolerate environmental extremes. It displays generalist and opportunistic feeding habits, consuming macrophytes and preying on amphibians. Procambarus clarkii can also replace indigenous crayfish by a combination of mechanisms, including competitive exclusion and transmission of the fungus-like Aphanomyces astaci, responsible for the crayfish plague. Finally, this species shows a wide behavioral flexibility when coping with new types of predators. The results of these studies, combined with the increasing information available in the scientific literature on this and other crayfish species, will help us understand invasions in this taxon and make predictions about the identity of future crayfish invaders.     

Austropotamobius pallipes reduction vs. Procambarus clarkii spreading: Management implications

One of the main threats to native European crayfish is the spread of alien crayfish species that are immune carriers of the detrimental crayfish plague Aphanomyces astaci. In this study we analyzed both at a regional and at a local scale factors determining native and alien crayfish distribution in an area where the species Procambarus clarkii is currently spreading. We aim to understand which management strategies could prevent the extinction of native populations. We sampled 81 waterbodies in Lombardy (NW Italy) to assess the Austropotamobius pallipes complex and alien crayfish occurrence; we also monitored the only first order stream in our study area that we found to be currently inhabited by A. pallipes upstream and by P. clarkii downstream. A. pallipes generally occurred in small brooks, near the spring, and was linked to low periphyton abundance, while P. clarkii occurred in sites at lower altitudes, far from the spring area, mainly in lentic waterbodies with large widths; this allochthonous species was positively related to periphyton abundance. Our monitoring showed that physical barriers such as dams may prevent P. clarkii dispersal upstream. Our results confirm that A. pallipes and P. clarkii have different ecological requirements and show that, at least during the first years of invasion, P. clarkii spreading involves lowland or downstream altered sites. We suggest the need for management strategies maximizing connectivity among native populations, to avoid isolation, and promoting the separation of native populations from those of P. clarkii.     

Comparison of trophic function between the globally invasive crayfishes <Emphasis Type="Italic">Pacifastacus leniusculus</Emphasis> and <Emphasis Type="Italic">Procambarus clarkii</Emphasis>

Impacts of invasive species may manifest most strongly if these organisms are highly distinct functionally from the native species they often replace. Yet, should we expect functional differences between native and invasive species of generalist organisms like freshwater crayfish? Some existing evidence has pointed to native and invasive crayfish species as ecologically equivalent. We contribute to this literature by comparing the trophic niches of the globally invasive crayfishes Pacifastacus leniusculus and Procambarus clarkii, by applying carbon and nitrogen stable isotope analyses to replicated allopatric (alone) and sympatric (together) lake populations in western Washington State, USA, where P. clarkii has been recently introduced and P. leniusculus is presumed native. Our study corrected for potential inherent differences in lake food webs as a consequence of lake abiotic or biotic characteristics using random effects in linear mixed effects models. We found that although overall trophic niche size or area of these species was not significantly different, P. leniusculus was significantly higher in trophic position than P. clarkii when also accounting for the effects of body size, sex, and lakes as random effects. This pattern of increased trophic position of P. leniusculus over P. clarkii was conserved over time in one sympatric lake for which we had data over multiple years. Cumulatively, our findings point to trophic differences between the globally cosmopolitan crayfishes P. leniusculus and P. clarkii, particularly when accounting for the ways that ecosystem context can affect food web structure of communities and the trophic resources available to these consumers.     

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.     

Wound reactions and Aphanomyces astaci growth in crayfish cuticle

Superficial wounding of crayfish soft cuticle by removal of the epicuticle caused hemocyte aggregation beneath the wound. The aggregation seemed to be induced by osmotic factors. Subsequently, melanin was only formed in parts of the wound region. Swimming zoospores of the fungal parasite Aphanomyces astaci preferentially encysted in the near vicinity of fresh superficial wounds. Cysts attached onto the naked endocuticle became encapsulated by melanin and were mostly killed during the process. The induced melanization reactions may have antifungal effects. The intermolt cuticle of a highly resistant crayfish species, Pacifastacus leniusculus, was easily penetrated by the fungus only via wounds. The cell walls of the penetrating hyphae became heavily melanized, growth was visibly disturbed, and they grew sparsely in the wound region. As soon as they reached outside the wound region they grew profusely. In susceptible crayfish Astacus astacus melanization was slower and the wound reactions prevented fungal growth much less as evidenced by microscopy. The preferential direction of hyphal growth is parallel to the chitin fibrils in both the resistant crayfish P. leniusculus and the susceptible A. astacus.     

Invasion of the shelter snatchers: behavioural plasticity in invasive red swamp crayfish,Procambarus clarkii

1. In many freshwater systems, competition for shelter plays an important role in determining the persistence of both native and alien species. The red swamp crayfish, Procambarus clarkii, is currently invading the native habitat of the signal crayfish, Pacifastacus leniusculus, in southern Oregon, and interspecific competition for shelter may be driving the species replacement in this region. 2. We designed a 2 × 3 factorial mesocosm experiment, with shelter density and species combination as factors, to investigate shelter occupancy and resource competition. Contrary to our predictions, the two crayfish species are equal competitors for shelter. Further, the invasive P. clarkii modified its shelter occupancy behaviour in the presence of the native P. leniusculus and has broader microhabitat preferences. 3. Specifically, we found that P. clarkii alters shelter occupancy and space use patterns when the two species occurred together, such that shelter use was identical between P. clarkii and P. leniusculus in mixed‐species treatments. In such treatments, both species increased their use of shelters when shelter density increased. When P. clarkii was alone, however, individuals did not alter shelter use as a function of shelter density, whereas P. leniusculus exhibited similar density‐dependent behaviour in both mixed‐ and single‐species treatments. 4. In a complementary field survey, we employed an ‘epicentre‐based’ design to sample two field sites. We observed patterns of microhabitat use and breadth for each species similar to those in our mesocosm experiment: the invasive P. clarkii was more abundant across different habitats and used a broader range of microhabitats than the native P. leniusculus. As such, we found that P. clarkii was more abundant across both field sites than the P. leniusculus, occupying microhabitats within and beyond the preferred range of P. leniusculus. Both field sites were affected by urban development and agriculture. 5. The use of microhabitats by both species was similar in the laboratory and the field. This study confirms that P. clarkii individuals can, and do, successfully occupy microhabitats preferred by P. leniusculus in the Willamette Valley. The results from our study may be relevant to other freshwater systems inhabited by P. clarkii and contribute to the understanding of ‘niche opportunity’, a concept which defines the environmental conditions that promote biological invasions.     

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.     

Home-field advantage: native signal crayfish (Pacifastacus leniusculus) out consume newly introduced crayfishes for invasive Chinese mystery snail (Bellamya chinensis)

The introduction of non-indigenous plants, animals and pathogens is one of today’s most pressing environmental challenges. Freshwater ecologists are challenged to predict the potential consequences of species invasions because many ecosystems increasingly support novel assemblages of native and non-native species that are likely to interact in complex ways. In this study we evaluated how native signal crayfish (Pacifastacus leniusculus) and non-native red swamp crayfish (Procambarus clarkii) and northern crayfish (Orconectes virilis) utilize a novel prey resource: the non-native Chinese mystery snail (Bellamya chinensis). All species are widespread in the United States, as well as globally, and recent surveys have discovered them co-occurring in lakes of Washington State. A series of mesocosm experiments revealed that crayfish are able to consume B. chinensis, despite the snail’s large size, thick outer shell and trapdoor defense behaviour. Crayfish exhibited size-selective predation whereby consumption levels decreased with increasing snail size; a common pattern among decapod predators. Comparison of prey profitability curves—defined as the yield of food (weight of snail tissue) per second of feeding time (the time taken to crack the shell and consume the contents)—suggests that small and very large snails may represent the most profitable prey choice. By contrast, previous studies have reported the opposite pattern for crayfish consumption on thin-shelled snails. For all snail size classes, we found that native P. leniusculus and invasive O. virilis consumed greater numbers of snails than invasive P. clarkii. Moreover, P. leniusculus consistently handled and consumed snails at a faster pace compared to both invasive crayfishes across the range of snail sizes examined in our study. These results suggest not only that B. chinensis is a suitable food source for crayfish, but also that native P. leniusculus may ultimately out-consume invasive crayfishes for this new prey resource.     

A comparative study of the physiological condition of native and invasive crayfish in Croatian rivers

The physiological condition of two invasive crayfish species identified in Croatian rivers (Orconectes limosus and Pacifastacus leniusculus) was compared with that of native crayfish populations (Astacus astacus and A. leptodactylus). Hepatosomatic, gonadosomatic and abdominal muscle indices were examined for all four species and within a specific invadernative pair. The results demonstrate that invasive crayfish had better overall physiological condition when compared to native species, with a higher energy content of the hepatopancreas, abdominal muscle and gonads in invasive than in native species, with the exception of A. leptodactylus females which demonstrated an increased ability to allocate energy to reproduction in comparison with other species. These results also indicate that A. astacus is physiologically more unstable than A. leptodactylus and thus more likely to be outcompeted and replaced by non-indigenous crayfish species.