Causes and consequences of crayfish extinction: Stream connectivity,habitat changes,alien species and ecosystem services

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Invasive species of crayfish use a broader range of predation-risk cues than native species

The responses of invasive and native species of crayfish to conspecific and heterospecific alarm odors were recorded in the laboratory. Individuals of the North American invasive Procambarus clarkii responded just as strongly to odors from crushed Austropotomobius pallipes as they did to crushed conspecifics. The North American invasive Orconectes limosus also responded as strongly to P. clarkii odor as to conspecific odor. The native Italian species A. pallipes responded more strongly to conspecific alarm than to heterospecific alarm from P. clarkii. The pattern of invasive species of crayfish using a broader range of danger signals than displaced native species appears to be robust.     

The Decline of the Endangered Populations of the Native Freshwater Crayfish (Austropotamobius pallipes) in Southern Spain: It is Possible to Avoid Extinction?

The southeastern mountains of Spain represent the southernmost limit of the genus Austropotamobius and the species A. pallipes (Lereboullet). The taxonomic position of this isolated crayfish in southern Spain is not clear, being genetically close to A. italicus, but morphologically distinct. A severe decline occurred during the 1980s, especially due to expansion of the alien species Procambarus clarkii, a North American freshwater crayfish and a vector of the aphanomycosis disease. In order to design a strategy for native crayfish conservation, recent trends in native crayfish populations, influence of isolation and habitat variables on their survival and possibilities for their recovery through restocking were studied. A decline in populations was observed between 1991 and 2002 (from 26 to 14 populations), and a total extinction could be predicted within the next 13 years. Two well-defined periods of rapid extinction rates were detected, 1991–1994 (1.25 populations/year) and 1999–2002 (1.50 populations/year). Main causes of extinction for these two periods were invasion by P. clarkii and mortality by unknown causes, respectively. The isolation variables had some positive effects on survival of populations but these cannot offer a sufficient guarantee, since several cases of extinction can be affected by a large component of stochastic factors, including random catastrophes. On the other hand, survival trials and restocking experiments showed that it was possible to recover lost habitats, when P. clarkii was absent and environmental conditions were good. It is concluded that it is possible to avoid extinction of the native crayfish populations; however, the conservation strategies must be based on an urgent stocking/restocking program.     

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.     

Early assessment of the impact of alien species: differential consequences of an invasive crayfish on adult and larval amphibians

Aim Early assessment of the impact of invasive alien species is crucial to set up timely management, but often the impact is evident when it is too late for action. We evaluated relationships between the alien crayfish, Procambarus clarkii, the distribution of native amphibians, and the abundance of their larvae. We assessed whether considering measures of reproductive success provide a more prompt measure of impact than considering just species distribution. Location One hundred and twenty‐five wetlands in Northern Italy, in an area recently invaded by P. clarkii. Methods We surveyed wetlands to assess the presence of breeding activity of amphibians and the distribution of P. clarkii. We measured the abundance of amphibian larvae before metamorphosis through pipe sampling. We built models analysing the relationships between amphibian and crayfish distribution, while taking into account spatial autocorrelation and environmental features. Analyses were performed at both the species level (generalized linear models and spatial eigenvector mapping) and community level (constrained redundancy analysis). Results In terms of breeding site distribution, only two amphibians (Lissotriton vulgaris and Hyla intermedia) were negatively associated with P. clarkii, while the relationships between other the species and P. clarkii were positive or not significant. However, larval abundance for all amphibian species was negatively associated with the alien crayfish. Analyses performed at community and single species levels yielded consistent results. Main conclusions Procambarus clarkii impacts amphibians through different processes. Newts probably avoid invaded wetlands for breeding. Other species attempt breeding in wetlands with crayfish, but suffer very low success. Considering distribution data alone would not provide a correct picture of the impact of this alien species; measures of reproductive success may allow a more accurate assessment of the impact.     

Factors affecting the establishment of the invasive crayfish Procambarus clarkii (Crustacea, Decapoda) in the Mediterranean rivers of the northeastern Iberian Peninsula

It is essential to find the combination of factors associated with ecosystem invasibility, as this forms part of basic knowledge on biological invasions and provides important information to guide management and conservation decisions. We surveyed 325 sampling sites in Catalonia to investigate relationships between crayfish presence and a series of biotic and abiotic factors, including fish abundance and species richness, geographical features, and water mineralization and eutrophication. Abiotic data provided by 29 environmental variables were studied by principal-components analysis. We then used a combination of three statistical approaches (comparison of average scores, general linear mixed models, and hierarchical partitioning analysis) to determine the potential relationship between crayfish occurrence and predictors. Our findings seem to indicate that the presence of crayfish was associated with geographical features, water mineralization and eutrophication, and the introduction of non-indigenous fish species to Catalonia. Our results also suggest that re-establishment of the natural hydrology of Mediterranean streams could hinder the spread of Procambarus clarkii. This, combined with preservation of headwater streams and attempts at local extirpation of P. clarkii, would favour native species and, potentially, enable the successful reintroduction of the native white-clawed crayfish (Austropotamobius pallipes species complex).     

Complex impact of an invasive crayfish on freshwater food webs

Invasive alien species can have complex effects on native ecosystems, and interact with multiple components of food webs, making it difficult a comprehensive quantification of their direct and indirect effects. We evaluated the relationships between the invasive crayfish, Procambarus clarkii, amphibian larvae and predatory insects, to quantify crayfish impacts on multiple levels of food webs, and to evaluate whether crayfish predation of aquatic insects has indirect consequences for their preys. We used pipe sampling to assess the abundance of crayfish, amphibian larvae and their major predators (Ditiscidae, Notonectidae and larvae of Anisoptera) in invaded and uninvaded ponds within a human dominated landscape. We disentangled the multivariate effects of P. clarkii on different components of food web through a series of constrained redundancy analyses. The crayfish had a negative, direct impact on both amphibian communities and their predators. Amphibian abundance was negatively related to both predators. However, the negative, direct effects of crayfish on amphibians were much stronger than predation by native insects. Our results suggest that this crayfish impacts multiple levels of food webs, disrupting natural prey-predator relationships.     

Is the exotic red swamp crayfish (Procambarus clarkii) a current threat for the Mediterranean tree frog (Hyla meridionalis) in the Camargue (Southern France)?

The non-indigenous red swamp crayfish (Procambarus clarkii) has been shown to be a threat for amphibian conservation. Many amphibian species breed in temporary ponds to diminish predation risk as such ecosystems are free of large predators. However P. clarkii, occurring as an invasive species in the Camargue delta, can readily disperse on the ground and thus colonize isolated ponds. We studied the current impact of the exotic crayfish on the reproductive success of the Mediterranean tree frog (Hyla meridionalis). In a mesocosm experiment, we tested the effect of two crayfish densities (1 and 3 crayfish/m²) on tadpole abundance. We also tested in a field experiment, within a temporary pond, the crayfish’s predation on the tree frog’s eggs. Finally, we developed site occupancy models using data from 20 ponds to assess the effect of crayfish abundance on tadpole abundance. Neither the experiments, nor the site occupancy models showed a negative impact of the current crayfish abundance on the tree frog populations breeding in ponds. We found that recorded crayfish densities were lower than in other areas where crayfish has impacted amphibian populations, but we hypothesize that current crayfish abundance in the area may increase in the future, thus impacting tree frog populations.     

Complex impacts of an invasive omnivore and native consumers on stream communities in California and Hawaii

The effects of invasive species on native communities often depend on the characteristics of the recipient community and on the food habits of the invasive species, becoming complicated when the invader is omnivorous. In field enclosure experiments, we assessed the direct and interactive effects of an invasive omnivorous crayfish (Procambarus clarkii) and either native herbivorous snails (Physella gyrina) or shrimp (Atyoida bisulcata) on stream communities in California and Hawaii, respectively. Based on literature data and the characteristics of each study site, we predicted that crayfish would affect primarily algal-based trophic linkages in an open California stream but detritus-based trophic linkages in a shaded Hawaiian stream, with trophic cascades mediated through crayfish effects on primary consumers being observed in both systems. As predicted, crayfish in California directly reduced periphyton, filamentous algae, sediment, and snail levels, but generated a cascade by decreasing snail densities and increasing periphyton biomass. Contrary to prediction, crayfish did not reduce total invertebrate biomass. As predicted, crayfish in Hawaii reduced leaf litter, filamentous algae, and benthic invertebrate biomass. Contrary to our predictions, however, a trophic cascade was not observed because shrimp did not affect periphyton levels, crayfish did not reduce shrimp abundance, and crayfish had greater negative impacts on filamentous algae than did shrimp. Our findings highlight that the same invasive species can generate different effects on disparate systems, probably as mediated through the availability of different food types, flexibility in the invasive species’ food habits, and complex pathways of trophic interaction.     

Multi‐faceted impacts of native and invasive alien decapod species on freshwater biodiversity and ecosystem functioning

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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.     

Transformation of detritus by a European native and two invasive alien freshwater decapods

Invasive alien species have the potential to alter biodiversity and ecosystem processes. In freshwaters, detritus decomposition is a major ecosystem service but it remains uncertain whether invasive alien decapods process detritus differently to natives. This study examined leaf litter processing, and cascading effects on biofilms, by the European native white clawed crayfish (Austropotamobius pallipes) compared to two invasive alien decapod species: the American signal crayfish (Pacifastacus leniusculus) and the Chinese mitten crab (Eriocheir sinensis). Invasive alien decapods were responsible for higher leaf litter decomposition than the native. In comparison with native crayfish, invasive alien crab and crayfish showed higher rates of litter consumption, increased production of smaller leaf fragments, fine particulate organic matter (FPOM) and dissolved organic carbon. Nutrients (ammonia and soluble reactive phosphorous) derived from excretion (measured separately in the absence of biofilms) varied among decapod species, being lower for P. leniusculus. However, nutrient concentrations did not vary among species in the detritivory experiments with biofilm, implying nutrients were utilised for biofilm production and respiration as no differences in biomass were evident among decapod treatments. These results show invasive alien decapods have the potential to increase the magnitude of detrital processing to FPOM in rivers, but indirect impacts on primary producers due to nutrient release are uncertain based on this experimental context.     

Predatory impacts of alien decapod Crustacea are predicted by functional responses and explained by differences in metabolic rate

Alien predators can have large impacts on prey. It is important that we understand, and ideally predict, these impacts. Here, we compare predatory impacts of size-matched decapod crustaceans—invasive alien Eriocheir sinensis and Pacifastacus leniusculus, and native European Austropotamobius pallipes—and use this case study to inform methods for impact prediction. We quantify functional responses (FRs) on three macroinvertebrate prey species, examine switching behaviour, and measure metabolic rates as a possible mechanistic explanation for differences in predation. FRs show a consistent pattern: attack coefficients and maximum feeding rates are ordered E. sinensis?≥?P. leniusculus?≥?A. pallipes for all prey species. Attack coefficients of E. sinensis are up to 6.7 times greater than those of size-matched crayfish and maximum feeding rates up to 3.0 times greater. FR parameters also differ between the invasive and native crayfish, but only up to 2.6 times. We find no evidence of switching behaviour in crayfish but suggestions of negative switching in E. sinensis. Differences in FR parameters are mirrored by differences in routine, but not standard, metabolic rate. Overall, our data predict strong predatory impacts of E. sinensis, even relative to alien P. leniusculus. Strong impacts of P. leniusculus relative to A. pallipes may be driven more by body size or abundance than per capita effect. FRs vary between prey types in line with existing knowledge of impacts, supporting the use of FRs in quantitative, prey-specific impact predictions. MRs could offer a general mechanistic explanation for differences in predatory behaviour and impacts.     

Effectiveness of dam construction to contain the invasive crayfish Procambarus clarkii in a Mediterranean mountain stream

Invasive crayfish are a worldwide problem for aquatic ecosystems. So far, no control method has proven successful. Field data from invaded streams have suggested that physical structures may hamper the spread rate of invasive crayfish into new areas. However, given the difficulties for carrying out dam construction in natural habitats, data about their effectiveness in incipient invading populations are practically nonexistent. This paper evaluates the effectiveness of small dams to contain the advance of an incipient population of the invasive Procambarus clarkii in a mountain stream harboring the European southernmost population of the endangered Austropotamobius pallipes. The management strategy involved the construction of 3 artificial small (<3 m high) dams that were complemented with specific design solutions to increase their theoretical efficacy. Catch Per Unit Effort (CPUE) obtained during monitoring surveys carried out for 4 years were used as an indicator of containment effectiveness. The dams successfully prevented Procambarus clarkii from extending its range into the area occupied by A. pallipes. In addition, regardless of whether the construction of new dams isolated the leading edge of the invading population between two dams, the CPUE declined to below detectable limits. Therefore, dams are suggested to effectively stop, or at least hinder, the advance of invasive crayfish. Long-term monitoring is recommended to verify the on-going success of the dams in preventing upstream invasion.     

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.     

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.     

Physicochemical habitat association of a native and a non-native crayfish in the lower Flint river, Georgia: implications for invasion success

Invasive species must cope with a suite of environmental conditions that are different from those in their native ranges. We examine how the physicochemical environment contributes to the invasion success of Orconectes palmeri, a non-native crayfish, in the lower Flint River basin, Georgia, USA. We examined the distribution of Procambarus spiculifer, a native crayfish, and O. palmeri within the lower Flint River basin, and examined associations between species relative abundance and physicochemical variables. Within the lower Flint River, O. palmeri was found almost exclusively at upstream sites, while P. spiculifer was more abundant downstream. We did not detect small O. palmeri downstream, suggesting little recruitment in this area. Within tributaries, only native crayfish were observed. O. palmeri was more abundant at sites with warmer water temperatures, and P. spiculifer was more abundant at sites with cooler water temperatures, which were maintained by ground water seepage. P. spiculifer abundance was also positively associated with abundance of coarse wood. Laboratory studies demonstrated that O. palmeri selected warmer temperatures than P. spiculifer, suggesting that warmer temperatures in the upstream area favor O. palmeri. Water temperatures may have increased in recent years due to human withdrawals from the aquifer and the installation of upstream dams, creating a thermal regime that P. spiculifer has not historically encountered. Our findings suggest that the maintenance of groundwater inputs and a forested riparian buffer is crucial to protect populations of P. spiculifer and to prevent further spread by O. palmeri, especially if climatic changes result in warmer waters.     

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.     

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.     

Indicators of movement and space use for two co-occurring invasive crayfish species

Red swamp crayfish (Procambarus clarkii) and signal crayfish (Pacifastacus leniusculus) are two invasive freshwater species with a worldwide distribution. The objective of this work was to investigate how the two species move and use space in an area of recent coexistence. Simultaneously, we test the use of new tools and indices to describe their movement patterns. To accomplish this we performed a radio-tracking program within a river-type habitat during two different periods (September/October 2010 and June/July 2013). We used spatial analysis tools to map crayfish radio-location data with and without accounting for the curvature of the river. To assess the consistency of the direction of movement and of the distances traveled by crayfish, two indices were developed. To assess the habitat preferences of each species we applied Ivlev's Electivity Index and the Standardized Forage Ratio. Movement of P. clarkii and P. leniusculus differed. The average detected movement was 8.8 m day⁻¹ for P. clarkii and 17.5 m day⁻¹ for P. leniusculus. However, crayfish behavior ranged from almost complete immobility – sometimes during several days – to large movements, in half a day, up to a maximum of 255 m for P. clarkii and 461 m for P. leniusculus. The proportion of upstream or downstream movements was independent of the species and both species displayed no preference for either direction. The indices of consistency of movement showed a large interindividual variation. Species and period (2010 or 2013) affected the mean daily distance traveled, maximum observed distance from location of release and percentage of observations under vegetation cover. The Ivlev's Electivity Index and the Standardized Forage Ratio presented similar results. P. clarkii showed a preference for pool areas with riparian vegetation cover while P. leniusculus preferred riffle and pool areas with riparian vegetation cover. Our work provided new and valuable data for modeling the active dispersal of these two problematic invaders in a context of coexistence.