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.     

Predatory functional response and prey choice identify predation differences between native/invasive and parasitised/unparasitised crayfish

Background

Invasive predators may change the structure of invaded communities through predation and competition with native species. In Europe, the invasive signal crayfish Pacifastacus leniusculus is excluding the native white clawed crayfish Austropotamobius pallipes.

Methodology and Principal Findings

This study compared the predatory functional responses and prey choice of native and invasive crayfish and measured impacts of parasitism on the predatory strength of the native species. Invasive crayfish showed a higher (>10%) prey (Gammarus pulex) intake rate than (size matched) natives, reflecting a shorter (16%) prey handling time. The native crayfish also showed greater selection for crustacean prey over molluscs and bloodworm, whereas the invasive species was a more generalist predator. A. pallipes parasitised by the microsporidian parasite Thelohania contejeani showed a 30% reduction in prey intake. We suggest that this results from parasite-induced muscle damage, and this is supported by a reduced (38%) attack rate and increased (30%) prey handling time.

Conclusions and Significance

Our results indicate that the per capita (i.e., functional response) difference between the species may contribute to success of the invader and extinction of the native species, as well as decreased biodiversity and biomass in invaded rivers. In addition, the reduced predatory strength of parasitized natives may impair their competitive abilities, facilitating exclusion by the invader.     

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.     

Movement, dispersal and refuge use of co-occurring introduced and native crayfish

1. Dispersal and habitat use are key elements in determining impacts of introduced species. We examined if an invasive crayfish species showed a different pattern of movement, dispersal and refuge use to that of a species that it displaces. 2. Fifteen adults of the introduced American signal crayfish, Pacifastacus leniusculus and 20 adult native white‐clawed crayfish Austropotamobius pallipes were radiotagged in an area of river where in 2003 they co‐occurred and the spatial behaviour and habitat use of the two species were examined. Subsequent surveys at the study site in 2005 recorded no A. pallipes and the density of P. leniusculus had increased. 3. Clear differences in the spatial behaviour of the two species were found. The median distance moved per day by signal crayfish was over twice that of white‐clawed crayfish, and dispersal from release locations was higher in signal crayfish. A similar range of refuges with a high degree of overlap was used by both species suggesting that the potential for competitive interaction between the two species exists. 4. The greater movement and dispersal by signal crayfish recorded here supports the hypothesis that invaders are better dispersers than the species that they displace. In addition, movements by signal crayfish may allow them to make better use of patchy resources than white‐clawed crayfish and this, coupled with similar microhabitat use, may contribute to the observed replacement.     

Niche modelling to guide conservation actions in France for the endangered crayfish Austropotamobius pallipes in relation to the invasive Pacifastacus leniusculus

1. The white-clawed crayfish (Austropotamobius pallipes) is globally endangered due to the impacts of habitat modification and fragmentation, water pollution, climate change, and invasive species, particularly the signal crayfish (Pacifastacus leniusculus). These pressures have caused the decline of A. pallipes populations in Europe, demonstrating the importance of predicting the species' potential distribution under current and future conditions. Focusing on the watercourses of mainland France, we aimed to identify suitable areas for A. pallipes to guide the conservation of current populations and future introduction actions or protection measures.
2. We applied ecological niche modelling to model the potential distribution of both A. pallipes and P. leniusculus and identified locations suitable for A. pallipes only. We also assessed the potential distribution of the species under two representative concentration pathway (RCP) scenarios: RCP 2.6 and RCP 8.5, respectively describing low-warming and high-warming conditions.
3. We found that A. pallipes and P. leniusculus exploit equivalent niches in France. Despite this, under current conditions, about 5% of the study area simultaneously records a high suitability for A. pallipes and a low suitability for P. leniusculus and is therefore of significant conservation interest. This percentage remains relatively stable under RCP 2.6 for 2050 and 2100, but decreases to 2% under RCP 8.5 for 2100.
4. Ecological niche modelling can supply crucial guidance for conservation actions aimed at protecting endangered species at a national scale by identifying sites most suitable for protection and sites where climate change and invasive species constitute a threat.

     

Behavior and season affect crayfish detection and density inference using environmental DNA

Although the presence/absence of aquatic invertebrates using environmental DNA (eDNA) has been established for several species, inferring population densities has remained problematic. The invasive American signal crayfish, Pacifastacus leniusculus (Dana), is the leading cause of decline in the UK's only native crayfish species, Austropotamobius pallipes (Lereboullet). Methods to detect species at low abundances offer the opportunity for the early detection, and potential eradication, of P. leniusculus before population densities reach threatening levels in areas occupied by A. pallipes. Using a factorial experimental design with aquaria, we investigated the impacts of biomass, sex ratio, and fighting behavior on the amount of eDNA released by P. leniusculus, with the aim to infer density per aquarium depending on treatments. The amount of target eDNA in water samples from each aquarium was measured using the quantitative Polymerase Chain Reaction. We show that the presence of eggs significantly increases the concentration of crayfish eDNA per unit of mass, and that there is a significant relationship between eDNA concentration and biomass when females are egg‐bearing. However, the relationship between crayfish biomass and eDNA concentration is lost in aquaria without ovigerous females. Female‐specific tanks had significantly higher eDNA concentrations than male‐specific tanks, and the prevention of fighting did not impact the amount of eDNA in the water. These results indicate that detection and estimate of crayfish abundance using eDNA may be more effective while females are ovigerous. This information should guide further research for an accurate estimation of crayfish biomass in the field depending on the season. Our results indicate that detection and quantification of egg‐laying aquatic invertebrate species using eDNA could be most successful during periods when eggs are developing in the water. We recommend that practitioners consider the reproductive cycle of target species when attempting to study or detect aquatic species using eDNA in the field.     

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.     

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.     

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.     

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.     

Competitive interactions between co-occurring invaders: identifying asymmetries between two invasive crayfish species

Ecosystems today increasingly suffer invasions by multiple invasive species. Complex interactions between invasive species can have different fitness implications for each invader, which can in turn determine the future progression of their invasions and result in differential impacts on native species and ecosystems. To this end, through pair-wise and group scale experiments, we examined possible interaction outcomes, competition effects and their potential fitness implications for two widespread invasive species of crayfish that increasingly co-occur in freshwater ecosystems of Europe (Pacifastacus leniusulus and Orconectes limosus). In all trials, P. leniusculus demonstrated the potential to outcompete O. limosus in both staged encounters and direct resource competition, being more likely to win heterospecific agonistic encounters and to acquire shelters at a higher rate. Observed dyadic dominance was translated to a broader social context of group-scale experiments, in which dominance of P. leniusculus was further strengthened by size differential between species. O. limosus was not able to compensate for competitive pressure by the dominant P. leniusculus and suffered wet weight loss and more frequent injuries in the presence of P. leniusculus. While both species are detrimental to native ecosystems, the ability of P. leniusculus to withstand competition pressure from another successful invasive species underscores its potential to establish dominant populations. Our results highlight the importance of understanding interspecies competition in prioritizing potential management activities or control efforts in contact zones.     

Cryptic microsporidian parasites differentially affect invasive and native Artemia spp.

We investigated the host specificity of two cryptic microsporidian species (Anostracospora rigaudi and Enterocytospora artemiae) infecting invasive (Artemia franciscana) and native (Artemia parthenogenetica) hosts in sympatry. Anostracospora rigaudi was on average four times more prevalent in the native host, whereas E. artemiae was three times more prevalent in the invasive host. Infection with An. rigaudi strongly reduced female reproduction in both host species, whereas infection with E. artemiae had weaker effects on female reproduction. We contrasted microsporidian prevalence in native A. franciscana populations (New World) and in both invaded and non-invaded Artemia populations (Old World). At a community level, microsporidian prevalence was twice as high in native compared with invasive hosts, due to the contrasting host-specificity of An. rigaudi and E. artemiae. At a higher biogeographical level, microsporidian prevalence in A. franciscana did not differ between the invaded populations and the native populations used for the introduction. Although E. artemiae was the only species found both in New and Old World populations, no evidence of its co-introduction with the invasive host was found in our experimental and phylogeographic tests. These results suggest that the success of A. franciscana invasion is probably due to a lower susceptibility to virulent microsporidian parasites rather than to decreased microsporidian prevalence compared with A. parthenogenetica or to lower microsporidian virulence in introduced areas.     

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.     

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.     

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.     

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.     

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

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

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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.     

Feeding behaviour,predatory functional responses and trophic interactions of the invasive Chinese mitten crab (Eriocheir sinensis) and signal crayfish (Pacifastacus leniusculus)

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