Evaluation of the suitability of the parthenogenetic marbled crayfish for aquaculture: potential benefits versus conservation concerns

The parthenogenetic marbled crayfish, Procambarus virginalis, is currently being discussed as a promising new candidate for aquaculture that could supply people in developing countries with high-quality protein and income. The main advantage of marbled crayfish is parthenogenetic reproduction. Comparison of growth between marbled crayfish and red swamp crayfish, Procambarus clarkii, the leading species in crayfish aquaculture revealed inferior body size and considerably slower growth in marbled crayfish. Only a very small proportion of the production would meet the size requirement of the international market and could serve as a cash crop. Aquaculture for local markets in extensive outdoor systems is probably economically feasible in developing countries, but the highly invasive and competitive marbled crayfish could easily escape from such sites, invade natural ecosystems and impair the autochthonous fauna and flora. Culture in closed indoor systems would be a safe alternative but this cost-intensive approach is economically not profitable. Because of small body size and slow growth, conservation concerns, and economic reasons, the marbled crayfish is considered unsuitable for aquaculture. It should not be spread around the globe for aquaculture and sustainable fisheries as was earlier done with the congeneric Procambarus clarkii, resulting in devastating ecological effects in numerous countries.

     

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.     

An invaded invader: high prevalence of entocytherid ostracods on the red swamp crayfish <Emphasis Type="Italic">Procambarus clarkii</Emphasis> (Girard, 1852) in the Eastern Iberian Peninsula

The American red swamp crayfish Procambarus clarkii (Girard, 1852) was introduced in 1973 into the Iberian Peninsula for commercial purposes. As a result of both the expansion from the Iberian Peninsula and, probably, further introductions in other European countries, now it is widely distributed throughout much of Europe. The ecological impacts of this invading crayfish have received increasing attention, but nothing is known about its symbiotic entocytherid ostracods outside the American continent. The present survey has examined more than 200 crayfishes from 12 localities distributed over a wide area of Eastern Spain. Entocytherid ostracods were extracted from individual crayfishes and they were identified, counted, assigned to developmental instars and sexed. In all the study locations but one, we found at least one crayfish individual infected by entocytherid ostracods and the species determined was the same in all cases: Ankylocythere sinuosa (Rioja, 1942). The number of ostracods on individual P. clarkii varied notably in relation to crayfish size and also differed significantly among sampling sites. The crayfish size effects on ostracod densities might be related to the amount of resources and to the crayfish age and moulting frequency affecting ostracod distribution and population structure. In addition, the spatial variation in ostracod densities could also be related to site-specific habitat traits and the variability of crayfish population dynamics. Our study represents the first citation of an alien entocytherid species in Europe and demonstrates its wide distribution in the Iberian Peninsula. Further research is needed to know the potential effects of this ostracod species on the ecology of P. clarkii and of native species, with implications on the management of this aquatic invader.     

Geographic expansion of the invasive red crayfish <Emphasis Type="Italic">Procambarus clarkii</Emphasis> (Girard, 1852) (Crustacea: Decapoda) in Mexico

The red crayfish Procambarus clarkii, which is native to southcentral USA and northeastern Mexico, has been successfully introduced into several countries around the world. This study documents the geographic expansion of the exotic red crayfish in Mexico and discusses the consequence of a greater propagation of this species in Mexican inland waters. New state records of this crayfish in the Baja California peninsula and in the states of Durango and Sinaloa indicate its progressive dispersion. The propagation of P. clarkii in Mexico has been caused mainly by human introduction, but it is also facilitated because of the species’ tolerance to an ample range of environmental conditions. Because of the invasive capability of P. clarkii, we suspect that this exotic species is competing for habitat and food with native freshwater shrimp of the genus Macrobrachium in many sites of northern Mexico.     

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 structure and dynamics of <Emphasis Type="Italic">Procambarus clarkii</Emphasis> (Girard, 1852) in a Mediterranean brackish wetland (Central Italy)

In 2006 an unusual find of Procambarus clarkii, today considered one of the most dangerous exotic crayfish, was made within the preserved brackish Mediterranean biotope “Palude di Torre Flavia” (Rome, Italy). Here the investigation on the population structure and dynamics of P. clarkii inhabiting this brackish wetland is presented in an attempt to describe the life history pattern in this type of habitat. The present study showed that this species has a lower growth rate and higher longevity than other studied European P. clarkii populations, and that it can damage brackish habitats and human livelihoods. The main results of this study chiefly concern the differences found between several life-history parameters of the studied population and those obtained in previous studies. These results showed the high ecological plasticity of P. clarkii, indicate the need to intervene before the species spreads further in brackish water, for the conservation of Mediterranean coastal habitats.     

Native European eels as a potential biological control for invasive crayfish

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Habitat use and dispersal of the invasive crayfish Procambarus clarkii in ephemeral water bodies of Portugal

We used radio-telemetry to analyze habitat use and dispersal of the invasive crayfish Procambarus clarkii in the extreme environmental conditions of a temporary river in southern Portugal. The rationale of this study was that an understanding of the properties that make this species a successful invader can be of help for the conservation of freshwater biodiversity. The results showed that: (1) crayfish displaced at a similar rate (ranging 2.5–38?m?d^?1) as other European populations; (2) movement was faster at night; (3) crayfish movement had no clear environmental correlates, except for water temperature; (4) peaks of more intense locomotion were intercalated with longer periods of slow or null speed; and (5) P. clarkii did not excavate burrows in the study habitat, but took refuge under boulders and most often occupied complex microhabitats (e.g., vegetated sections of the river). The conclusion was that, notwithstanding their extreme conditions, ephemeral water bodies in southern Europe are highly susceptible to invasion by P. clarkii.     

Shifts in aquatic macroinvertebrate biodiversity associated with the presence and size of an alien crayfish

To investigate the effects of Procambarus clarkii on macroinvertebrate diversity, we conducted a mesocosm experiment simulating small pools in rice field pads after the rice season. We hypothesized that crayfish predation would negatively impact macroinvertebrate diversity, and the magnitude of this impact should vary with the size of P. clarkii. We conducted a short-term mesocosm experiment to determine macroinvertebrate diversity in the presence of three size classes and in the absence of crayfish, as well as the diet composition of crayfish from the three size classes. At the end of the experiments, the diet of crayfish was composed of the most available taxa (Culicidae, Chironomus, Tanytarsini and Orthocladinae). These results also show evidence that, in confined areas, crayfish are important predators of major rice pests such as rice Chironominae larvae. Macroinvertebrate diversity was negatively affected by crayfish presence, but the effect was inversely proportional to crayfish size. The highest diversity index was obtained in the absence of P. clarkii, and juvenile crayfish significantly reduced macroinvertebrate diversity. Thus, the impact of P. clarkii on aquatic macroinvertebrates is size dependent and may be relevant in small pools formed in rice field pads from early autumn to late winter. Overall, our findings suggest that the negative effects of P. clarkii on macroinvertebrate diversity may be particularly strong in local natural assemblages confined to puddles of water or small ponds in wetland areas.     

Can the parthenogenetic marbled crayfish Marmorkrebs compete with other crayfish species in fights?

The parthenogenetic marbled crayfish, Marmorkrebs, has no known wild population, but has been introduced into natural ecosystems in two continents. Interactions with native crayfish, particularly through fighting, could affect the ecological impact of Marmorkrebs introductions. Marmorkrebs have been characterized anecdotally as having low levels of aggression, which could mitigate their potential to compete with native species. We isolated Marmorkrebs and Louisiana red swamp crayfish (Procambarus clarkii), then conducted size-matched intra and interspecific pairings. Marmorkrebs were as likely to win a fight as P. clarkii, although contests between P. clarkii and Marmorkrebs began significantly faster than contests between two Marmorkrebs. These results suggest that Marmorkrebs have the potential to compete with other species on the same level as P. clarkii, which is itself a highly successful introduced species around the world.     

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.     

Genome survey sequencing of red swamp crayfish <Emphasis Type="Italic">Procambarus clarkii</Emphasis>

Red swamp crayfish, Procambarus clarkii, presently is an important aquatic commercial species in China. The crayfish is a hot area of research focus, and its genetic improvement is quite urgent for the crayfish aquaculture in China. However, the knowledge of its genomic landscape is limited. In this study, a survey of P. clarkii genome was investigated based on Illumina’s Solexa sequencing platform. Meanwhile, its genome size was estimated using flow cytometry. Interestingly, the genome size estimated is about 8.50 Gb by flow cytometry and 1.86 Gb with genome survey sequencing. Based on the assembled genome sequences, total of 136,962 genes and 152,268 exons were predicted, and the predicted genes ranged from 150 to 12,807 bp in length. The survey sequences could help accelerate the progress of gene discovery involved in genetic diversity and evolutionary analysis, even though it could not successfully applied for estimation of P. clarkii genome size.     

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.     

Biological control of invasive populations of crayfish: the European eel (<Emphasis Type="Italic">Anguilla anguilla</Emphasis>) as a predator of <Emphasis Type="Italic">Procambarus clarkii</Emphasis>

The red swamp crayfish, Procambarus clarkii, is a paradigmatic invader of freshwater systems. Several attempts have been made to mitigate its multiple impacts but none was successful. Among the different methods proposed, the use of the European eel (Anguilla anguilla) as an indigenous predator is promising but the available information about its predatory ability on crayfish is to date scanty. To fill this gap in knowledge, we ran three experiments in wetlands and irrigation ditches in Italy. The first experiment, in the laboratory, was aimed at quantifying the extent of predation by eels on crayfish, the second, in enclosures, the size classes of crayfish mainly preyed and the possible effect of the eels on P. clarkii behaviour, and the third, in the field, its ability to effectively reduce crayfish populations. Results showed that eels prey on small-sized or soft crayfish, attacking them from the back; an indirect effect was to reduce crayfish trophic activity, which in turn might increases crayfish mortality due to starvation and decreases impact on the community. However, as shown in the field, the use of eels should be appropriately calibrated to the context of application. Taken together, our results show that eels might be used as a complement to the traditional trapping method. However, additional studies are necessary to understand the adequate number of eels to be introduced and to develop appropriate methods for quantifying such effects.     

A chromosome-level reference genome of red swamp crayfish Procambarus clarkii provides insights into the gene families regarding growth or development in crustaceans

Red swamp crayfish Procambarus clarkii is an ecologically and economically important crustacean species. Here, based on a de novo assembly strategy combining PacBio with Hi-C sequencing, we presented a high quality chromosome-level P. clarkii genome. The assembled genome is 2.75 Gb in size with a contig N50 of 216.75 kb. Transposable elements (TEs) make up the largest fraction of the genome (~79.61%), and LINEs comprise the majority of the TEs. Frequent molting and rapid growth of the red swamp crayfish may be explained by the expansion of multiple gene families regarding growth or development. Phylogenetic analysis revealed that P. clarkii diverged from Portunus trituberculatus at 278–407 million years ago (Mya). PSMC analysis identified multiple bottleneck events of the P. clarkii population between 2 kaBP to 14 kaBP. The obtained P. clarkii genome should not only facilitate us understanding the development and evolution of the crayfish species, but also contribute to the genetic improvement in future breeding selections.     

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.     

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.     

Invasive crayfish in Europe: the impact of Procambarus clarkii on the littoral community of a Mediterranean lake

1. Despite the growing number of non‐indigenous crayfish species introduced worldwide, little scientific attention has been given to their effects on the recipient communities. Here, we quantified the impact of adult red swamp crayfish (Procambarus clarkii) on key components of the littoral community of a mesotrophic lake in central Italy. We used two densities of crayfish plus a no‐crayfish control, and two complementary methods –in situ enclosures and a laboratory study. 2. Both experiments showed that P. clarkii strongly affects the community even at a low density (4 m⁻²), although a high crayfish density (8 m⁻²) showed a more pronounced impact in a shorter time. 3. In enclosures, P. clarkii quickly consumed the pond snail Haitia acuta, notwithstanding its anti‐predator behaviour, but not the mosquitofish Gambusia affinis. The biomass of the hydrophytes Nymphoides peltata and Potamogeton spp. was strongly reduced by crayfish grazing, coupled with their non‐consumptive plant clipping and uprooting, which were particularly intense in the case of Potamogeton crispus. In contrast, Utricularia australis was avoided by P. clarkii, even when other resources were exhausted. 4. The introduction of P. clarkii could reduce biodiversity and increase biotic homogenisation in a short time.     

Impact of an introduced Crustacean on the trophic webs of Mediterranean wetlands

Based on a review and our own data, we present an overview of the ecological impacts on the trophic web of Mediterranean wetlands by an introduced Decapod Crustacean, the red swamp crayfish (Procambarus clarkii). P. clarkii lacks efficient dispersal mechanisms but is very well adapted to the ecological conditions of Mediterranean wetlands (fluctuating hydroperiods with regular intervals of drought). As an opportunistic, omnivorous species, which adapts its ecology and life history characteristics, such as timing and size at reproduction to changing environmental conditions, it became readily established in most of the Mediterranean wetland environments. High reproductive output, short development time and a flexible feeding strategy are responsible for its success as an invader. Like most crayfish, it occupies a keystone position in the trophic web of the invaded system and interacts strongly with various trophic levels. It efficiently grazes on macrophytes and is one of the main factors, besides the impact of flamingos, cattle and introduced fish, of the change of many water bodies from a macrophyte dominated, clear water equilibrium to a phytoplankton driven turbid water balance. Juveniles feed on protein rich animal food with the corresponding impact on the macroinvertebrate community in competition with other crayfish or fish species. At the same time, it serves as a prey for mammals, birds and fish. Due to its predatory and grazing activity, it efficiently canalises energy pathways reducing food web complexity and structure. Feeding also on detritus it opens, especially in marshlands, the detritic food chain to higher trophic levels which results in an increase of crayfish predators. As a vector of diseases, it has a severe impact on the preservation and reintroduction of native crayfish. P. clarkii accumulates heavy metals and other pollutants in its organs and body tissues and transmits them to higher trophic levels. Due to the long history of its presence, the complex interactions it established within the invaded ecosystems and the socio-economic benefits it provides to humans, prevention and control seem the most promising management measures to reduce the negative impact of this crayfish species. This revised version was published online in July 2006 with corrections to the Cover Date.