Rainfall stochasticity controls the distribution of invasive crayfish and its impact on amphibian guilds in Mediterranean temporary waters

Invasive crayfish have severely impacted invaded aquatic ecosystems worldwide. We studied temporal and spatial variation in the range expansion of the red swamp crayfish at one of the first European localities to which it was introduced: Doñana National Park (SW Spain). In contrast to the rapid range expansion witnessed in other areas, this invasive crayfish has not spread across the entire park. Instead, its distribution has expanded during wet periods, but contracted during drought periods. The red swamp crayfish has caused steep amphibian declines in other invaded areas. However, after approximately 35 years of crayfish presence in Doñana National Park, we have yet to detect a reduction in the number or occurrence of amphibian species. Amphibians may thus be protected by the large abundance of temporary ponds in the area, which provides them with an effective refuge network. We show that natural fluctuations in annual rainfall and in the number of ponds filled can temporarily eliminate invasive crayfish from particular areas. This fact should be taken into account when attempting to reduce the impact of crayfish on aquatic communities, intensifying crayfish removal during particularly dry years, when it is most effective.     

克氏原螯虾幼体及亚成体对中华鳖的趋避行为

【背景】在我国,克氏原螯虾是一种外来入侵水生生物,已经对入侵地的生态环境造成严重的破坏。【方法】在Y形水迷宫中,研究有经验和无经验的幼体及亚成体克氏原螯虾对中华鳖的趋避行为。【结果】幼虾无论是否有经验都会显著回避中华鳖,降低外倾性;而亚成体虾对中华鳖的反应不及幼虾灵敏。【结论与意义】2种不同发育阶段的外来入侵物种克氏原螯虾均会回避土著物种中华鳖,为外来入侵生物防治和动物行为学及相关研究提供了参考。     

Effects of an introduced crayfish, Procambarus clarkii, on the distribution of south-western Iberian amphibians in their breeding habitats

The introduction of exotic species in aquatic habitats is one of the causes for the amphibian declines observed worldwide. In the 1970s, the red swamp crayfish Procambarus clarkii was introduced in the southwest Iberian Peninsula, where no native crayfish occur. In this study we assess the effect of P. clarkii presence in the breeding site distribution of each of the 13 southwest Iberian amphibians, while simultaneously accounting for the effects of potentially confounding habitat variables, as well as for the effects of the other large aquatic predators in the study area – predatory fish. Amphibian species richness was lower in places where P. clarkii was present than in places without P. clarkii , regardless of fish presence. After accounting for habitat variables and fish, crayfish presence was a negative predictor of the breeding probability for all urodeles ( Pleurodeles waltl , Salamandra salamandra , Triturus boscai and T. marmoratus ) and for two anurans ( Pelobates cultripes and Bufo bufo ). The majority of the species affected usually breed in temporary ponds without fish, but that may be colonized by the crayfish. The ongoing expansion of P. clarkii may eventually lead to a growing isolation of amphibian populations and ultimately to local extinctions and a permanent alteration of the amphibian communities in southwest Iberian Peninsula.     

Managing invasive crayfish: use of X-ray sterilisation of males

1. In the last decade, many attempts have been made to contain the spread of the North American crayfish Procambarus clarkii , an invader of many European water bodies, but none has been successful.
2. This study investigates the effects that ionising irradiation has on the reproduction of P. clarkii males by analysing the behaviour of the treated individuals, their reproductive output, the vitality and survival of their offspring and the damages induced to their gonads.
3. We found that a dose of 20 Gy X-rays did not compromise either the survival or the mating ability of males, but reduced the size of their testes and significantly altered spermatogenesis. The number of aborted eggs was larger in clutches sired by treated males, with a consequent reduction (by 43%) in the number of offspring.
4. These results foster hopes in our efforts to control invasive crayfish, showing the potential effectiveness of ionising irradiation to reduce male fertility in the perspective of adopting the Sterile Male Release Technique to control P. clarkii populations.     

Reproduction in an Irish lake population of the crayfish Austropotamobius pallipes (Lerehoullet)

SUMMARY. 1. Mature crayfish were collected in 1984 from an alkaline Irish lake before and after the mating season.
2. There was some correlation between frequency of mating and decrease in vasa deferentia weight in captive males, but in the field vasa deferentia weight losses were highly variable. The data indicate that one third of adult males may not have mated in the wild.
3. All females appear to have spawned, whether or not mated, with an average 85% reduction in ovary weights over the season.
4. Pleopodal egg counts directly after laboratory spawning were on average 81% of ovarian counts; in the field, an estimated 50 days after spawning, they were only 61% of estimated ovarian egg numbers.
5. Average ovarian egg size was positively correlated with female size. Also, larger crayfish had a wider range of egg sizes than smaller crayfish.
6. It is suggested that aggression and competition for shelter among brooding females may result in a progressive loss of eggs.     

A Comparison of Trace Metal Accumulation in Indigenous and Alien Freshwater Macro-Decapods

Concentrations of Cd, Cu, Fe, Mg, Mn, Ni, Pb and Zn were determined in the exoskeleton and hepatopancreas of three freshwater macro-decapods widely distributed in Tuscany, Italy. The species were the indigenous Austropotamobius pallipes (the white-clawed crayfish) and Potamon fluviatile (the river crab) and the alien Procambarus clarkii (the red swamp crayfish, in Italy aquacultured since 1977 and invasive since 1989). Water and sediments from the three environments in which they occur were analysed for trace metals to evaluate the degree of contamination of the habitats. Procambarus clarkii showed a significantly higher accumulation of most of the metals analysed, including the non-essential cadmium, nickel and lead. Interspecific differences were not related to exposure to higher concentrations of metals, but indigenous and alien macro-decapods possibly differ in their physiological requirements for essential trace metals and/or in their rates of essential and non-essential metal uptake, accumulation, detoxification and excretion.     

A Comparison of Trace Metal Accumulation in Indigenous and Alien Freshwater Macro-Decapods

Concentrations of Cd, Cu, Fe, Mg, Mn, Ni, Pb and Zn were determined in the exoskeleton and hepatopancreas of three freshwater macro-decapods widely distributed in Tuscany, Italy. The species were the indigenous Austropotamobius pallipes (the white-clawed crayfish) and Potamon fluviatile (the river crab) and the alien Procambarus clarkii (the red swamp crayfish, in Italy aquacultured since 1977 and invasive since 1989). Water and sediments from the three environments in which they occur were analysed for trace metals to evaluate the degree of contamination of the habitats. Procambarus clarkii showed a significantly higher accumulation of most of the metals analysed, including the non-essential cadmium, nickel and lead. Interspecific differences were not related to exposure to higher concentrations of metals, but indigenous and alien macro-decapods possibly differ in their physiological requirements for essential trace metals and/or in their rates of essential and non-essential metal uptake, accumulation, detoxification and excretion.     

High prevalence of multiple paternity in the invasive crayfish species,Procambarus clarkii

Reproductive strategy is a central feature of the ecology of invasive species as it determines the potential for population increase and range expansion. The red swamp crayfish, Procambarus clarkii, has invaded many countries and caused serious problems in freshwater ecosystems. However, little is known about the effects of environmental conditions on crayfish paternity and offspring traits in the wild. We studied these reproductive characteristics of P. clarkii in wild populations from two different habitats (ponds and ditches) in three locations with different environmental conditions in China. Genotyping of 1,436 offspring and 30 mothers of 30 broods was conducted by using four microsatellites. An analysis of genotyping results revealed that gravid females were the exclusive mother of the progeny they tended. Twenty-nine of 30 mothers had mated with multiple (2-4) males, each of which contributed differently to the number of offspring in a brood. The average number of fathers per brood and the number of offspring per brood were similar (P > 0.05) among six sampling sites, indicating that in P. clarkii multiple paternity and offspring number per brood are independent of environmental conditions studied. Indirect benefits from increasing the genetic diversity of broods, male and sperm competition, and cryptic female choice are a possible explanation for the high level multiple paternity and different contribution of fathers to offspring in this species.     

Dormancy, dispersal and the survival of cyclopoid copepods (Cyclopoida, Copepoda) in a lowland floodplain

1. The survival of cyclopoid copepods was investigated in a floodplain for 2 years where flooding occurred during the cold season. The cyclopoid community was studied in three waterbodies with distinct hydroperiods: a permanent pond connected to the flooded area during inundation, a temporary pool that is part of the flooded area and an isolated temporary pool.
2. Field studies, including data obtained from samples of water, sediment and soil, showed the overall predominance of species with a summer diapause over those with a winter diapause or without diapause. Emergence of cyclopoid copepods at the onset of flooding, examined using emergence traps and data from recently filled or still isolated temporary pools, showed that some species can survive several months of drying.
3. The ability of the diapausing fourth copepodid stages of Cyclops strenuus and C. insignis , the two cyclopoids most abundant during winter and spring flooding, to survive terrestrial conditions was tested in laboratory experiments. Both species survived for several months, but rates differed among the species. A higher percentage of C. strenuus survived for a longer period, possibly explaining why this species was relatively more abundant in more temporary habitats.
4. Both dormancy and dispersal facilitated survival of cyclopoid copepods in transient habitats connected to each other during flood periods. Dormancy was the most important survival strategy, whereas dispersal could be more important following prolonged periods without flooding.     

Colonization of freshwater habitats by an introduced crayfish, <Emphasis Type="Italic">Procambarus clarkii</Emphasis>, in Southwest Iberian Peninsula

The introduction of some crustacean species has produced alterations of freshwater environments and declines of native species worldwide. The red swamp crayfish, Procambarus clarkii Girard, was introduced in the Southwest Iberian Peninsula in the 1970’s, producing severe impacts on rice agriculture and on native biota such as macrophytes, gastropods, native crayfish and amphibians. We studied the distribution of P. clarkii in two areas of SW Iberian Peninsula: the Sado River basin (SW Portugal), an area colonized by this species around 1990, and the Parque Natural del Entorno de Doñana (SW Spain), colonized soon after its introduction in the Iberian Peninsula, in the 1970’s. Our main goal was to determine which factors limit crayfish distribution, which could help to identify the most effective management practices to contain its spread. Procambarus clarkii was found in most types of water bodies, including small and shallow ones. Distance to a crayfish source was the single predictor variable explaining crayfish occurrence in most types of habitats and in both areas. The only exception was for the Sado permanent stream points, where crayfish presence was negatively affected by an interaction between elevation and flow velocity. Other habitat characteristics have apparently little or no importance for its successful colonization. Moreover, this study indicated that overland dispersal is apparently a frequent phenomenon in this species. Our findings can be used to determine which habitats are most likely to be colonized by the crayfish and to develop practical measures which may limit its spread and minimize its impacts.     

Availability of and access to critical habitats in regulated rivers: effects of low-head barriers on threatened lampreys

1.  Conservation of freshwater animal populations requires their access to, as well as sufficient availability of, critical habitats, such as those for reproduction. Abundant small-scale barriers may cause extensive fragmentation of freshwater habitat but, by comparison to larger structures their effects are rarely considered by catchment managers. The relationship between the distribution of, and access to, spawning habitat in a regulated river, characterized by abundant small barriers, was examined for river lamprey Lampetra fluviatilis , a threatened migratory fish.
2.  Telemetry of adult lamprey in the River Derwent, North East England was used to quantify upriver migration and access to spawning habitat, together with surveys of spawning habitat availability and spawning activity between 2002 and 2007.
3.  Access in to the Derwent appeared severely restricted by a tidal barrage, beyond which lamprey migrated rapidly in unobstructed reaches. Of all lamprey tagged in the lower 4 km of river, or ascending the barrage, 64% and 17% passed the first and second weirs respectively, with high flows crucial for this. Although over 98% of lamprey spawning habitat occurred more than 51 km upstream, on average just 1.8% of river lamprey spawners were recorded there.
4.  In order to protect or rehabilitate species or species assemblages, greater attention needs to be paid to the relative spatial distribution of low-head barriers and the resultant availability of key habitats within individual catchments. This is particularly important given the renewed emphasis internationally on low-head hydropower solutions as a source of renewable energy, and the rapid growth in numbers of low-head barriers in many catchments.     

Viability analysis of endangered crayfish populations

The noble crayfish Astacus astacus L. is a threatened freshwater invertebrate. Many of the remaining populations are isolated and there is considerable concern that diseases and the increased frequency of flooding events may drive these remnant populations to extinction. We performed a population viability analysis for a typical isolated noble crayfish population. We quantified the extinction risk by the mean time to extinction within 1000 years for several scenarios (flooding events, restocking of adults). For a set of parameters derived from field estimates, we estimated the mean time to extinction to be 240 years. However, the median was only 80 years. Multiple sensitivity analysis by logistic regression revealed that spawning probability, juvenile and adult mortality were the important parameters for the survival of the population. The mean time to extinction decreased with increasing frequency of floodings. This is alarming, considering the magnitude of the effect and the expectation of an increasing number of floodings with global warming. Restocking, however, was found to have only a minor effect on the mean time to extinction. Overall, our simulations suggested that for the long-term and self-sustaining survival of the noble crayfish, particularly where they remain isolated, we have to improve the extent and quality of habitats. Nevertheless, additional measures are necessary, especially the removal of dispersal barriers to allow some exchange of individuals between populations. However, this also calls for a control of invasive crayfish species.     

Life history and production of Paranephrops zealandicus in a forest stream, with comments about the sustainable harvest of a freshwater crayfish

1. Life history and production were assessed for the crayfish Paranephrops zealandicus in three reaches of a headwater stream with a catchment of regenerating coniferous-broadleaf forest in the south-east of the South Island of New Zealand.
2. Crayfish density ranged from 3 to 4 m⁻² in riffles and 4–12 m⁻² in pools, depending on reach. Crayfish biomass (4–33 g AFDW m⁻²) and annual production (2–11 g AFDW m⁻²) were high compared with values reported elsewhere, while P:B ratio was low (0.33–0.43). This substantial production was dependent primarily upon high biomass rather than high growth rate.
3. The crayfish of this population rank amongst the longest lived and slowest growing ever recorded. Individuals estimated to be 16+ year of age were not uncommon. Females became reproductively active at 6+ year. Fewer than 4% of females carried eggs, and young remained attached to females for at least 15 months.
4. We propose that characteristics of this population are the consequence of a cool thermal regime (mean daily stream temperature = 7.0 °C, range 1.8–11.9 °C), and that low biomass turnover and poor reproductive rate precludes any sustainable commercial harvest of crayfish from streams in New Zealand with similar thermal regimes.     

The invasive red swamp crayfish as a predictor of Eurasian bittern density in the Camargue, France

Few data exist on the relationships between food levels and breeding density of the Eurasian bittern Botaurus stellaris , a vulnerable species of high-priority concern in Europe. Concurrent data were obtained on male bittern density and relative food abundance over a 3-year period in two wetlands totalling 2500 ha of Mediterranean reed marsh enclosing 25% of the French bittern population. Food abundance was estimated by sampling up to 25 hydrological units using a beach seine in early June of 2002, 2003 and 2004. The density of booming males in each hydrological unit was obtained by point counts and acoustic triangulation in May of the same years. The impact of food abundance on male bittern density was assessed by general regression models using a forward stepwise procedure with mosquitofish Gambusia affinis , carp Cyprinus carpio , other fish species, amphibians, red swamp crayfish Procambarus clarkii and other invertebrates as prey groups. Of these, only to crayfish abundance was bittern density related, contributing to 45% of the variance observed. When the impact of water level was taken into account, the relative abundance of crayfish explained 56% of the inter-annual differences in bittern density. Because crayfish are rich in calcium and well adapted to fluctuating hydroperiods alternating with drought intervals, they provide a good food source for the bitterns throughout the breeding season at the study sites. The loss of diversity and degradation reported from macrophyte-dominated marshes following crayfish invasion does not seem to apply to reed-dominated wetlands. It is further suggested that the recent increase in bittern numbers in the Camargue, while other French populations were decreasing, could in part be related to red swamp crayfish abundance.     

Eleven polymorphic microsatellites isolated from red swamp crayfish, Procambarus clarkii

Eleven microsatellites were isolated from a genomic DNA library enriched for CA- and GA-repeats, and were characterized in 48 individuals of red swamp crayfish Procambarus clarkii. All 11 microsatellites were polymorphic with an average of allele number of 6.6 per locus. Genotypic distributions of these 11 markers were found to be in conformance with the expectations of Hardy-Weinberg equilibrium. All 11 markers were unlinked. These markers are being used to study the invasion routine, genetic diversity and population structure of the species P. clarkii.     

Historical,human, and environmental drivers of genetic diversity in the red swamp crayfish (Procambarus clarkii) invading the Iberian Peninsula

1. Patterns of genetic diversity in invasive populations can be modulated by a range of factors acting at different stages of the invasion process, including the genetic composition of the source population(s), the introduction history (e.g. propagule pressure), the environmental suitability of recipient areas, and the features of secondary introductions.
2. The North American red swamp crayfish, Procambarus clarkii, is one of the most widely introduced freshwater species worldwide. It was legally introduced into Spain twice, near the city of Badajoz in 1973 and in the Guadalquivir marshes in 1974. Thereafter the species rapidly colonised almost the entire Iberian Peninsula.
3. We used seven nuclear microsatellites to describe the genetic diversity and structure of 28 locations distributed across the Iberian Peninsula and to explain the expansion process of the red swamp crayfish. Additionally, we analysed the relationship between environmental suitability and genetic diversity of the studied locations.
4. The red swamp crayfish had a clear spatial genetic structure in the Iberian Peninsula, probably determined by the two independent introduction events in the 1970s, which produced two main clusters separated spatially, one of which was dominant in Portugal and the other in Spain.
5. The human-mediated dispersal process seemed to have involved invasion hubs, hosting highly genetically diverse areas and acting as sources for subsequent introductions. Genetic diversity also tended to be higher in more suitable environments across the Iberian Peninsula .
6. Our results showed that the complex and human-mediated expansion of the red swamp crayfish in the Iberian Peninsula has involved several long- and short-distance movements and that both ecological and anthropogenic factors have shaped the genetic diversity patterns resulting from this invasion process. Early detection of potential invasion hubs may help to halt multiple short-distance translocations and thus the rapid expansion of highly prolific invasive species over non-native areas.

     

Loss of diversity and degradation of wetlands as a result of introducing exotic crayfish

The introduction of the alocthonous Louisiana red swamp crayfish (Procambarus clarkii) in Chozas (a small shallow lake situated in León (North-West Spain)) in 1996 switched the clear water conditions that harboured an abundant and a quite high richness of plants, invertebrates, amphibians and birds to a turbid one followed by strong losses in abundance and richness in the aforementioned groups. Crayfish exclusion experiments done in Chozas previous to this work confirmed the role of crayfish herbivorism on macrophyte destruction that had a trophic cascade effect on the wetland ecosystem. Direct and indirect effects of crayfish introduction on Chozas lake communities have been evaluated and compared with previous conditions before 1996 or with other related lakes in which crayfish were no present. Crayfish had a main role in submerged plant destruction and a potential effect on amphibia and macroinvertebrate population decrease. Plant destruction (99 % plant coverage reduction) was directly related to invertebrates (71 % losses in macroinvertebrate genera), amphibia (83 % reductions in species), and waterfowls (52 % reduction). Plant-eating birds were negatively affected (75 % losses in ducks species); nevertheless, fish and crayfish eating birds increased their presence since the introduction. Introduction of crayfish in shallow plant-dominated lakes in Spain is a main risk for richness maintenance in these endangered ecosystems. This revised version was published online in July 2006 with corrections to the Cover Date.     

Physiological roles of free D- and L-alanine in the crayfish Procambarus clarkii with special reference to osmotic and anoxic stress responses

Under hyper-salinity stress from freshwater to 17 and 25 ppt seawater, red swamp crayfish Procambarus clarkii largely accumulated D- and L-alanine together with glycine, L-glutamine, and L-proline in both muscle and hepatopancreas. The increases of D- and L-alanine in muscle were the highest in all amino acids and reached 6.8- and 5.4-fold, respectively, from freshwater to 25 ppt seawater. These results indicate that both D- and L-alanine are the most potent osmolytes for intracellular isosmotic regulation in crayfish as well as other crustaceans thus far examined. Under anoxia stress below 0.1 mg/l dissolved oxygen for 12 h and subsequent recovery in normoxia for 12 h in freshwater, 17 and 25 ppt seawater, muscle ATP decreased dramatically in all salinity levels and almost depleted in seawater. Along with the decrease of muscle glycogen level, the significant increase of L-lactate was found in muscle, hepatopancreas, and hemolymph for each salinity level, suggesting the transport of L-lactate from muscle into hepatopancreas via hemolymph. Under anoxia, D- and L-alanine also largely increased in both muscle and hepatopancreas for each salinity level. The increase was much higher in seawater than in freshwater. Thus, both D- and L-alanine are possible to be anaerobic end products during prolonged anaerobiosis of this species.     

Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology

Biological invasions are a significant driver of human-induced global change and many ecosystems sustain sympatric invaders. Interactions occurring among these invaders have important implications for ecosystem structure and functioning, yet they are poorly understood. Here we apply newly developed metrics derived from stable isotope data to provide quantitative measures of trophic diversity within populations or species. We then use these to test the hypothesis that sympatric invaders belonging to the same functional feeding group occupy a smaller isotopic niche than their allopatric counterparts. Two introduced, globally important, benthic omnivores, Louisiana swamp crayfish (Procambarus clarkii) and carp (Cyprinus carpio), are sympatric in Lake Naivasha, Kenya. We applied our metrics to an 8-year data set encompassing the establishment of carp in the lake. We found a strong asymmetric interaction between the two invasive populations, as indicated by inverse correlations between carp abundance and measures of crayfish trophic diversity. Lack of isotopic niche overlap between carp and crayfish in the majority of years indicated a predominantly indirect interaction. We suggest that carp-induced habitat alteration reduced the diversity of crayfish prey, resulting in a reduction in the dietary niche of crayfish. Stable isotopes provide an integrated signal of diet over space and time, offering an appropriate scale for the study of population niches, but few isotope studies have retained the often insightful information revealed by variability among individuals in isotope values. Our population metrics incorporate such variation, are robust to the vagaries of sample size and are a useful additional tool to reveal subtle dietary interactions among species. Although we have demonstrated their applicability specifically using a detailed temporal dataset of species invasion in a lake, they have a wide array of potential ecological applications.     

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.