Assessing mate size in the red swamp crayfish Procambarus clarkii: effects of visual versus chemical stimuli

1. Mate assessment requires an efficient system of information exchange between the sexes and often relies on several forms of communication. Both sexes of the crayfish, Procambarus clarkii , select a mate on the basis of its body size, independently of chelar size/symmetry and dominance status, large size being a proxy for a high quality partner. Here, we explored the effects that visual and chemical stimuli, emitted alone or in combination, exert on the assessment of size of a potential mate.
2. We followed a binary choice test paradigm, in which two male or female 'targets', of either large or small size, were simultaneously presented to a female or a male 'chooser'. We recorded the first target visited, the total duration of the visits per target, and the behaviour of the chooser when approaching the target area.
3. Our results show that females require a combination of visual and chemical stimuli to select the larger male. A more complex pattern was found when males were the choosers. While visual and chemical cues together rendered them willing to mate with the larger female, their initial choice and the total time spent near her depended only on smell. In mate assessment by P. clarkii , visual and chemical information seem to act as 'non-redundant signals'.     

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.     

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.     

Mutual mate choice in crayfish: large body size is selected by both sexes, virginity by males only

Mate choice is often assumed to be a prerogative of females because of their putatively larger reproductive investment than males. However, recent evidence suggests that spermatogenesis is far from being limitless and that males show a high selectivity towards their mates, thus maximizing their reproductive success. We investigated mutual mate choice in the crayfish Procambarus clarkii through two experiments. The first experiment explored the effects of body size, chelar size and chelar symmetry and social status of a potential partner. In the second experiment, we asked whether this species can discriminate between partners of the same body size but with different mating status. We used a binary choice test paradigm, in which two 'targets' with opposing characteristics were simultaneously presented to a test animal, the 'chooser'. The results showed that P. clarkii males are more selective than expected. Similar to the other sex, they were significantly attracted by targets with large body sizes, but not by individuals with larger and symmetric chelae or with a dominant status. An inter-sexual difference was found in the second experiment, in which only males seemed to select virgin potential mates. The several adaptive explanations for these preferences, still under debate, are finally discussed.     

Intensive trapping and increased fish predation cause massive population decline of an invasive crayfish

1. Invasive species frequently have adverse impacts on native communities and ecosystems. Management options are often limited. Our goal is to evaluate the effect of intensive trapping and fish predation on the population dynamics of an invasive crayfish. 2. From 2001 to 2005, we removed invasive rusty crayfish (Orconectes rusticus) by trapping in Sparkling Lake in northern WI. In addition, the Wisconsin Department of Natural Resources restricted harvest of fish species known to consume crayfish, thereby increasing predation on crayfish that are too small to trap. 3. After an initial increase, catch rates of rusty crayfish declined by approximately 95%, from 11 crayfish per trap per day in 2002 to 0.65 in 2004. The catch rate in 2005 remained low at 0.5 crayfish per trap. Females comprised nearly 50% of the catch from 2002 to 2004. Unlike rusty crayfish in Sparkling Lake, catch rates of O. rusticus and Orconectes propinquus in three nearby lakes increased or remained relatively constant over the 5‐year removal period. 4. We also examined the influence of habitat and temperature on crayfish catch rates. Catch rates were highest at water temperatures between 20 and 25 °C and on cobble, log or macrophyte habitats that may serve as refuge from fish predation. 5. Five summers of intensive trapping and fisheries management practices reduced abundances, but did not extirpate rusty crayfish in Sparkling Lake. To determine the potential of trapping as a management option for invasive crayfishes, these methods must be tested in other systems.     

Behavioural and growth differences between experienced and naïve populations of a native crayfish in the presence of invasive rusty crayfish

1. Species invasions are a leading threat to native species and ecosystems. How populations of native species respond to the presence of invasive species will ultimately determine their long-term persistence.
2. In this study, we capitalise on a unique opportunity to compare the behaviour and growth of naïve and experienced virile crayfish ( Orconectes virilis Hagen) populations in the presence of invasive rusty crayfish ( O. rusticus Girard ) . In behavioural trials, experienced O. virilis (coexisted with O. rusticus for >30 years) showed more aggressive behaviour than their naïve counterparts. Naïve O . virilis retreated from aggressive interactions with O. rusticus 38% more often than experienced O . virilis. Experienced O. virilis spent 39% more time occupying shelter than naïve O. virilis.
3. There were also differences in O. rusticus behaviour: O. rusticus spent 24% more time occupying shelter with naïve O. virilis relative to experienced O. virilis .
4. In field mesocosm experiments with O. rusticus , naïve O . virilis declined in body mass by 1% while experienced O. virilis' body mass increased by 6%, thus highlighting the potential population-level implications of the previously observed behavioural effects.
5. Our work demonstrates significant behaviour and growth differences between naïve and experienced O. virilis in the presence of invasive O. rusticus. Whether this difference is the result of phenotypic plasticity or evolution by natural selection remains to be determined. Either way, this area of inquiry has implications for managing native populations and species in an increasingly invaded world.     

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.     

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.     

Exploration of potential microbial control agents for the invasive crayfish,Orconectes virilis

The introduced crayfish, Orconectes virilis (Cambarinae; Hagen 1870), has become a serious invasive species in Arizona (USA), altering stream ecosystems and contributing to the decline of native species. But because it is native to the eastern US, and related crayfish including endangered species inhabit nearby states, introduction of a biological control agent presents a unique challenge. This represents a feasibility study, in which we explored bacteria, nematodes, and a virus as potential biological control agents for O. virilis while avoiding harm to native species. White Spot Syndrome Virus (WSSV) from shrimp was found to be highly pathogenic and readily passed by cannibalistic behavior but not by water transmission. Potential activity of WSSV against representative non-target arthropods that may be found in the same ecosystems was also explored.     

Effects of an invasive crayfish on the littoral macroinvertebrates of large boreal lakes are habitat specific

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Disturbance and species displacement: different tolerances to stream drying and desiccation in a native and an invasive crayfish

1. Crayfish are among the most threatened taxa in the world and invasive crayfish are the primary cause of the decline of native crayfish. Most research has emphasised biotic interactions as the mechanism by which native crayfish are displaced by invasives, although crayfish occupy variable environments and the role of disturbance in facilitating crayfish invasion and displacement is understudied. 2. We compared tolerance to a disturbance, stream drying, in a native and invasive crayfish as a potential mechanism to explain their distribution. Our experiments and observations were conducted across scales, from laboratory environmental chambers to stream mesocosms to field sampling. We hypothesised that the invasive crayfish would be more tolerant of desiccation than the native, and that this physiological distinction between the two would be reflected in their distribution in relation to stream drying. 3. In the laboratory, the native crayfish Orconectes eupunctus was less tolerant of desiccation than the invasive Orconectes neglectus chaenodactylus, with all native crayfish dying within 2 days without water, while some of the invasive crayfish survived for nearly 2 weeks. Under simulated stream drying in mesocosms, only the native O. eupunctus survived less well than in a control. Field sampling demonstrated a significant negative relationship between O. eupunctus density and low summer flows, while O. neglectus density was positively associated with low summer flows. The greater resistance of O. neglectus to drying could, through priority effects, inhibit recolonisation by O. eupunctus once flow resumes. 4. Abiotic disturbances are potentially important to the displacement of native by invasive crayfish. Disturbance mediated displacement of aquatic species provides both an opportunity to conserve native species by maintaining or restoring habitat and disturbance regimes and is also a challenge due to increasing human water demand, flow regime alteration and global climate change.     

Niche differentiation among invasive crayfish and their impacts on ecosystem structure and functioning

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Optimising control of invasive crayfish using life‐history information

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Insight into invasion: Interactions between a critically endangered and invasive crayfish

Invasive species are known to competitively displace native species via direct behavioural interactions, or contests, which can result in limited access to valuable resources such as food or shelter for the native. Here, we aimed to determine the dynamics and outcome of agonistic contests between the critically endangered Fitzroy Falls Spiny Crayfish (Euastacus dharawalus) and the invasive yabby (Cherax destructor) in a controlled laboratory setting. Although C. destructor has been listed as a key threatening process for E. dharawalus, the magnitude and nature of its impact have not been formerly assessed. We recorded the frequency and intensity of aggressive interactions between the species, as well as the winner of the contest and subsequent dominance during staged encounters. In addition to this, we recorded the time individuals spent consuming food and actively moving on the substratum. Contrary to our predictions, the frequency of aggressive behaviours performed by the two species did not significantly differ, but E. dharawalus engaged in more intensely aggressive behaviours and was less submissive than C. destructor. As a result, E. dharawalus won significantly more contests than its invasive rival and subsequently achieved a higher dominance score overall. Despite this result, C. destructor spent significantly more time consuming food than did E. dharawalus. These results suggest that dominance in agonistic contests did not translate into dominance over food resources in our study. Ultimately, reduced access to food, combined with the costs of agonistic contests including injury and the relatively low reproductive rates of E. dharawalus indicate that C. destructor may have a negative effect on the survival and persistence of the critically endangered E. dharawalus.     

The importance of allochthonous litter input on the biomass of an alien crayfish in farm ponds

To evaluate the effects of allochthonous litter input on the population density of invasive red swamp crayfish (Procambarus clarkii) in Japanese farm ponds, we analyzed gut contents, stable isotope ratios, and the correlation between crayfish biomass and environmental factors in the ponds. For our correlation analysis, we used Akaike’s information criterion (AIC) corrected for small sample size (AIC_C) to select appropriate models within the generalized linear model. Allochthonous litter input was the most influential variable affecting crayfish biomass, followed by pond area. Gut content analysis demonstrated a positive correlation between the percentage of litter in the crayfish gut and the amount of litter input into the pond from which animals were collected. Crayfish δ¹³C became increasingly similar to litter δ¹³C as litter input into ponds increased. Nitrogen isotope signature analysis suggested that microorganisms attached to litter may contribute to crayfish diet. The above results obtained by three complementary approaches demonstrated an important influence of allochthonous litter input on crayfish biomass in farm ponds. We propose that the appropriate management of surrounding forests may be effective in controlling the abundance of exotic crayfish with minimized impacts on native communities.     

Managing the invasive crayfish Procambarus clarkii: Is manual sterilisation the solution?

1. Management of invasive alien crayfish is challenging, as once established their eradication or control is difficult, even impossible in some areas. Sterile male release technique has been previously assessed in crayfish with encouraging results, however, the methods have not demonstrated the complete sterility of released competitive males. The present study explores whether manual removal of male gonopods, i.e. the appendages responsible for sperm transfer, as a sterilisation technique, might affect male competitiveness and sexual behaviour as well as reproductive potential in the red swamp crayfish Procambarus clarkii.
2. Under controlled laboratory conditions, we analysed the agonistic and sexual behaviour of 64 treated and 64 control males both coupled with a female in single pairs, and 40 treated and 40 control males together with 80 females in a natural-like social context.
3. Removal of gonopods partly altered sexual behaviour, affecting duration of copulation and competitiveness in treated males. However, male readiness to initiate sexual interaction with females was not affected by the treatment. Treated males needed to invest more in agonistic interactions with females to successfully dominate a female for the copulation to take place. Females coupled with treated males did not produce any offspring, compared to females coupled with control males. Treated males were able to regenerate removed gonopods, even if sometimes only partially or malformed. Females that mated with 11 treated males with regenerated gonopods did not produce any juveniles.
4. Although treated males managed to mate with females and impair their reproductive capability under the laboratory conditions, shorter copulation and elevated number of abdominal extensions were observed in treated couples. This indicates that males and/or females are able to sense the lack of gonopods and/or lack of the contact. We believe that female receptivity after an initial mating requires further investigation. Assessment of receptivity in an experimental setting where females are provided with refuges (e.g. burrows) would help us to elucidate whether there is a compensation for unsuccessful copulation. More research is needed on underlying biological mechanisms to better assess male competitiveness, technique effectiveness and limits of technique application.

     

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.     

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.     

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.