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.     

Neuroanatomy of the terminal (sixth abdominal) ganglion of the crayfish,Procambarus clarkii (Girard)

Summary We studied the neuroanatomy of the terminal (sixth abdominal) ganglion in the crayfish Procambarus clarkii with silver-impregnated sections and nickel fills. We describe the fiber tracts, commissures and neuropilar areas, and give the topological relationships of motoneurons and intersegmental interneurons with reference to their neuropilar landmark structures.All five anterior abdominal ganglia have an almost identical number of 600–700 neurons with a similar pattern of distribution. Each contains a single neuromere with a common plan of neuropil organization. In contrast, the terminal ganglion consists of two neuromeres which appear to be derived from the intrinsic sixth abdominal and telson ganglion. The basic organization of each neuromere parallels that of the third abdominal ganglion in the appearance and arrangement of fiber tracts and commissures, although some modifications occur. The fusion of two neuromeres is represented by the duplication of segmentally homologous neurons, MoGs and LGs, whose topological relationships to the neuropil structures are similar to those of the anterior ganglion.We also discuss the origin of the telson and its ganglion (the seventh abdominal neuromere), and dispute the classical theory that the telson derives from a postsegmental region.     

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.     

The topological organization of primary afferents in the terminal ganglion of crayfish,Procambarus clarkii

Summary The central projections of primary afferents in the terminal ganglion of the crayfish can be seen when an axonal filling with nickel chloride with subsequent silver intensification was used for identification. We describe here the topological relationships of the projections to the landmark structures of the neuropil.The terminal ganglion has five pairs of sensory nerves associated with the mechanosensory hairs and internal proprioceptors. The projection fields of the primary sensory neurons in the nerves Rl and R2 are almost entirely restricted to the ipsilateral half of the ganglion, whereas those of the nerves R3, R4 and R5 cross the midline to form three sensory commissures, A6SCI, A7SCI and A7SCII. The projection fields are segregated from each other, although all are restricted to the ventral neuropil which lies under the ventral intermediate tract (VIT). The intersegmental projections that ascend via the connective ipsilateral to their origins could be observed. This pattern of projection correlates well with the receptive fields exhibited by several mechanosensory interneurons on the body surface of the final segment.     

Structure and dynamics of an invasive population of the red swamp crayfish (<Emphasis Type="Italic">Procambarus clarkii</Emphasis>) in a Mediterranean wetland

This study analyzes the population structure and dynamics of an invasive population of Procambarus clarkii (Girard, 1852) in a Mediterranean wetland using the Bhattacharya’s and Von Bertallanfy’s analytical methods. The main purpose was to collect biological data necessary for the management of this nuisance species. A maximum of five age classes were identified for both sexes, three of which being composed of a few or zero individuals. Age classes were classified into two subgroups––spring (SpL) and summer (SuL) lines––on the basis of the different hatching periods. Individuals of SpL showed a faster growth rate and reached a larger body size than those belonging to SuL, probably because they were able to grow for a longer time. No between-sex differences were found in growth patterns except for the asymptotic length (L_∞), which was reached faster by the females. Other population properties were analyzed, such as a high mortality rate, a maximum longevity of 4 years, and a low mean life-time (<12 months). Finally, a relatively small fraction of individuals seemed to survive after the first reproductive peak in spring. Consequently, the structure and dynamics of the study population seem to reveal its stability and spreading potential, as a confirmation of the invasiveness of P. clarkii in Mediterranean wetlands. Handling editor: P. Viaroli     

Breeding biology of the Louisiana red swamp crayfish Procambarus clarkii Girard in Lake Naivasha,Kenya

This paper describes the breeding biology of the Louisiana red swamp crayfish (Procambarus clarkii Girard) that has been introduced in a tropical lake, Naivasha. Notable differences in crayfish biology are found between the place of origin in Louisiana and lake Naivasha.In Naivasha sexual maturity in females is reached at a larger size (42 mm carapace length (CL), 76 mm full length (FL)) than in males (40 mm CL, 71 mm FL). The corresponding figures for Chalmette area of Louisiana are 31–32 mm CL for both sexes and at Ben Hur Research Centre, Louisiana, 33 mm CL. The females weigh between 15 and 20 g at the onset of egg deposition. The corresponding Louisiana values are from 5 to 10 g. Crayfish in Naivasha as in Louisiana breed both inside burrows which are 10–70 cm deep, and on the sediment in shallow water at a depth of between 0.5 and 4 m. These observations suggest that reproduction is very much a lake edge activity. The number of breeding individuals in Naivasha varies with the trend of the water surface level. Sexually active females (form I) as judged from secondary sexual characters (appearance of basal hooks at the base of 3rd and 4th walking legs) persist throughout the year at no less than 60% of the adult male population. This is confirmed by the appearance of recently hatched juveniles (3.4 to 6.5 mm CL) in the water throughout the year. Similarly berried females in Naivasha are found throughout the year, though with peaks at irregular intervals. In Louisiana breeding takes place only from August through November with a single peak in October. The fecundity of crayfish in Naivasha is 433 (SE ± 21, N = 133) and there is a positive correlation between body length and egg number.     

Morphology of descending statocyst interneurons in the crayfish Procambarus clarkii Girard

Summary The morphological features of descending interneurons that responded to the artificial bending of statolith hairs were assessed with intracellular recording and staining techniques. Seven statocyst interneurons were identified on the basis of their structure and response characteristics and designated as interneurons S1 to S7. All seven identified interneurons project to the optic lobe, where the optic nerve also projects, and to the dorsal part of the tritocerebrum, where the eyestalk motoneurons originate. All except interneuron S6 also extend their major branches to other neuropilar regions. S2 projects to the dorsal part of the deutocerebrum, where the statocyst nerve terminates, and S3 to the dorsal part of deutocerebrum and the antennal lobe. Four other interneurons (S1, S4, S5, S7) also extend their branches to the parolfactory lobe to which the statocyst nerve projects as well as to the deutocerebrum and antennal lobe. The extensive dendritic projections of S1–S7 suggest that they are complex multimodal interneurons rather than simple relay interneurons, receiving at least visual and statocyst sensory information. The function of the antennal lobe branches, however, has yet to be determined since the functional role of antennal input in equilibrium control is unknown.     

Distribution of synapses on two types of ascending interneurons in the crayfish,Procambarus clarkii

Summary About 60 pairs of ascending interneurons are present in the terminal ganglion of the crayfish Procambarus clarkii (Girard). Some of these interneurons have been impaled intracellularly, characterized physiologically, and then labeled with horseradish peroxidase (HRP) to examine the distribution and ultrastructure of synapses. A close relationship between ultrastructure and physiological properties has been found between two types of interneurons, which either have a pre-motor effect upon motor neurons or have no such effect. In one interneuron with a pre-motor effect (6D2), input and output synapses are intermingled on thicker branches, whereas only input synapses are found on small diameter branches. Only input synapses have been observed on the branches in another interneuron with-out a pre-motor effect (6B1). No differences in branch morphology are found in these two interneurons. Interneuron 6D2 contains large numbers of small round agranular vesicles, but the same type of synaptic vesicles is rarely seen in interneuron 6B1, which has no output synapses. Our results indicate a good correlation between the synaptic distribution and pre-motor effects of interneurons in the terminal ganglion.Abbreviations A6, 7 Sixth and seventh abdominal segment of the terminal ganglion - AVC anterior ventral commissure - DC I dorsal commissure I - DIT dorsal intermediate tract - DMT dorsal medial tract - eLG extra lateral giant interneuron - LVT lateral ventral tract - LG lateral giant interneuron - LVT lateral ventral tract - MDT median dorsal tract - MG medial giant interneuron - MoG motor giant neuron - MVT median ventral tract - PVC posterior ventral commissure - R1s sensory fiber tract of nerve root 1 - R3m motor fiber tract of nerve root 3 - R4–7 nerve roots 4–7 - SC I,II sensory commissure I,II - VC I,III ventral commissure I, III - VIT ventral intermediate tract - VLT ventral lateral tract - VMT ventral medial tract     

Organochlorine and organophosphorus pesticide concentrations in water,sediment, and selected organisms in Lake Naivasha (Kenya)

Water, sediment, red swamp crayfish (Procambarus clarkii) and black bass (Micropterus salmoides) from Lake Naivasha were analyzed for selected organochlorine and organophosphorus pesticide residues. The mean p,p'-DDT, o,p'-DDT and p,p'-DDE residue levels recorded in black bass (28.3 (± 30.0), 34.2 (±54.0) and 16.1 (±16.1) g kg^–1, respectively) and crayfish (4.6 (±5.1), 3.2 (±2.8), and 1.4 (±1.1) g kg^–1, respectively), were higher than previously recorded. This indicated recent usage of technical DDT in the lake's catchment. Levels of p,p'-DDT, higher than those of p,p'-DDE further emphasized this. Mean lindane, dieldrin, -endosulfan and aldrin concentrations in black bass were 100.5, 34.6, 21.6 and 16.7 g kg^–1, respectively. The same residues were detected at lower concentrations in crayfish at 2.0, 2.0, 2.0 and 1.9 g kg^–1, respectively. The higher fat content (3.7 ± 2.7% SD) in black bass (compared to 0.6 ± 0.3% in crayfish) accounted for the significantly higher residue concentrations in black bass. Organophosphate pesticides were the most commonly used pesticides in the lake's catchment, but none was detected in any of the samples. The results indicate that there is need for further work to identify sources and fate of pesticide contaminants, as well as to improve monitoring of pesticide use throughout the catchment.     

Molecular characterization of the sarcoplasmic calcium-binding protein (SCP) from crayfish Procambarus clarkii

Sarcoplasmic Calcium-binding Protein (SCP) is believed to function as the invertebrate equivalent of vertebrate parvalbumin, namely to “buffer” cytosolic Ca²⁺. We have cloned and characterized a novel SCP from axial abdominal muscle of crayfish Procambarus clarkii (referred to as pcSCP1), and have examined tissue specific distribution and expression as a function of molting stage in non-epithelial and epithelial tissues. The complete sequence of pcSCP1 consists of 1052 bp with a 579 bp open reading frame, coding for 193 amino acid residues (molecular mass of 21.8 kDa). There is a 387 bp 3′ terminal non-coding region with a poly (A) tail. The deduced pcSCP1 protein sequence matched most closely with published SCP sequences from another crayfish Astacus leptodactylus (92.8%) and from shrimp (78.6–81.2%) and fruit fly (53%). Real-time PCR analysis confirmed that pcSCP1 is ubiquitously expressed in all tissues tested (gill, hepatopancreas, intestine, antennal gland, muscle); however it is most abundant in muscle particularly in the axial abdominal muscle. The real-time PCR analysis revealed that pcSCP1 expression is downregulated in pre- and postmolt stages compared with intermolt. Epithelial (hepatopancreas and antennal gland) SCP expression exhibited a more dramatic decrease than that observed in muscle. Expression trends for pcSCP1 paralleled published trends for sarco/endoplasmic reticular calcium ATPase (SERCA), suggesting that their cellular function in regulating intracellular Ca²⁺ is linked.     

Feeding of the exotic Louisiana red swamp crayfish,Procambarus clarkii (Crustacea,Decapoda), in an African tropical lake: Lake Naivasha,Kenya

The Louisiana red swamp crayfish, Procambarus clarkii, has had a major impact on aquatic ecosystems in Europe and America where it has been introduced for human consumption. In Lake Naivasha, where it was introduced in 1970, it is suspected of causing the complete disappearance of native floating-leaved and submerged plants by 1982 and again by 1996; recovery of submerged plants occurred in between, concurrent with a decline in P. clarkii. Examination of the feeding of P. clarkii by microscopic analysis of gut contents collected from the lake confirmed information from both its native and exotic ranges; that it is an omnivore with green plants and insects the predominant items recognised. Feeding experiments confirmed this omnivory, with a preference from herbivory over carnivory. They further showed the importance of native plants as opposed to exotic water hyacinth Eichhornia crassipes. It is concluded that P. clarkii could well have accounted for the observed elimination of native plant species in Lake Naivasha; the cyclical nature of populations of submerged plant species and of P. clarkii in inverse proportion to each other lead us to hypothesise that P. clarkii is a `keystone' species in the lake ecosystem.     

Multimodal responses of the nonspiking giant interneurons in the brain of the crayfish Procambarus clarkii

Three pairs of nonspiking giant interneurons (NGIs; G1, G2, and G3) of the crayfish brain responded with depolarizing and hyperpolarizing graded potentials to body tilt in roll to the ipsi- and contralateral sides in the dark. The higher and the larger the angle of body tilt, the larger was the amplitude of the geotactic responses. In ipsilaterally statocystectomized animals, all the NGIs responded with hyperpolarizing potentials only to the contralateral side-down tilt, whereas in contralaterally statocystectomized animals, they responded with depolarizing potentials only to the ipsilateral side-down tilt. In bilaterally statocystectomized animals, none of the NGIs responded to body tilt in the dark, but in the presence of an overhead light, they exhibited depolarizing and hyperpolarizing potentials in response to body tilt to the ipsi-and contralateral sides, respectively. All the NGIs responded with depolarizing and hyperpolarizing graded potentials to illumination of the contra- and ipsilateral eyes, respectively. The amplitude of these visual responses, however, varied in association with the amplitude of the geotactic response produced by body tilt. These results indicate that the NGIs integrate the sensory inputs from eyes and statocysts and that the interaction between sensory inputs from the left and right sensory organs with either the same modality or with different modalities enhance the directional sensitivity of NGIs as premotoneurons in the compensatory oculomotor system.     

Laboratory conditioning to still or flowing water does not affect the responses to a food stimulus by red swamp crayfish (Procambarus clarkii) in flowing water habitats

We tested the role of hydrodynamics in the use of chemical signals by the red swamp crayfish (Procambarus clarkii). We conditioned the crayfish in either a still water or flowing water habitat for 2 weeks. We then observed the crayfish in control (no stimulus) and experimental (food stimulus) trials in one of two flowing water habitats-laminar or turbulent. Habitat use was significantly different between control and experimental observations, but there was no effect of conditioning habitat or experimental habitat on the responses to the food stimulus. This study adds to a growing body of literature consistent with the idea that gross responses to chemical stimuli in crayfish are not affected by the hydrodynamic context in which they are encountered.     

Shelter competition between resident male red swamp crayfish Procambarus clarkii (Girard) and conspecific intruders varying by sex and reproductive status

The shelter defense dynamics of reproductively active (Form I) male red swamp crayfish Procambarus clarkii (Girard) were investigated by staging serial intrusions by male, maternal or non-maternal female conspecifics after one day of residence. The male residents showed a direct contest advantage only against non-maternal females, and won a significantly higher proportion of the encounters against non-maternal females than against either male or maternal female intruders. However, there was no significant difference in success against male or maternal female intruders. Further experiments against male intruders showed that increasing male prior residence to either 2 or 4 days did not significantly improve the residents’ proportion of successful encounters. A final experiment revealed extremely low shelter fidelity in male P. clarkii, the most likely reason why male shelter defense against conspecific males and maternal females is not successful. These results, combined with those of past research, suggest that non-maternal females, juveniles and recently molted conspecifics are most vulnerable to predation and cannibalism, since males and maternal females easily out-compete non-maternal females for shelter, and adults out-compete juveniles. These findings may have implications for P. clarkii aquaculture and general management.     

Zoogeography, taxonomy, and conservation of West Virginia's Ohio River floodplain crayfishes (Decapoda, Cambaridae)

The crayfish fauna of West Virginia consists of 23 species and several undescribed taxa. Most survey efforts documenting this fauna have been conducted in lotic waterways throughout the Appalachian plateau, Allegheny Mountains, and Ridge and Valley physiographic provinces. Bottomland forests, swamps, and marshes associated with large river floodplain such as the Ohio River floodplain historically have been under-surveyed in the state. These habitats harbor the richest primary burrowing crayfish fauna in West Virginia, and are worthy of survey efforts. In an effort to fill this void, the crayfish fauna of West Virginia's Ohio River floodplain was surveyed from 2004 through 2009. From this survey, nine species from four genera were documented inhabiting the floodplain. Zoogeography, biology, and conservation status is provided for all nine crayfishes. The dominant genus along the floodplain is Cambarus, which includes Cambarus (Cambarus) carinirostris, Cambarus (Cambarus) bartonii cavatus, Cambarus (Procambarus) robustus and Cambarus (Tubericambarus) thomai. Cambarus (Tubericambarus) thomai is the most prevalent burrowing species occurring along the floodplain. The genus Orconectes consists of two native species, Orconectes (Cambarus) obscurus and Orconectes (Cambarus) sanbornii; and two invasive taxa, Orconectes (Gremicambarus) virilis and Orconectes (Procambarus) rusticus. Orconectes (Cambarus) obscurus has experienced a range extension to the south and occupies streams formerly occupied by Orconectes (Cambarus) sanbornii. Both invasive taxa were allied with anthropogenic habitats and disturbance gradients. The genera Fallicambarus and Procambarus are represented by a single species. Both Fallicambarus (Cambarus) fodiens and Procambarus (Orconectes) acutus are limited to the historic preglacial Marietta River Valley.     

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.     

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.     

Purification and properties of alanine racemase from crayfish Procambarus clarkii

Fresh water crayfish Procambarus clarkii is known to accumulate d-alanine remarkably in muscle after seawater acclimation, accompanied by an increase in alanine racemase activity. We have purified alanine racemase from crayfish muscle to homogeneity. The enzyme is a monomeric protein with a molecular mass of 58 kDa. It is highly specific to alanine and does not racemize l-serine, l-aspartate, l-glutamate, l-valine and l-arginine. The enzyme shows the highest activity at pH 9.0 in the conversion of l- to d-alanine and at pH 8.5 in the reverse conversion. Properties such as amino acid sequence, quaternary structure, pyridoxal 5′-phosphate (PLP)-dependency, pH-dependency and kinetic parameters seem to be distinct from those of the microbial alanine racemases. Various salts including NaCl at concentrations around seawater level were potently inhibitory for the activity in both of l- to -d and d- to -l direction.     

Differential growth of crayfish Procambarus alleni in relation to hydrological conditions in marl prairie wetlands of Everglades National Park, USA

Environmental conditions influence crustacean growth by affecting molt intervals and incremental increases in length and weight. In the seasonally-flooded marl prairie wetlands of eastern Everglades National Park, U.S.A., hydropattern exerts considerable influence on aquatic primary productivity, and so may influence the availability of food resources for higher trophic levels. The seasonal hydroperiod has been drastically altered by anthropogenic factors, but the impacts on the aquatic community are not well known. We studied whether differences in growth of crayfish Procambarus alleni could be detected in habitats with different hydroperiods. We first described growth patterns based on incremental increases in length and weight of crayfish on a high protein diet in the laboratory. Regression analyses indicated that growth patterns in males and females were similar. Although the intermolt period increased with age, the proportional increases in length and weight were similar through successive molts. The relationship between length and weight of crayfish was best described by a power equation for allometric growth. We then compared growth curves for crayfish subpopulations from different areas of the marl prairie. In habitats with the longest hydroperiods, crayfish weight-at-size was not significantly different from that in laboratory crayfish on the high protein diet. However, weight gain per unit increase in length in short hydroperiod sites was significantly less than in long hydroperiod sites or in the laboratory. These results indicate that crayfish productivity may be associated with hydroperiod in these stressed wetlands, and this may contribute to observed source-sink population regulation.