Circadian rhythm does not affect responses to chemical cues in the red swamp crayfish, Procambarus clarkii

Studies of crayfish chemical ecology have been conducted in both day and night conditions. This variation may hinder the comparison of data among studies, if the responses by crayfish to chemical cues are dependent upon the time at which the cues are encountered. We tested the hypothesis that responses to chemical cues are dependent on observation time using the red swamp crayfish, Procambarus clarkii. Procambarus clarkii is known to exhibit a light-regulated circadian rhythm, with nocturnal activity peaks. Habitat use differed significantly between non-stimulated periods and periods of exposure to a food stimulus, but no effects of photoperiod (normal vs. reversed) or laboratory conditions (dark vs. light) were observed. The results suggest that, all else being equal, (1) studies of crayfish chemical ecology can be successfully conducted in a variety of experimental conditions, and (2) previous studies conducted at various times of the day should have comparable results.     

Snail responses to cues produced by an invasive decapod predator

Abstract. Cues released by predators and injured prey often induce shifts in prey behavior that allow prey to evade predators, but also affect prey resource use. I investigated the effects of chemical and mechanical signals produced by injured snails (Physella gyrina) and predatory crayfish (Procambarus clarkii) on microdistributions of P. gyrina. In an initial experiment, I observed snail responses to the presence of a caged crayfish predator, to injured conspecifics, or to both. There were significant effects of time and the treatment × time interaction on the proportion of snails moving above the water line, with greater proportions of snails above the water line at night than during the day and with weak snail crawl‐out behavior being elicited by caged crayfish at night, but not during the day. In a second experiment, I examined snail microdistributions when exposed to crayfish confined to a small cage within each aquarium, crayfish confined to half of each aquarium, and crayfish ranging freely throughout each aquarium. Snails responded most strongly to free‐ranging crayfish by moving above the water line, but also demonstrated significant, but reduced, crawl‐out responses to crayfish confined to half of each aquarium; however, snails did not respond behaviorally to crayfish confined to small cages. In both experiments, there were marginally significant effects of unfed caged crayfish on the proportions of snail populations hiding under benthic shelters, with this response being the strongest at the start of the experiments but weak overall (with only 4–5% of P. gyrina responding in each experiment). These results indicate that cues (e.g., chemical or mechanical) produced by predators altered prey microdistributions, but that the exact prey responses (e.g., moving above the water line or into horizontal or benthic refugia) depended on the intensity and nature of cues.     

Embryonic and larval defensive responses of agile frog (Rana dalmatina) to alien crayfish

Red swamp crayfish Procambarus clarkii, a widespread invasive alien crayfish, represents a serious threat for several freshwater species, including amphibians, which are declining at a global scale. As a shared coevolutionary history is the main factor determining the emergence of antipredator responses, Anuran tadpoles may not be able to cope effectively with this introduced predator. We performed two experiments to assess agile frog's (Rana dalmatina) defensive responses to both P. clarkii and native dragonfly larvae (Anax imperator). First, we conditioned embryos (collected from two ponds 30 km away from each other) with predators’ chemical cues to explore possible variation in hatching time caused by predation risk. In the second experiment, to evaluate how predators’ diet affects tadpole behavior, we conditioned tadpoles for a 5‐week period with cues from tadpole‐fed and gammarid‐fed predators and recorded behavioral and morphological responses. Embryos did not alter hatching time in the presence of any predator cue, while tadpoles from both populations strongly reduced activity and visibility when raised in the presence of tadpole‐fed dragonfly larvae. Morphological changes were less straightforward and were induced only in one population, for which broader tails and a slight increase in body size of tadpoles exposed to tadpole‐fed predators were observed. The lack of defensive responses in crayfish‐exposed tadpoles suggests that the spreading of this invasive species in agricultural lowlands of northern Italy may represent a further threat to their conservation.     

Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study

Antipredator behaviour is an important fitness component in most animals. A co-evolutionary history between predator and prey is important for prey to respond adaptively to predation threats. When non-native predator species invade new areas, native prey may not recognise them or may lack effective antipredator defences. However, responses to novel predators can be facilitated by chemical cues from the predators’ diet. The red swamp crayfish Procambarus clarkii is a widespread invasive predator in the Southwest of the Iberian Peninsula, where it preys upon native anuran tadpoles. In a laboratory experiment we studied behavioural antipredator defences (alterations in activity level and spatial avoidance of predator) of nine anurans in response to P. clarkii chemical cues, and compared them with the defences towards a native predator, the larval dragonfly Aeshna sp. To investigate how chemical cues from consumed conspecifics shape the responses, we raised tadpoles with either a tadpole-fed or starved crayfish, or dragonfly larva, or in the absence of a predator. Five species significantly altered their behaviour in the presence of crayfish, and this was largely mediated by chemical cues from consumed conspecifics. In the presence of dragonflies, most species exhibited behavioural defences and often these did not require the presence of cues from predation events. Responding to cues from consumed conspecifics seems to be a critical factor in facilitating certain behavioural responses to novel exotic predators. This finding can be useful for predicting antipredator responses to invasive predators and help directing conservation efforts to the species at highest risk.     

淡水螯虾生理生态学与环境毒理学研究进展

综述了我国2种主养的淡水螯虾(克氏原螯虾和红螯螯虾)在生理生态学与环境毒理学方面的研究进展。总结了淡水螯虾的环境条件(盐度、温度和pH)适应范围、毒性污染物(氨氮、亚硝酸盐、重金属和农药等)的半致死浓度和安全浓度,以及环境胁迫和毒性污染物暴露对淡水螯虾生长、组织结构、生理代谢和免疫功能等的影响,为淡水螯虾养殖的水环境监测与调控提供参考依据。     

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.     

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.     

Comparison of Two Chemicals for Removing an Entocytherid (Ostracoda: Crustacea) Species from Its Host Crayfish (Cambaridae: Crustacea)

Entocytherids are epifauna on larger crustaceans. We assessed the effectiveness of chlorobutanol and carbonated water for removing entocytherid, Ankylocythere sinuosa, from crayfish, Procambarus clarkii. This was done using different exposure times and by assessing entocytherid and crayfish survival, together with the number of entocytherids removed. According to our results, chlorobutanol submersion of crayfishes in shorter time periods is more effective for removing entocytherids without killing the crayfish host. However, carbonated water submersion is better to extract larger amounts of living entocytherids. Finally, both chemicals are appropriate tools to establish standardised protocols for removing entocytherids from crayfish for ecological studies because the proportions of removed entocytherids per crayfish become constant whatever the entocytherid load of the crayfish. (© 2011 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

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.     

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.     

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.     

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.     

Crayfish learning abilities: how does familiarization period affect the capture rate of a new prey item?

This study explores the effect of the length of learning period on capture rate of a previously unfamiliar prey by an invasive freshwater crayfish (Procambarus clarkii). Juvenile crayfish were subjected to different periods of contact (learning period) with a larvae prey (Chaoborus sp.). The length of the learning period significantly affected the number of prey consumed by the predator. Our results indicate that the naive crayfish require less than 12 h to learn to maximize capture rate of this prey. The learning coefficient, adopted in the present study, may be useful in exploring predation capabilities of alien species in newly invaded habitats.     

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.     

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.

     

Role of the olfactory pathway in agonistic behavior of crayfish, <Emphasis Type="Italic">Procambarus clarkii</Emphasis>

Crayfish establish social dominance hierarchies through agonistic interactions, and these hierarchies are maintained through assessment of social status. Chemical signals influence several aspects of fighting behavior, but the specific chemosensory sensilla involved in detecting these signals in crayfish are unknown. The goal of our study was to examine the importance of aesthetasc sensilla—olfactory sensors on the antennules of decapod crustaceans—in regulating changes in fighting behavior in crayfish, Procambarus clarkii, over the course of repeated pairings. We selectively ablated aesthetascs from pairs of crayfish after the first day of trials and compared the behavior of these ablated animals to that of pairs of intact controls. Results show that unablated crayfish significantly decreased the number and duration of fights over repeated pairings, whereas crayfish lacking aesthetascs continued to engage in similar amounts of fighting across all three trial days. This difference shows that aesthetascs regulate fighting behavior in P. clarkii.     

The smell of danger: chemical recognition of fish predators by the invasive crayfish Procambarus clarkii

1. Since avoiding predation can compromise animal fitness, prey are expected to respond to different predator species with an intensity appropriate to the level of risk. In fresh waters, the threat of predation is typically assessed by chemical cues, in particular by odours released by either injured/disturbed conspecifics (conspecific alarm odour) or predators (predator odours). Here, we used the most widely distributed crayfish in the world, the invasive North American Procambarus clarkii, to investigate the relative effectiveness of odours emitted by fish predators compared with conspecific alarm odour. We also tested whether P. clarkii is able to discriminate between fish predators of which it has ‘experience’ (either recent, via introduction to the same water body, or old, by sharing a native range), as well as between fish predators that pose low or high risk. 2. The study was carried out on introduced populations of P. clarkii from two sites, characterised by different fish assemblages: the Malewa River (a tributary of Lake Naivasha, Kenya) and Lake Trasimeno (Italy). Laboratory experiments consisted of three sequential phases (‘water’, ‘food’ and ‘smell’ phases) and five treatments. Treatments differed in the odour presented during the smell phase, i.e. no odour (plain water) and odours from either injured conspecifics or three fish species per site. Crayfish from the Malewa River population were confronted with the odours of largemouth bass (Micropterus salmoides), common carp (Cyprinus carpio) and tilapia (Tilapia zillii) (all introduced to Lake Naivasha but absent from the Malewa River), and those from the Lake Trasimeno population with the odours of the introduced largemouth bass and carp and the native chub (Squalius cephalus). Largemouth bass is the only predator that imposes a high risk to crayfish, and it also shares its native range with P. clarkii. We analysed the time spent by crayfish feeding, in locomotion and in adopting a raised or lowered posture. A reduction in the time spent feeding and in locomotion, and an increase in the time spent in the lowered posture were considered to indicate alarm. 3. Crayfish from both populations responded with a more pronounced reduction in feeding to conspecific alarm odour rather than to predator odours. Crayfish from the Malewa River reacted with the same intensity to the odours of the three fish species tested, whereas, in Lake Trasimeno, the odour of largemouth bass was significantly more threatening than the odours of the other two species. 4. Procambarus clarkii seems to perceive a general fish odour that alerts it to possible predation risk without the need of either a direct recent experience or via sharing a common native range. However, where they coexist with fish, crayfish become able to distinguish among species, adapting the intensity of their response to the effective risk. Our results confirm the relatively high learning capacity of P. clarkii reported in previous studies and suggest the existence of mechanisms that make predator recognition particularly efficient in this extraordinarily successful 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.     

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.     

Predatory Efficiency of Crayfish: Comparison Between Indigenous and Non-Indigenous Species

The invasive crayfish Procambarus clarkii is highly dispersed within lentic waters in northern and central Italy. It is a polytrophic predator, exerting a strong influence on animal communities, including amphibians, fish, gastropods, and insect larvae. The indigenous species Austropotamobius italicus, inhabiting lotic waters, behaves as a generalist – but not opportunistic – species. The object of this study was to compare the predatory pressure exercised by the two species on potential prey, i.e., anuran tadpoles, urodelan larvae, fish fry, larvae of insects, and gastropods. Three main conclusions were drawn: (1) both species are skilled predators, adopting a sit-and-wait strategy, (2) the two crayfish seemed to form a `search image' of familiar prey, as the result of either visual or chemical perceptual changes, and (3) at least in the laboratory, P. clarkii readily switched to naive prey for it (tadpoles of Rana italica and larvae of Limnephilidae), unlike the less opportunistic A. italicus. These results furnish suggestions on the trophic preferences of the two crayfish species and provide a partial understanding of the effects that the invasive species have on the community dynamics. This revised version was published online in July 2006 with corrections to the Cover Date.