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.     

Crayfish effects on seeds and seedlings: identification and quantification of damage

1. The red‐swamp crayfish (Procambarus clarkii) is an invasive species and an important pest of wet‐seeded rice fields (Oryza sativa) in California (U.S.A.) and in Portugal. Our work quantifies rice consumption and non‐consumptive destruction and identifies the types of direct damage inflicted by crayfish. 2. The following fractions were quantified in the presence and absence of crayfish and at 3 and 6 days of rice development: (1) non‐germinated seeds, (2) damaged seeds, (3) seeds not recovered, (4) intact rooted seedlings, (5) rooted damaged seedlings, (6) uprooted intact seedlings, (7) uprooted damaged seedlings. 3. Coarse particulate organic matter (CPOM) fragments produced during the feeding process were <2% of the material removed by crayfish. 4. Damage occurred with or without uprooting of the plants, but the incidence of uprooting without consumption was low (1.4%). 5. Consumption of recently developed parts of the rice plant was the main cause of damage and the observed effect was stronger on 6‐day‐old than on 3‐day‐old seedlings. Seedlings were more affected by crayfish than were seeds. 6. Crayfish affected the majority of seeds and seedlings available although consumption was low: 0.015 g dry weight (DW) rice g^?1 wet weight (WW) crayfish per 12 h at 3 days and 0.063 g DW rice g^?1 WW crayfish per 12 h at 6 days. 7. Our results are important for the mitigation of crayfish related problems in rice fields and for understanding the mechanisms of crayfish‐macrophyte interactions.     

Burrowing activity of Procambarus clarkii on levees: analysing behaviour and burrow structure

The North American crayfish Procambarus clarkii is considered among the most invasive freshwater species. However, burrowing behaviour and the possible impact of P. clarkii on levees have not yet been studied in depth. To assess shape, volume and structure of its burrows and the associated behaviour, experiments were conducted introducing two size-matched adult crayfish into an artificial setup and video-recording their behaviour for 96 h. At the end of each replicate, casts of excavated burrows made with polyethylene foam were retrieved. Crayfish (n?=?40) dug 17 burrows, six of which having an enlarged terminal chamber. The average excavated levee volume of burrows was 1.9% (0.00528 m³; 5.0256 l)?±?0.86% of the total volume with a maximum of 4% (0.0109 m³; 10.9 l) and the chambers (mean volume of 0.9?±?0.6 dm³) contributed to up to 50% of the excavated volume. No significant difference between sexes was found for any observed behaviour. Our study also demonstrated how P. clarkii female and male behaviours are similar for burrowing activity. As a result, we quantify the potential pressure exerted by the red swamp crayfish on levees and lastly highlight the observation of cooperating burrowing behaviour of male and female individuals in this species.

     

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 effects of serotonin and octopamine on behavioral arousal in the crayfish

1. In the crayfish, behavioral arousal is known to elicit walking and to enhance compensatory eye movements.2. To see if serotonin and octopamine modulate arousal, we measured their effects on walking and eye movements in tethered crayfish, Procambarus clarkii. Serotonin strongly suppresses both walking and eye movements.3. In contrast, octopamine elicits an arousal-like state of continuous jittery leg movements and increased eye movements.4. Serotonin's effect on arousal is uncertain, but octopamine remains a plausible modulator of behavioral arousal.     

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.     

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.     

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.     

How consumption and fragmentation of macrophytes by the invasive crayfish Procambarus clarkii shape the macrophyte communities of temporary ponds

Crayfish are major herbivores in freshwaters, and their activity may change invaded freshwater ecosystems. Macrophyte removal by crayfish results from consumption and fragmentation of plant material and may depend upon the palatability of each species. We studied the impact of Procambarus clarkii on the macrophyte community of Mediterranean temporary ponds, testing in laboratory if consumption and fragmentation of five macrophyte species were correlated in palatability tests and in a preference test. We performed an experiment in a natural pond, where we introduced crayfish and estimated its effects on macrophyte biomass, number of rooted stalks and number of floating cut stalks. P. clarkii consumed preferably Juncus heterophyllus in both tests and avoided Carex divisa and Ranunculus peltatus in the preference test. In the presence of preferred species, consumption and fragmentation of the non-preferred species were heavily reduced. In the field trial, the “Crayfish” compartment had 31% less macrophyte biomass, 41% less rooted stalks and 92% more floating cut stalks. Crayfish may remove macrophyte species from the community sequentially, from the most to the least preferred species. Impacts of crayfish in temporary ponds may depend on time of invasion and on the composition of the macrophyte community.     

PHOTOPERIODIC INDUCTION OF OVARIAN MATURATION IN CRAYFISH PROCAMBARUS CLARKII IS MEDIATED BY EXTRARETINAL PHOTORECEPTION

The current study was carried out to investigate whether thephotoperiodic induction of ovarian maturation in crayfish is based on a photosensitiverhythm related to extraretinal photoreceptors. To test this, two batches of61 juvenile crayfish Procambarus clarkiiconsisting of intact organisms and animals lacking retina and lamina were exposed to 24hlight-dark cycles of different photoperiodic schedules based on a night-breakprotocol for 3 months. Both batches of crayfish showed the greatest ovarianmaturation (size, color, degree and size of oocytes) when the light pulseinterrupted the scotophase at 21:00 and 05:00, showing a bimodal photoinduciblerhythm. Results of the current study indicate that crayfish ovarian maturationdepends on a photoinducible rhythm with two possible states that is relatedto the circadian clock of crayfish. This phenomenon is mediated by extraretinalphotoreceptors. Results are interpreted in the light of models of externalcoincidence. (Chronobiology International, 18(3),423–434, 2001)     

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.     

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.     

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.     

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.

     

Population dynamics of an epibiont Ostracoda on the invasive red swamp crayfish Procambarus clarkii in a western Mediterranean wetland

Recently, the American entocytherid ostracod Ankylocythere sinuosa was discovered for the first time in Europe to inhabit widely distributed populations of the invasive American crayfish Procambarus clarkii in the Iberian Peninsula. Based on this finding, the aim was to describe the population dynamics of exotic entocytherids for the first time beyond their original area, and to analyse the main variables modulating temporal demographic patterns. We monitored a population of A. sinuosa and its host, P. clarkii, in the Pego-Oliva wetland (Eastern Iberian Peninsula) monthly for 1 year. Crayfish entocytherid loads strongly related to crayfish weight, moult-related exoskeleton hardening stage and water temperature. The proportion of earliest juvenile entocytherid instars, an indicator of recent hatching periods, also related to water temperature and conductivity. According to our results, the most important factors affecting entocytherid dynamics are individual crayfish moulting events, which diminish ostracod load, together with water temperature and ionic concentration, both influencing the life cycle of the exotic epibiont ostracod A. sinuosa.     

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.     

The influence of Procambarus clarkii (Cambaridae,Decapoda) on water quality and sediment characteristics in a Spanish floodplain wetland

This study describes the effects of the American red swamp crayfish, Procambarus clarkii Girard, on water quality and sediment characteristics in the Spanish floodplain wetland, Las Tablas de Daimiel National Park. Our short term enclosure study during a summer drawdown revealed that crayfish acted as a nutrient pump that transformed and translocated sediment bound nutrients to the water column. Water quality impoverishment was mainly due to the increase of dissolved inorganic nutrients (soluble reactive phosphorus and ammonia), and a significant increase of total suspended solids occurred likely as a result of crayfish associated bioturbation. At the same time, crayfish reduced the content of organic matter in the sediment and we observed a slight increase of total sediment phosphorus and nitrogen content as a result of crayfish benthic activity. P. clarkii effects, in terms of internal nutrient loading (229.91 mg TP m^–2 d^–1), were shown to be important on a local scale, indicating the significance of internal nutrient supply to water column primary producers particularly under low external supply (summer). Extrapolations to the whole ecosystem, however, revealed a negligible crayfish contribution (0.06%) to total internal nutrient loading (0.035 mg TP m^–2 d^–1). Hence, crayfish spatial heterogeneity patterns are important in global and local matter fluxes and nutrient cycles in wetlands.     

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.     

Home-field advantage: native signal crayfish (Pacifastacus leniusculus) out consume newly introduced crayfishes for invasive Chinese mystery snail (Bellamya chinensis)

The introduction of non-indigenous plants, animals and pathogens is one of today’s most pressing environmental challenges. Freshwater ecologists are challenged to predict the potential consequences of species invasions because many ecosystems increasingly support novel assemblages of native and non-native species that are likely to interact in complex ways. In this study we evaluated how native signal crayfish (Pacifastacus leniusculus) and non-native red swamp crayfish (Procambarus clarkii) and northern crayfish (Orconectes virilis) utilize a novel prey resource: the non-native Chinese mystery snail (Bellamya chinensis). All species are widespread in the United States, as well as globally, and recent surveys have discovered them co-occurring in lakes of Washington State. A series of mesocosm experiments revealed that crayfish are able to consume B. chinensis, despite the snail’s large size, thick outer shell and trapdoor defense behaviour. Crayfish exhibited size-selective predation whereby consumption levels decreased with increasing snail size; a common pattern among decapod predators. Comparison of prey profitability curves—defined as the yield of food (weight of snail tissue) per second of feeding time (the time taken to crack the shell and consume the contents)—suggests that small and very large snails may represent the most profitable prey choice. By contrast, previous studies have reported the opposite pattern for crayfish consumption on thin-shelled snails. For all snail size classes, we found that native P. leniusculus and invasive O. virilis consumed greater numbers of snails than invasive P. clarkii. Moreover, P. leniusculus consistently handled and consumed snails at a faster pace compared to both invasive crayfishes across the range of snail sizes examined in our study. These results suggest not only that B. chinensis is a suitable food source for crayfish, but also that native P. leniusculus may ultimately out-consume invasive crayfishes for this new prey resource.     

Phoma glomerata, a potential new threat to Italian inland waters

Non-indigenous crayfish species, carrier of the oomycete Aphanomyces astaci, are the most important threats to European crayfish species. However, other ectoparasite species have been reported to be the pathogen of aquatic organisms. As little is known about other potential pathogens carried by the red swamp crayfish Procambarus clarkii, a total of 86 individuals of this species was collected in Lake Trasimeno from June 2007 to 2008. Phoma glomerata, never recorded in Italy, colonised more than 65% of the captured crayfish. No significant differences in prevalence were recorded between sexes, among life stages and between soft- and hard-shelled crayfish. This Coelomycetes is the causal agent of many diseases in plants, animals and humans. These results may contribute to a better understanding of the implications of epibiontic microfungi on the invasive crayfish P. clarkii, for both ecological and sanitary purposes.