The signal crayfish is not a single species: cryptic diversity and invasions in the Pacific Northwest range of Pacifastacus leniusculus

1. We used historical sources, morphology‐based taxonomy and mtDNA sequence data to address questions about the signal crayfish Pacifastacus leniusculus. These included evaluating unrecognised cryptic diversity and investigating the extent to which P. leniusculus may have been introduced within its presumed native range in the Pacific Northwest region of North America. Our study builds and expands on Pacific Northwest phylogeographic knowledge, particularly related to patterns of glacial refugia for freshwater species. 2. Extensive collections (824 specimens) from British Columbia (Canada), Idaho, Nevada, Oregon and Washington (United States) were used to characterise P. leniusculus at the mitochondrial 16S rRNA gene. Genetic groups within the species were elucidated by phylogenetics and amova ; evolutionary relationships within the most common and diverse group were investigated using a statistical parsimony haplotype network, a nested amova , and tests of isolation by distance. Morphological measurements were used to relate findings of molecular analyses to three historically recognised P. leniusculus subspecies and characterise cryptic diversity by morphology. 3. We found substantial cryptic diversity, with three groups highly distinct from P. leniusculus in discrete geographic regions: the Chehalis River glacial refugium, Central Oregon and the Okanagan Plateau. Disjunct distributions of P. leniusculus relative to these cryptic groups and known patterns of Pleistocene glaciation and landscape evolution cast doubt on whether P. leniusculus is native to some areas such as coastal drainages of northern Washington and southern British Columbia. Morphological traits previously used to characterise P. leniusculus subspecies still persist but may be incapable of distinguishing P. leniusculus from newly discovered cryptic groups. 4. Cryptic diversity found within P. leniusculus highlights the pressing need for a thorough investigation of the genus Pacifastacus using data based on more extensive gene and taxon sampling. It also warrants conservation attention, as introductions of P. leniusculus within the Pacific Northwest may carry risks of hybridisation and introgression for cryptic groups. Owing to high genetic diversity and limited dispersal capacity relative to more vagile organisms like freshwater fish, crayfish of the genus Pacifastacus offer powerful potential insights into the geological history and phylogeography of the Pacific Northwest region. Finally, by shedding light on the long‐neglected native range of P. leniusculus, our results should also better inform our understanding of potential source populations for, and the ecology of, this important invasive species in regions including Europe, Japan and elsewhere in North America.     

A symbiont's dispersal strategy: condition-dependent dispersal underlies predictable variation in direct transmission among hosts

Direct horizontal transmission of pathogenic and mutualistic symbionts has profound consequences for host and symbiont fitness alike. While the importance of contact rates for transmission is widely recognized, the processes that underlie variation in transmission during contact are rarely considered. Here, we took a symbiont''s perspective of transmission as a form of dispersal and adopted the concept of condition-dependent dispersal strategies from the study of free-living organisms to understand and predict variation in transmission in the cleaning symbiosis between crayfish and ectosymbiotic branchiobdellidan worms. Field study showed that symbiont reproductive success was correlated with host size and competition among worms for microhabitats. Laboratory experiments demonstrated high variability in transmission among host contacts. Moreover, symbionts were more likely to disperse when host size and competition for microhabitat created a fitness environment below a discrete minimum threshold. A predictive model based on a condition-dependent symbiont dispersal strategy correctly predicted transmission in 95% of experimental host encounters and the exact magnitude of transmission in 67%, both significantly better than predictions that assumed a fixed transmission rate. Our work provides a dispersal-based understanding of symbiont transmission and suggests adaptive symbiont dispersal strategies can explain variation in transmission dynamics and complex patterns of host infection.     

The first record of the non-indigenous signal crayfish <Emphasis Type="Italic">Pasifastacus leniusculus</Emphasis> in Norway

The non-indigenous signal crayfish Pasifastacus leniusculus was registered for the first time in Norway in October 2006. The location represents an isolated pond about 100 km in air line from the nearest known signal crayfish population in the neighbouring country Sweden without any connecting watercourses. The occurrence is therefore undoubtedly caused by human introduction. Molecular analyses confirmed that tested individuals from the signal crayfish population were carriers of the crayfish plague agent Aphanomyces astaci. Disease carrying signal crayfish represents a severe threat to the indigenous and endangered noble crayfish Astacus astacus. Norwegian authorities are currently considering actions for the eradication of the signal crayfish population.     

Stable isotopes, mesocosms and gut content analysis demonstrate trophic differences in two invasive decapod crustacea

1. Improving our understanding of dietary differences among omnivorous, benthic crustacea can help to define the scope of their trophic influence in benthic food webs. In this study, we examined the trophic ecology of two non‐native decapod crustaceans, the Chinese mitten crab (Eriocheir sinensis) (CMC) and the red swamp crayfish (Procambarus clarkii) (RSC), in the San Francisco Bay ecosystem to describe their food web impacts and explore whether these species are functionally equivalent in their impacts on aquatic benthic communities. 2. We used multiple methods to maximise resolution of the diet of these species, including N and C stable isotope analysis of field data, controlled feeding experiments to estimate isotopic fractionation, mesocosm experiments, and gut content analysis (GCA). 3. In experimental enclosures, both CMC and RSC caused significant declines in terrestrially derived plant detritus (P < 0.01) and algae (P < 0.02) relative to controls, and declines in densities of the caddisfly Gumaga nigricula by >50% relative to controls. 4. Plant material dominated gut contents of both species, but several sediment‐dwelling invertebrate taxa were also found. GCA and mesocosm results indicate that CMC feed predominantly on surface‐dwelling invertebrates, suggesting that trophic impacts of this species could include a shift in invertebrate community composition towards sediment‐dwelling taxa. 5. Stable isotope analysis supported a stronger relationship between CMC and both algae and algal‐associated invertebrates than with allochthonous plant materials, while RSC was more closely aligned with terrestrially derived detritus. 6. The trophic ecology and life histories of these two invasive species translate into important differences in potential impacts on aquatic food webs. Our results suggest that the CMC differs from the RSC in exerting new pressures on autochthonous food sources and shallow‐dwelling invertebrates. The crab's wide‐ranging foraging techniques, use of intertidal habitat, and migration out of freshwater at sexual maturity increases the distribution of the impacts of this important invasive species.     

Metabolic rate in the signal crayfish (Pacifastacus leniusculus) is temporally consistent and elevated at molting

Although the temporal consistency of resting metabolic rate in individual animals is generally considered to be a universal phenomenon, studies on invertebrates are still scarce. Here, we studied the repeatability of standard metabolic rate in the signal crayfish (Pacifastacus leniusculus). We measured oxygen consumption twice on the same individuals, on average in 97-day intervals. At intermolt stage, the standard metabolic rate was a repeatable trait. However, molting increased significantly the minimum metabolic rate, thus emphasizing the role of animal physiological state in determining the rate of metabolism.     

The impacts of flow on chemical communication strategies and fight dynamics of crayfish

Signal transmission is influenced by the physics of an environment. Consequently, a physical effect on sensory signals can influence how animals send or sample sensory information. Habitat-specific physics may constrain or enhance signal transmission (e.g. sound transmission in a flowing river versus a still pond) and provide a mechanism for the evolution of sensory biases. This study investigated how the transmission of chemically mediated social signals in crayfish is influenced by two different aquatic environments. Agonistic bouts between crayfish were performed under lotic (flowing water) and lentic (nonflowing, still water) conditions. When crayfish (Orconectes rusticus) collected from a lotic system (river) interacted under lotic conditions, we noted that dominant O. rusticus spent more time upstream than subordinate O. rusticus. Orconectes rusticus positioned themselves randomly and spent equal amounts of time with respect to upstream and downstream in the nonflowing environment. We tested another species, Orconectes virilis, collected from a nonflowing environment (lake) and they showed no positional preference when tested in flow. Additionally, both O. rusticus and O. virilis took longer to reach high fight intensities under flow conditions. It was possible to visualize O. rusticus urine release, and they released urine more often when upstream of an opponent in a flow environment during these agonistic bouts. These results suggest that O. rusticus collected from lotic environments release urine to maximize the transmission of chemical cues to a fight opponent. It appears that crayfish may adapt their signalling processes based upon their long-term ambient environments.     

Post-mating spermatophore storage strategies in two species of crayfish: implications for broodstock management

Female crayfish stores male gametes after mating until the beginning of egg laying and fertilization. The aim of the present study was to investigate the duration of post-mating spermatophore storage as well as the timing and temperature of spawning in two crayfish species of economic importance, namely the signal crayfish Pacifastacus leniusculus and the noble crayfish Astacus astacus. Results showed that the average duration of the post-mating spermatophore storage is significantly (P<0.05) longer in the noble crayfish (34.6±1.7 days, range: 19 to 60 days) than the signal crayfish (3.9±0.5 days, range: 1 to 18 days). The highest percentages of the post-mating spermatophore storage duration in the signal crayfish (46.5%) and the noble crayfish (44.5%) were 1 and 31 to 40 days, respectively. While there is an overlap in the timings of mating and egg laying in the signal crayfish, these two reproductive processes were not observed at the same days in the noble crayfish and there was at least 2 weeks interval between last mating and first egg laying individuals. Average mating and egg laying temperatures were significantly (P<0.05) higher in the signal crayfish than the noble crayfish. The average temperatures for mating in both species were significantly (P<0.05) higher than the temperatures that they utilized for egg laying. In conclusion, female noble crayfish stores post-mating spermatophores a longer duration compared with the signal crayfish. Also, the signal crayfish mates and lays egg in temperatures that are higher than the noble crayfish. Spawning season is shorter in the signal crayfish compared with the noble crayfish. The results of present study provide information contributing to the crayfish broodstock management in aquaculture.     

Commensalism or mutualism: conditional outcomes in a branchiobdellid–crayfish symbiosis

A growing body of evidence suggests that the costs and benefits involved in cleaning interactions can vary over space and time depending on the environmental conditions. However, whether the same cleaners actually induce variable net outcomes in terms of host fitness remains unclear to date. Branchiobdellid annelids are generally regarded as commensals or rarely parasites of their freshwater crayfish hosts, but a recent study suggests that they may also function as cleaning organisms. Under natural conditions, crayfish can experience fouling of the exposed surfaces of their exoskeletons and their gills (e.g., epibiosis) by various epibionts and particles of organic debris, and branchiobdellids graze on these sources of fouling. Here, we examined the extent to which variation in fouling pressure in the environment alters the outcome of the interaction between branchiobdellids and their crayfish host Cambaroide similis. A series of manipulations were performed in artificial environments designed to simulate either high or low fouling pressure. We used crayfish growth rates and mortality as direct measurements of the net costs and benefits of cleaning. Branchiobdellids had no significant effect on crayfish growth or mortality when cultured under low fouling pressure. However, their presence had a significant positive impact on host growth rates when cultured under high fouling pressure. These results suggest that the relationship between crayfish and branchiobdellids can fluctuate between commensalism and mutualism depending mainly on the environmental fouling pressure. We hypothesize that the outcome of cleaning interactions may largely depend on the factors directly related to the need for cleaning, such as parasite loads or fouling pressure.     

Linking phenotypic correlations from a diverse set of laboratory tests to field behaviors in the crayfish,Orconectes virilis

The presence of phenotypic behavioral correlations and their connection to fitness consequences of organisms have received considerable debate within the literature. Yet, little work has been carried out to connect any behavioral correlates found within a set of laboratory studies to natural behavior observed under complex environmental conditions. To help fill this gap, individual crayfish, collected from the same local population, completed five different behavioral assays in a laboratory setting in a random order. These data were used to reveal any possible correlations for behavioral scores across all of the laboratory tests. Subsequently, these same individuals were placed into the field and video recorded for 24 hr. A separate set of field behaviors, related to the laboratory assays, were quantified from the field videos. The normalized laboratory and field behaviors were used in three stepwise statistical analyses. First, normalized data were loaded into a PCA to generate a priori hypotheses on potential behavioral correlates. These hypotheses were subsequently tested using general multiple linear regression. Finally, structural equation modeling was performed to elucidate any behavioral modules from the laboratory assays that correlated with behavioral patterns present from the fieldwork. Three laboratory‐based behavioral modules were connected to three separate field assays: exploration–avoidance, bold–shy, and aggressiveness. Yet, some behaviors exhibited in the laboratory assays were uncorrelated with any behaviors found in the field and vice versa. Results from this study provide evidence that although many different behavioral correlates may exist within laboratory settings, these same modules may not translate directly into predicting behavior under natural settings.