Orconectes Virilis Research Articles

Data for “Invasive virile crayfish (Faxonius virilis Hagen, 1870) hybridizes with native spothanded crayfish (Faxonius punctimanus Creaser, 1933) in the Current River watershed of Missouri, U.S.”

Data for “Invasive virile crayfish (Faxonius virilis Hagen, 1870) hybridizes with native spothanded crayfish (Faxonius punctimanus Creaser, 1933) in the Current River watershed of Missouri, U.S.”

Invasive virile crayfish (Faxonius virilis Hagen, 1870) hybridizes with native spothanded crayfish (Faxonius punctimanus Creaser, 1933) in the Current River watershed of Missouri, U.S.

Invasive virile crayfish (Faxonius virilis Hagen, 1870) hybridizes with native spothanded crayfish (Faxonius punctimanus Creaser, 1933) in the Current River watershed of Missouri, U.S.

Crayfish tissue metabolomes effectively distinguish impacts of wastewater and agriculture in aquatic ecosystems

Environmental metabolomics has been proposed as a tool for biomonitoring because organisms regulate production or consumption of metabolites in response to environmental conditions. We evaluated the efficacy of the metabolome of three tissues (hepatopancreas, gill, and tail muscle) from the northern crayfish (Faxonius virilis) to detect and differentiate between impacts of human activities (i.e., reference, municipal wastewater, and agriculture). We conducted a reciprocal transfer study exposing crayfish for 1 or 2 weeks in three streams with different amounts and types of human activities in southern Manitoba, Canada. Tissue samples were analyzed using nuclear magnetic resonance spectroscopy to generate a metabolic profile. Findings indicated the gill tissue metabolome best detected and differentiated between human activities. In particular, the gill metabolome was able to rapidly integrate abrupt changes in environmental conditions associated with municipal wastewater activity. In contrast, the tail metabolome best differentiated between crayfish collected at the reference site from those collected at the two impacted sites. Metabolites extracted from hepatopancreas tissue showed limited and inconsistent detection of among site differences. Based on our findings, we conclude that the metabolome of the northern crayfish can be an effective biomonitoring tool, but monitoring purpose will dictate tissue selection. Indeed, we recommend the gill metabolome be used for short-term assays aimed at detecting acute effects, whereas the tail be applied for survey monitoring aimed at detecting deviations in ecological condition at test sites from reference site conditions.

DESS deconstructed: Is EDTA solely responsible for protection of high molecular weight DNA in this common tissue preservative?

DESS is a formulation widely used to preserve DNA in biological tissue samples. Although it contains three ingredients, dimethyl sulfoxide (DMSO), ethylenediaminetetraacetic acid (EDTA) and sodium chloride (NaCl), it is frequently referred to as a DMSO-based preservative. The effectiveness of DESS has been confirmed for a variety of taxa and tissues, however, to our knowledge, the contributions of each component of DESS to DNA preservation have not been evaluated. To address this question, we stored tissues of three aquatic taxa, Mytilus edulis (blue mussel), Faxonius virilis (virile crayfish) and Alitta virens (clam worm) in DESS, each component of DESS individually and solutions containing all combinations of two components of DESS. After storage at room temperature for intervals ranging from one day to six months, we extracted DNA from each tissue and measured the percentage of high molecular weight (HMW) DNA recovered (%R) and normalized HMW DNA yield (nY). Here, HMW DNA is defined as fragments >10 kb. For comparison, we also measured the %R and nY of HMW DNA from extracts of fresh tissues and those stored in 95% EtOH over the same time intervals. We found that in cases where DESS performed most effectively (yielding ≥ 20%R of HMW DNA), all solutions containing EDTA were as or more effective than DESS. Conversely, in cases where DESS performed more poorly, none of the six DESS-variant storage solutions provided better protection of HMW DNA than DESS. Moreover, for all taxa and storage intervals longer than one day, tissues stored in solutions containing DMSO alone, NaCl alone or DMSO and NaCl in combination resulted in %R and nY of HMW DNA significantly lower than those of fresh tissues. These results indicate that for the taxa, solutions and time intervals examined, only EDTA contributed directly to preservation of high molecular weight DNA.

Sex Differences in Offensive and Defensive Investment in Crayfish Claws

Many animals possess weapons that have evolved to inflict damage to opponents during territorial encounters. Although the offensive capabilities of these weapons are important determinants of contest success, the defensive capabilities of the weapons are also important. However, current theory only accounts for investment into offensive performance, and not defensive endurance. To help better understand these dynamics, we investigated claw strength, cuticle thickness, and injury rates in male and female virile crayfish (Faxonius virilis). To measure the offensive capacity of a claw, we collected the max pinch of 3–5 pinches of each claw using a force transducer. To measure the defensive capacity of the claw, we dissected and measured the cuticle thickness of the carapace and seven sections of the claw: merus, dorsal manus, ventral manus, dorsal dactyl, ventral dactyl, dorsal pollex, and the ventral pollex. Injury rate was determined by visual inspection of the claw. Both male and female virile crayfish engage in aggression over access to both food and shelter. Thus, we expected each sex to invest similarly into the offensive and defensive abilities of their weapons. Interestingly, we found that despite males having proportionally larger claws, the average strength for a given size of the claw was similar between the sexes. Furthermore, we did not detect any sex differences in defensive ability as measured by cuticle thickness and injury rates. Overall, we demonstrated that both male and female virile crayfish invest similarly into the offensive and defensive ability of their claws.Support or Funding InformationNational Science Foundation (NSF) LEAP Scholars program

Virile crayfish escalate aggression according to body size instead of weapon size

Many crustaceans use their large claws to signal fighting ability during territorial contests. However, the size of a claw does not always reflect its strength or the bearer's ability to fight. If strength predicts the outcome of a fight, the mismatch between the size and strength of a claw creates dishonest signalling. Still, only a handful of species have been studied, leaving a gap in our knowledge of the taxonomic diversity and evolutionary history of dishonest signalling. To help fill this gap, we studied signalling and fighting between virile crayfish, Faxonius virilis. First, we measured the relationship between the size and strength of a claw in males and females. Then, we staged encounters between members of the same sex to determine how carapace length, claw size and claw strength influence the probability of fighting and the probability of winning. Both males and females possessed claws whose size poorly predicted their strength, especially at larger sizes. Unlike other species, which escalate aggression based on claw size, virile crayfish escalated aggression based on relative body size. When fighting occurred, however, both body size and claw strength determined the winner. Likely, virile crayfish ignore claw size because body size provides a more reliable signal of dominance. Our results stress the importance of observing behavioural dynamics in addition to functional relationships when studying the potential for dishonest signalling.

Behavioral responses of northern crayfish (Faxonius virilis) to conspecific alarm cues and predator cues from smallmouth bass (Micropterus dolomieu)

ABSTRACTWhile the ability for crayfish to detect visual and chemical cues is well documented, relatively few studies have probed the behavioral responses of crayfish to cues from key predators that they encounter in natural environments. Therefore, we examined how northern crayfish (Faxonius virilis) (Hagen 1870) responded to (1) alarm cues from conspecifics versus chemical cues from smallmouth bass (Micropterus dolomieu) (Lacepéde 1802), (2) varying concentrations of alarm cue from conspecifics, and lastly (3) smallmouth bass visual cues, chemical cues, and a combination of the two. We found that crayfish reduced walking activity in the presence of alarm cues. Chemical cues from smallmouth bass were also capable of eliciting a behavioral response, both alone and when paired with visual cues. Understanding the behavioral mechanisms by which crayfish respond to predatory fish is important to managing freshwater systems in the context of ongoing human- and climate-aided range expansions of both taxa.

Divergence in foraging and predator avoidance behavior across the geographic range of native and non-native crayfish

There is growing evidence that species’ traits may diverge during biological invasions; however, we still lack a general understanding of how the invasion process affects behavior. We used a biogeographic approach to compare foraging and antipredator behavior across a reciprocal invasion (in which each species invaded the native range of the other) of virile (Faxonius virilis) and rusty crayfish (F. rusticus). We hypothesized that the invasion process would select for individuals that invest more in foraging and less in defense than their native counterparts. We used laboratory experiments to examine crayfish boldness, activity, and foraging voracity and mesocosm experiments to examine antipredator behavior in response to fish. Non-native virile crayfish (Indiana, USA) were less bold, active and voracious than native virile crayfish (Wisconsin, USA), and they exhibited more antipredator behavior. Non-native rusty crayfish (Wisconsin) were more active in mesocosms and exhibited less antipredator behavior than native rusty crayfish (Indiana). Combined, these findings suggest a growth/mortality trade-off. Counter to our hypothesis, relative investment in foraging versus predator avoidance differed across regions and was not consistently associated with native or invasive populations. Thus, the substantial divergence in behavior we observed may by driven by local adaptation.

Effects of ontogeny and invasive crayfish on feeding ecology and mercury concentrations of predatory fishes

Lake food web structure dictates the flow of energy and contaminants to top predators, and addition of invasive species can shift these flows. We examined trophic position (TP), proportional reliance on the littoral zone (Proplittoral), and mercury (Hg) concentrations across the life-span of two predatory fishes, walleye (Sander vitreus) and northern pike (Esox lucius), in lakes with and without invasive virile crayfish (Faxonius virilis). The littoral zone was the dominant foraging zone for both species regardless of size, accounting for 59% and 80% of the diet of walleye and pike, respectively. Both species increased in TP and Hg with body size, as did crayfish. Walleye in crayfish-present lakes had lower Proplittoral, TP, and Hg concentrations compared with non-present lakes, but trophic magnification of Hg through the food web was consistent across all six lakes. These findings underscore a strong role for the littoral zone in channeling energy and contaminants to higher trophic levels and how invasive species can occupy new habitats at low abundance while altering food web structure and contaminant bioaccumulation.

Trophic status of a non-native crayfish in an oligotrophic lake: bottom-up view of a mixed warmwater and coldwater sport fishery food web

Loffredo JR, Moore BC, Lee RW, Katz SL, Cross BK. 2019. Trophic status of a non-native crayfish in an oligotrophic lake: Bottom-up view of a mixed warmwater and coldwater sport fishery food web. Lake Reserv Manage. 35:396–414.Numerous studies in recent decades have observed variable trophic status for freshwater crayfish among endemic and exotic populations in lentic or lotic habitats. In this study, we used stable isotope analyses (SIA) to explore trophic status of an introduced population of northern crayfish (Faxonius virilis) in Buffalo Lake, Washington. Northern crayfish are an important prey item for introduced warmwater and coldwater fish species in this lentic system and may buffer competitive interactions between largemouth bass (Micropterus salmoides), rainbow trout (Oncorhynchus mykiss), and kokanee (Oncorhynchus nerka). In 2017, the δ13C and δ15N values of liver samples from 208 crayfish informed proportional diet estimates. Crayfish diets were comprised of 8 littoral sources and were examined for cannibalism, temporal, spatial, and ontogenetic trophic shifts. There was no significant spatial or temporal trophic shift detected in this crayfish population. Seasonal δ15N values among all crayfish size classes mirrored seasonal abundance shifts of littoral macroinvertebrates. A multiple-source stable isotope mixing model and relative trophic positions provided evidence for an ontogenetic trophic shift between juvenile and adult crayfish, from a generalist detritivore to a predatory diet dominated by Chironomidae and Ephemeroptera. The trophic status of Buffalo Lake crayfish may affect salmonid management goals if interspecific competition for food between crayfish and sport fish is biologically significant. Our research is an important first step to understanding crayfish trophic status in a lentic food web, and should inform fish stocking regimes and fishery regulations in management efforts to achieve long-term sustainability of this diverse fishery.

Survival, behaviour, and morphology of larval wood frogs, Lithobates sylvaticus, under threat from an exotic crayfish predator, Orconectes virilis

There are numerous examples of species introductions that have caused declines in native populations. In many cases, exotic species are predators of native prey which do not respond correctly to these new and often much different threats. Amphibians, as a group, have been strongly affected by introductions of fish and other aquatic predators such as crayfish. Our goal in this study was to explore the potential impacts of exotic crayfish on the behaviour, morphology, and survival of naive wood frog tadpoles, Lithobates sylvaticus. In mesocosms, groups of tadpoles were exposed to either a native predator (larval beetle or dragonfly nymph) or an exotic crayfish, Orconectes virilis. Tadpoles were the largest following exposure to dragonflies, indicating that dragonflies were selecting smaller tadpoles. Vertical space use of tadpoles was highest in the presence of crayfish, suggesting that tadpoles were learning to avoid crayfish in the benthos. Mortality was highest in the presence of beetles and lowest with crayfish, and hence in isolation, exotic crayfish were poorer predators of wood frog tadpoles. However, half way through the experiment, we replaced each predator with a new predator of either the same species or a different species to assess how the impact of the new predator was affected by experience with the first predator. When crayfish were added following beetles, the mortality due to crayfish increased significantly, possibly due to differences in predator space use and foraging mode.

Distribution, habitat associations, and conservation status updates for the pilose crayfish Pacifastacus gambelii (Girard, 1852) and Snake River pilose crayfish Pacifastacus connectens (Faxon, 1914) of the western United States.

Our study evaluates the distribution, habitat associations, and current conservation status of the Snake River pilose crayfish Pacifastacus connectens (Faxon, 1914) and pilose crayfish Pacifastacus gambelii (Girard, 1852), two little-studied and data-deficient species endemic to the western United States. We first developed a species distribution model (SDM) for the pilose crayfishes based on their historical occurrence records using boosted regression trees and freshwater GIS data layers. We then sampled 163 sites in the summers of 2016 and 2017 within the distribution of these crayfishes, including 50 where these species were observed historically. We next compared our field results to modeled predictions of suitable habitat from the SDM. Our SDM predicted 73 sites (45%) we sampled as suitable for the pilose crayfishes, with a moderate AUC value of 0.824. The pilose crayfishes were generally predicted to occur in larger streams and rivers with less extreme upstream temperature and precipitation seasonality. We found the pilose crayfishes at only 20 (12%) of the 163 total sites we sampled, 14 (20%) of the 73 sites predicted as suitable for them by our SDM, and 12 (24%) of 50 historical sites that we sampled. We found the invasive virile crayfish Faxonius virilis (Hagen, 1870) at 22 sites total and 12 (24%) historical sites for the pilose crayfishes, and we found the “native invader” signal crayfish Pacifastacus leniusculus (Dana, 1852) at 29 sites total and 6 (12%) historical sites for the pilose crayfishes. We subsequently used a single classification tree to identify factors associated with our high rate of false positives for contemporary pilose crayfish distributions relative to our SDM. This classification tree identified the presence of invasive crayfishes, impairment of the benthic community, and sampling method as some of the factors differentiating false positives relative to true positives for the pilose crayfishes. Our study identified the historical distribution and habitat associations for P. connectens and P. gambelii using an SDM and contrasted this prediction to results of contemporary field sampling. We found that the pilose crayfishes have seemingly experienced substantial range declines, attributable to apparent displacement by invasive crayfishes and impairment or change to stream communities and habitat. We recommend increased conservation and management attention to P. connectens and P. gambelii in response to these findings.

Biogeographic differences between native and non-native populations of crayfish alter species coexistence and trophic interactions in mesocosms

Biogeographical comparisons of native and non-native populations allow researchers to understand the degree to which traits contributing to invasion success are intrinsic or change during the invasion process. Here, we investigate whether traits underlying interspecific competition change following invasion and whether these alter the impacts of two crayfish congeners that have invaded into each other’s native ranges. Specifically, we compared native and non-native populations of rusty (Faxonius rusticus) and virile crayfish (F. virilis). We compared native and non-native populations of each species using laboratory assays to examine aggression and large mesocosms with the congeners in sympatry to examine growth and survival as well as impacts on lower trophic levels. We found that non-native virile crayfish were more aggressive in response to a threat than native virile crayfish and exhibited greater growth and survival in sympatry with rusty crayfish. These intraspecific differences were large enough to alter coexistence between species in the mesocosm experiment, which is consistent with patterns of coexistence between these species in the field. We did not observe differences in traits between native and non-native rusty crayfish, but rusty crayfish were consistently competitively dominant over virile crayfish in paired laboratory assays. Non-native populations of both species had greater impacts on lower trophic levels than native populations. Taken together, these findings provide new evidence that trait changes during invasions may enhance ecological impacts of invasive animals and their ability to compete with closely related native species.

Transmission and terrestrial dispersal of non-native ectosymbionts on invasive crayfish

Symbionts are a fundamental component of biological systems, and their survival is highly dependent on transmission and host movement. Ectosymbionts of amphibious animals face the added challenge of having to survive dramatic environmental changes as their hosts cross ecosystem boundaries. Within freshwaters, crayfish are amongst the most widespread invasive species that readily disperse overland and are host to a wide range of ectosymbionts. Relatively little is known about the transmission of these ectosymbionts, including their ability to survive overland host migration. Here, we assessed terrestrial emigration and both inter- and intra-specific transmissions of Xironogiton victoriensis, a non-native branchiobdellidan (Annelida: Clitellata) recently found on invasive signal crayfish (Pacifastacus leniusculus) in the UK. These branchiobdellidans tolerated desiccation and did not alter host terrestrial behaviour. Transmission was rapid between natural signal and novel virile (Orconectes cf. virilis) crayfish hosts, with host interactions facilitating transmission. Thus, branchiobdellidans can disperse via amphibious host behaviour and readily infect novel hosts. These traits facilitate symbionts’ survival and provide access to additional dispersal pathways that are likely to aid transmission.

The influence of lake attributes and predatory bass on the distribution of northern crayfish (Orconectes virilis) in central New Hampshire

Introduced species influence the dynamics and structure of freshwater systems; understanding the variables that shape introduced species’ distributions can aid in anticipating their spread. We examined multiple factors that may influence the distribution of northern crayfish (Orconectes virilis (Hagen, 1870)), an introduced species, in New Hampshire, USA. Sampling occurred July to August 2010 in 20 lakes. We tested catch per unit effort (CPUE) and body size of crayfish against lake trophic status, size, depth, and shoreline development, as well as substrate type. We also compared CPUE and body size in the presence or absence of known predators, smallmouth bass (Micropterus dolomieu Lacepède, 1802) and largemouth bass (Micropterus salmoides (Lacepède, 1802)). Crayfish body size was not strongly associated with any tested variables, nor were there significant correlations between lake-level parameters and CPUE. CPUE increased with rocky substrates and decreased with macrophyte cover. We also found significantly lower CPUE in lakes with bass predators; this could be due to consumptive effects directly lowering crayfish abundance, nonconsumptive effects of bass on crayfish behavior, or both. Our work provides a baseline for future surveys examining northern crayfish or bass expansion in New Hampshire and highlights a variable that could be important as this crayfish colonizes additional locations outside its native range.

MicroRNAs regulate survival in oxygen-deprived environments

Some animals must endure prolonged periods of oxygen deprivation to survive. One such extreme model is the northern crayfish (Orconectes virilis), that regularly survives year-round hypoxic and anoxic stresses in its warm stagnant summer waters and in its cold, ice-locked winter waters. To elucidate the molecular underpinnings of anoxia resistance in this natural model, we surveyed the expression profiles of 76 highly conserved microRNAs in crayfish hepatopancreas and tail muscle from normoxic, acute 2 h anoxia, and chronic 20 h anoxia exposures. MicroRNAs are known to regulate a diverse array of cellular functions required for environmental stress adaptations, and here we explored their role in anoxia tolerance. The tissue-specific anoxia responses observed herein, with 22 anoxia-responsive microRNAs in the hepatopancreas and only four in muscle, suggest that microRNAs facilitate a reprioritization of resources to preserve crucial organ functions. Bioinformatic microRNA target enrichment analysis predicted that the anoxia-downregulated microRNAs in hepatopancreas targeted Hippo signalling, suggesting that cell proliferation and apoptotic signalling are highly regulated in this liver-like organ during anoxia. Compellingly, miR-125-5p, miR-33-5p and miR-190-5p, all known to target the master regulator of oxygen deprivation responses HIF1 (hypoxia inducible factor-1), were anoxia downregulated in the hepatopancreas. The anoxia-increased transcript levels of the oxygen-dependent subunit HIF1α highlight a potential critical role for miRNA-HIF targeting in facilitating a successful anoxia response. Studying the cytoprotective mechanisms in place to protect against the challenges associated with surviving in oxygen-poor environments is critical to elucidating the vast and substantial role of microRNAs in the regulation of metabolism and stress in aquatic invertebrates.

New records of the non-native virile crayfish Faxonius virilis (Hagen, 1870) from the upper Snake River drainage and northern Bonneville Basin of the western United States

New records of the non-native virile crayfish Faxonius virilis (Hagen, 1870) from the upper Snake River drainage and northern Bonneville Basin of the western United States

Predator recognition of chemical cues in crayfish: diet and experience influence the ability to detect predation threats

Abstract Aquatic prey often alter their morphology, physiology, and/or behaviour when presented with predatory chemical cues which are heavily influenced by the diet of the predator. We tested the roles that diet and prey familiarity with predators play in the ability of prey to recognize predator threats. Odours from two fish, bass and cichlid fed a vegetarian, protein, heterospecific, and a conspecific diet, were collected and presented to virile crayfish in a choice arena. Our results show that crayfish altered their behaviour in the presence of odours containing conspecific, as opposed to heterospecific diets, but only from familiar predators. A reduced anti-predator response was measured with odours from an unfamiliar predator fed conspecific crayfish. Therefore, crayfish may be able to determine different threat levels based on the different dietary cues from a potential predator, but only when the prey have familiarity with the predators.

Simultaneous determination of UV-filters and estrogens in aquatic invertebrates by modified quick, easy, cheap, effective, rugged, and safe extraction and liquid chromatography tandem mass spectrometry

Ultraviolet-filters (UV-filters) and estrogens have attracted increased attention as contaminants of emerging concern (CECs) due to their widespread occurrence in the environment. Most of these CECs are hydrophobic and have the potential to accumulate in aquatic organisms. To date, co-analysis of UV-filters and estrogens has not been reported due, in part, to the complex environmental matrices. Here, a multi-residue method has been developed for simultaneous determination of five UV-filters and three estrogens in tissue from aquatic and marine organisms. The procedure involved a modified Quick, Easy, Cheap, Effective, Rugged, and Safe (QuEChERS) extraction with a novel reverse-solid-phase extraction (reverse-SPE) cleanup in place of dispersive-SPE, followed by liquid chromatography tandem mass spectrometry (LC–MS/MS) analysis. The tissue mass, acetonitrile content, and salt conditions for QuEChERS extraction, along with the reverse-SPE cartridge material and elution conditions, were thoroughly investigated and optimized. Five UV-filters (i.e., 3-(4-methylbenzylidene) camphor, benzophenone-3, ethylhexylmethoxycinnamate, homosalate, and octocrylene) and three estrogens (i.e., estrone, 17β-estradiol, and 17α-ethinylestradiol) were simultaneously analyzed by taking advantage of wrong-way-round ionization in LC–MS/MS. The optimized analytical protocol exhibited good recoveries (>80%) for target compounds and enabled their detection at concentrations as low as 0.2ng/g in 50mg tissue samples. The method was applied to determine concentrations of target analytes in four invertebrates (i.e., Orconectes virilis, Procambarus clarkii, Crassostrea virginica, and Ischadium recurvum). All eight target analytes were detected at least once in the tissue samples, with the highest concentration being 399ng/g of homosalate in O. virilis. These results highlight the ubiquitous bioaccumulation of CECs in aquatic and marine invertebrates.

Invasive dreissenid mussels benefit invasive crayfish but not native crayfish in the Laurentian Great Lakes

Invasive ecosystem engineers, such as dreissenid mussels, may facilitate subsequent invaders. Despite their potential ecological importance, interactions between dreissenid mussels and crayfish in the Laurentian Great Lakes have received little research attention. Invasive rusty crayfish (Orconectes rusticus) have recently spread within the Great Lakes, and we hypothesized that food resources provided by invasive dreissenid mussels may have enhanced this spread. Dreissenid mussels may also benefit native crayfish such as the virile crayfish (O. virilis), but the distribution of virile species has not increased in the Great Lakes in recent years. We tested the interactive effects of dreissenid mussels and crayfish density on the growth, survival and activity of sympatric rusty and virile crayfish using a mesocosm experiment. We found that dreissenid mussels increased growth and activity of rusty crayfish while high crayfish densities negatively affected rusty crayfish growth. Dreissenid mussels did not affect growth or activity of virile crayfish, but high crayfish densities negatively affected their survival. The different responses of rusty and virile crayfish to mussels may be due to a greater ability of invasive crayfish to exploit mussel-associated food resources and/or to behavioral interactions between these species in sympatry. Our results suggest that dreissenid mussels may facilitate the establishment, spread, and potential impacts of invasive crayfish where these taxa co-occur.