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.     

Components of care: are they honest signals of parental care quality?

It has been argued that male parental care provides direct benefits to females and therefore should be under sexual selection. Given this, we expect signals that honestly indicate the quality of care to be favoured by selection. One such potential signal is care itself. Fish have several features that make them excellent model systems for studying the evolution and dynamics of parental care. We use the flagfish, Jordanella floridae , as a model to evaluate these general ideas. Males of this species guard, clean and fan empty nests and then eggs. Females prefer males that fan more (1) before spawning and (2) when eggs are newly received. When single males and females were paired, males that fanned and visited their nests more prior to spawning were more likely to be mated. Furthermore, among successful males, rates of fanning in the first day after spawning were correlated with the number of eggs received in the future (but not current egg numbers). We then considered whether these two putative signals were correlated and whether males that fan more in these contexts actually have higher egg survivorship. We found no correlation between nest fanning rates before and after spawning and neither 'signal' was predictive of variation in egg survivorship among mated males. We further considered whether pre‐spawning fanning rates were predictive of hatching success in an experiment in which single males were allowed to establish nests and provided eggs. We found little evidence that fanning is an honest signal of care quality and discuss alternative explanations. In particular, we discuss patterns of care elaboration in light of our results.     

The activity of signal crayfish (Pacifastacus leniusculus) in relation to thermal and hydraulic dynamics of an alluvial stream, UK

Signal crayfish (Pacifastacus leniusculus) are an invasive species of global significance because of their detrimental impacts on freshwater environments and native organisms. The movement of signal crayfish was continuously monitored for 150-days through a 20-m reach of an alluvial stream in the UK. Passive integrated transponder-tags were attached to crayfish, allowing their location to be monitored relative to 16 antennae which were buried beneath the river bed. The activity of crayfish was related to water depth and temperature, which were continuously monitored within the instrumented reach. Crayfish were highly nocturnal, with less than 6% of movements recorded during daylight hours. Activity declined from September and was minimal in November when water temperature was low and flow depth was high. However, relations between environmental parameters and crayfish activity had poor explanatory power which may partly reflect biological processes not accounted for in this study. Water depth and temperature had a limiting relationship with crayfish activity, quantified using quantile regression. The results extend existing data on signal crayfish nocturnalism and demonstrate that, although signal crayfish can tolerate a range of flows, activity becomes limited as water temperature declines seasonally and when water depth remains high in autumn and winter months.     

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.     

Artificial gills for robots: MFC behaviour in water

This paper reports on the first stage in developing microbial fuel cells (MFCs) which can operate underwater by utilizing dissolved oxygen. In this context, the cathodic half-cell is likened to an artificial gill. Such an underwater power generator has obvious potential for autonomous underwater robots. The electrical power from these devices increased proportionately with water flow rate, temperature and salinity. The current output at ambient temperature (null condition) was 32 microA and this increased by 200% (approximately 100 microA) as a result of a corresponding temperature increase (DeltaT) of 52 degrees C. Similarly, the effect of increasing the water flow rate resulted in an increase in the MFC output ranging from 135% to 150%. Furthermore, the same positive effect was recorded when artificial seawater was used instead, in which case the increase in the MFC current output was >100% (from 32 to 65 microA). There was a distinct difference in the MFC performance when operated under low turbulent as opposed to high turbulent flow rates. These findings can be advantageous in the design of underwater autonomous robots.     

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

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

The Fanner Honey Bee: Behavioral Variability and Environmental Cues in Workers Performing a Specialized Task

We tested the hypothesis that Apis mellifera workers exhibit plasticity in moving from fanning to guarding behavior. Bees marked when fanning are more likely to guard than fan on subsequent days, but guard to fanner reversals were common. Our findings suggest that bees can switch between these tasks, but that their bias between the two tasks changes over time, rather than a strict serial progression of worker tasks. The number of fanning workers is positively correlated with ambient temperature and negatively correlated with humidity; this conclusion gives insight into the environmental triggers for worker behavior.     

Winter movements and activity of signal crayfish Pacifastacus leniusculus in an upland river,determined by radio telemetry

Radio-telemetry was used to study the late autumn and winter movements of twenty adult signal crayfish Pacifastacus leniusculus (32.9–63.8 mm carapace length) an introduced exotic crayfish species, in the upland River Wharfe, northern England. The distances moved during the study varied greatly between individuals (0–328 m). Movements were generally sporadic; crayfish would remain in one position for several weeks and make occasional movements to new locations. Total distances travelled, linear range and ranging area did not differ significantly between males and females. The distance travelled in upstream and downstream directions did not differ significantly and there was no correlation between distance travelled and crayfish size. Several high flow events occurred during the study, but these did not cause any mortality or apparent displacement of crayfish downstream, suggesting that this is not a significant factor in downstream dispersal or mortality of adults of this invasive crayfish species in winter. A marked reduction in large-scale movements occurred in mid-December which coincided with a decline in water temperature. There was a less distinct pattern in local activity which was strongly correlated with water temperature and varied before and after mid-December.     

Systems of chemoperception in Decapod crayfish

The review presents data on some peripheral and central structures in the system of perception of chemical stimuli in crayfish and other Decapoda. The hair receptors on chelipeds, antennas, and antennules are innervated by mechano- and chemoreceptor neurons. Antennules are crayfish specialized chemoreceptor organs whose surface contains groups of exteroceptors. On claws of ambulatory feet (AF), antennas, antennules, and other mobile appendages there is a regular disposition of exteroceptor receptive fields in the form of receptor hair bushes. Behavioral experiments have shown sensitivity of crayfish to odor of individuals of their gender and sex partners as well as the presence in crayfish of pheromones providing connection of female with offspring at the initial stages of their life cycle. Individual chemosensory cells innervating hair bushes on the crayfish AF respond to amino acids, amines, nucleotides, and sugars. Minimal thresholds of reaction of the studied Decapoda chemoreceptors in response to some chemical compounds correspond to 0.1–1.0 μM. For some chemoreceptors, dose-dependent effects have been shown. Alongside with monomodal chemoreceptors, the crayfish have bimodal receptors perceiving mechanical and chemical stimuli. The efficient response of crayfish chemoreceptors can be obtained to the substance that has amino group with hydrogen bridge to carboxyl group, contains no more that 3 carbon atoms in the chain, is characterized by a certain stereoform. Among chemoreceptors there are fast and slow adapting cells. Efficiency of response of individual chemoreceptors depends on temperature of medium. In crayfish, chemoreceptors responding to ecdysterons have been revealed. Ecdysterons play a great role in intra- and inter-species communications in Crustacea. Based on the study of efferent responses of interneurons of the first and higher orders in the first thoracic crayfish ganglion to stimulation of the own receptive fields, a concept has been put forward of the structural-functional organization of afferent projections at the segmental level. Peculiarities of afferent projections from antennule chemoreceptors are considered. The data are presented on connections of these chemoreceptors with antennular, olfactory, and accessory lobules, various cell groups, interneurons of the first, second, and third orders located in various brain parts. An attention has been drawn to connections of serotonin neurons in glomeruli with endings of chemoreceptor neurons and projections of interneurons of the higher orders, which are located in the internal medulla of the crayfish eyestalks. Several principles of integration of the chemoreceptor information in central parts of the crayfish nervous system are discussed. The giant serotonin neurons revealed in crayfish glomeruli most likely participate in formation of memory to certain chemical actions. Polymodal receptor signals in the central chain of the perception system activate autonomic centers, and the changes of the animal functional state can be evaluated from the heart responses. These responses recorded by novel noninvasive methods allow detection of the initial and other phases of the stress state at changes of the medium chemical quality. Progress of the current biochemical and electrophysiological methods of study chemoreceptors allow hoping for learning of fine chemoperception mechanisms in invertebrate and vertebrate animals.     

A single muscle moves a crustacean limb joint rhythmically by acting against a spring containing resilin

Background  

The beating or fanning movements of three pairs of maxilliped flagella in crabs and crayfish modify exhalent gill currents while drawing water over chemoreceptors on the head. They play an integral part both in signalling by distributing urine odours, and in active chemosensation.     

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.     

Invertebrate-Inspired sensory-motor systems and autonomous, olfactory-guided exploration

The localization of resources in a natural environment is a multifaceted problem faced by both invertebrate animals and autonomous robots. At a first approximation, locomotion through natural environments must be guided by reliable sensory information. But natural environments can be unpredictable, so from time to time, information from any one sensory modality is likely to become temporarily unreliable. Fortunately, compensating mechanisms ensure that such signals are replaced or disambiguated by information from more reliable modalities. For invertebrates and robots to rely primarily on chemical senses has advantages and pitfalls, and these are discussed. The role of turbulence, which makes tracking a single odor to its source a complex problem, is contrasted with the high-fidelity identification of stimulus quality by the invertebrate chemoreceptor and by artificial sensors.     

Chemical orientation to food by the crayfish Orconectes rusticus: influence of hydrodynamics

Many different organisms orient to chemicals in a variety of habitats. Each of these habitats has a unique hydrodynamic environment that is dependent upon the structure of that habitat. Differences in the hydrodynamics (i.e. turbulence) of an environment will be reflected in the fine-scale structure of chemical signals. To determine what role dispersion dynamics play in influencing orientation behaviour, we studied crayfish searching for food sources in different artificial streams. Streams differed only in substrate composition (sand or cobbles), and the hydrodynamics associated with different substrates were quantified. A detailed analysis of orientation paths showed that crayfish could orient to food sources in streams with either substrate. The most parsimonious explanation is that animals are using information contained in the spatial and temporal distribution of chemicals in the flow to make directional decisions. Crayfish located the source more quickly, spent more time moving, and walked faster while orienting in streams having a cobble substrate compared with those having a sand substrate. These differences between substrates were not seen in control streams. These results show that the hydrodynamics associated with chemical signal structure can greatly influence the temporal properties of orientation to food sources. For crayfish, differences in the turbulent structure of flow may actually increase orientation efficiency by decreasing search time. On a broader scale, these results show that it is important to quantify orientation behaviour in a number of hydrodynamically different environments. Copyright 1999 The Association for the Study of Animal Behaviour.     

Exploration in a T-maze by the crayfish Cherax destructor suggests bilateral comparison of antennal tactile information

Many crayfish species inhabit murky waters or have a crepuscular lifestyle, which forces them to rely on chemical and mechanical information rather than visual input. Information on how they use one form of mechanical information-tactile cues-to explore their local environment is limited. We observed the exploratory behavior of the crayfish Cherax destructor in a T-maze under red light. Animals moved forward along the long arm of the maze and then moved equally in one of two available directions. The arm chosen by one crayfish did not affect that selected by a second crayfish tested immediately after in an unwashed maze. Previous experience in the maze also did not affect the choice. We found, however, that crayfish with one antenna denervated or splinted back to the carapace turned more often toward the unaltered side. Our data support the hypothesis that crayfish bilaterally compare information from their antennae.     

The relationship between body size and the field potentials generated by swimming crayfish

Aquatic animals generate electrical field potentials which may be monitored by predators or conspecifics. Many crustaceans use rapid, forceful contractions of the flexor and extensor muscles to curl and extend their abdomens during swimming in escape and locomotion. When crayfish swim they generate electrical field potentials that can be recorded by electrodes nearby in the water. In general, it is reasonable to assume that larger bodied crayfish will generate signals of greater amplitude because they have larger muscles. It is not known, however, how activity in particular muscles and nerves combines to produce the compound electrical waveform recorded during swimming. We therefore investigated the relationship between abdominal muscle, body size and the amplitude of nearby tailflip potentials in the freshwater crayfish (Cherax destructor). We found that amplitude was correlated positively with abdominal muscle mass. The mean amplitude recorded from the five smallest and five largest individuals differed by 440 microV, a difference sufficiently large to be of significance to predators and co-inhabitants in the wild.     

Disturbance and species displacement: different tolerances to stream drying and desiccation in a native and an invasive crayfish

1. Crayfish are among the most threatened taxa in the world and invasive crayfish are the primary cause of the decline of native crayfish. Most research has emphasised biotic interactions as the mechanism by which native crayfish are displaced by invasives, although crayfish occupy variable environments and the role of disturbance in facilitating crayfish invasion and displacement is understudied. 2. We compared tolerance to a disturbance, stream drying, in a native and invasive crayfish as a potential mechanism to explain their distribution. Our experiments and observations were conducted across scales, from laboratory environmental chambers to stream mesocosms to field sampling. We hypothesised that the invasive crayfish would be more tolerant of desiccation than the native, and that this physiological distinction between the two would be reflected in their distribution in relation to stream drying. 3. In the laboratory, the native crayfish Orconectes eupunctus was less tolerant of desiccation than the invasive Orconectes neglectus chaenodactylus, with all native crayfish dying within 2 days without water, while some of the invasive crayfish survived for nearly 2 weeks. Under simulated stream drying in mesocosms, only the native O. eupunctus survived less well than in a control. Field sampling demonstrated a significant negative relationship between O. eupunctus density and low summer flows, while O. neglectus density was positively associated with low summer flows. The greater resistance of O. neglectus to drying could, through priority effects, inhibit recolonisation by O. eupunctus once flow resumes. 4. Abiotic disturbances are potentially important to the displacement of native by invasive crayfish. Disturbance mediated displacement of aquatic species provides both an opportunity to conserve native species by maintaining or restoring habitat and disturbance regimes and is also a challenge due to increasing human water demand, flow regime alteration and global climate change.     

Do antennule and aesthetasc structure in the crayfish Orconectes virilis correlate with flow habitat?

The local flow environment affects the shape of waterborne chemical signals through a variety of physical mechanisms and at several scales. Since crayfish rely on these chemical signals to extract information about predators, prey, and mates, one might expect the chemical sensors (aesthetascs) on crayfish antennules to be physically tuned to the presentation of chemical cues by the flow environment. This hypothesis was tested by comparing length, diameter, and spacing of antennules and aesthetascs among geographically distinct populations of Orconectes virilis. Crayfish were collected from the Chagrin river, Hebron hatchery, and Burt lake. In addition, antennules were sampled from 43 museum populations representing 12 lake, 10 creek, and 21 river populations from multiple states and river drainages. Mean velocities from the collection sites were either measured directly or calculated from United States Geological Survey (USGS) historical data. Structural parameters were measured using Scion Image software on Scanning electron microscope micrographs, and analyses of variance were performed using StatView. Structural parameters of aesthetascs were found to vary with flow environment. Aesthetascs from lake populations were inserted at a larger angle, extended out farther from the supporting antennule relative to the width of the antennule, and were more widely spaced than aesthetascs from creek, hatchery, and river populations.     

Simulation of oscillating water movement in the laboratory for cultivation of shallow water sedentary organisms

1. Experiments in the natural habitat and under laboratory conditions have been conducted to analyse the factors responsible for the orientation of the fans of the colonial hydroidAglaophenia pluma. These experiments indicate that the prevailing direction of water movement significantly affects fan positioning. 2. Field experiments reveal thatAglaophenia pluma growing onCystoseira sp. orientates the dorsal side of its fans towards the base of this algae. After detaching and turning of substrate piecesA. pluma colonies lose their fans and re-orientate the regenerating fans prevailing to water current. 3. Laboratory experiments in running water onAglaophenia pluma var.teissieri show, as in the field, dorsal fan orientation perpendicular to the water current; however, rate of up growth is much slower than in the field. 4. Simulation of oscillating water movement, characteristic of the natural habitats of the species investigated, was possible via a special, newly designed pump system. The new system is described. 5. TheAglaophenia pluma var.teissieri fans were fixed with their rocky substrate on a turntable and exposed to the oscillating water movement in a current canal. After the fans have been cast off, the oscillating water movement induces a much higher rate of growth than the running water only. The orientation of the fans was strictly perpendicular to the current. 6. On the margins of the substrate exposed to the current, the fans were orientated with their dorsal surface toward the margin; in the centre of the rock fragments the fans are also strictly orientated perpendicular to the current with their dorsal sides showing in either direction. 7. A close study of the flow of current at the edges of the substrate showed that the whirls may diminish or even reverse the current coming from the substrate side. The orientation of the fans with their dorsal side outwards shows that they orientate themselves to the strongest current. 8. The orientation of a developing fan is basically determined by the first polyp. However, by slow, step by step turning of the upgrowing fan, a helically twisted fan could be obtained, indicating that secondary directioning is possible during growth. Twisted fans can also be found occasionally in the field; presumably they grew up under alternating current directions.Aglaophenia pluma var.teissieri exposed to permanent rotation give rise to regenerating fans which are orientated in the same way as the previous set of fans (preceding cast off).     

Male–Female Communication in the Crayfish Orconectes rusticus: The Use of Urinary Signals in Reproductive and Non-Reproductive Pairings

Animals use sensory communication to locate conspecifics, food, shelter, and avoid predators. Using urine visualization techniques as well as Digital Particle Illumination Velocimetry, we examined the role of urinary signals and current generations during social interactions of male and female crayfish. Both reproductive and non‐reproductive crayfish were paired to gain a better understanding of how reproductive state influences communication. Analyses of agonistic and mating events were paired in time with recorded urine release and current generation, illustrating a correlation of chemical communication with ritualized social behavior. Four treatment groups were run with specific combinations of different reproductive status: (1) both opponents reproductively active, (2) only the male in reproductive, (3) only the female reproductive, or (4) both opponents non‐reproductive. Results showed differences between treatment groups in urine release, current generation, and social behavior. Within reproductive pairings, both the male and female crayfish generated currents and released urine at higher rates than those in other treatment groups. Urine was released most often when opponents were in chelae contact with each other and these releases were often accompanied by anterior current generation. In addition, communication was different in reproductive trials where mating occurred. Overall, the results indicate that the use of hydrodynamic and chemical signals changes as a function of reproductive state and that this change in communication probably indicates readiness to mate.     

Habitat use by endangered Japanese crayfish (<Emphasis Type="Italic">Cambaroides japonicus</Emphasis>) in low-gradient streams of southern Hokkaido,Japan: reach and microhabitat-scale analysis

The Japanese crayfish (Cambaroides japonicus), the only native crayfish in Japan, is endangered and has experienced rapid population declines. We surveyed the habitat requirements of Japanese crayfish at the reach and microhabitat scales in semi-natural low-gradient streams. Habitat use by Japanese crayfish differed between the spatial scales. Reach-scale analysis revealed that the bed slope was the only positive predictor of crayfish density. This finding indicates that relatively high-gradient reaches, such as headwater reaches, are an important habitat for the conservation of Japanese crayfish in low-gradient streams. Microhabitat-scale analysis showed that crayfish density was positively affected by substrate coarseness and the presence of instream vegetation cover (bank vegetation, woody debris, and leaf patches), whereas it was negatively affected by distance from the stream edge. Coarse substrates and vegetation cover may function as shelters from water flows and predators during low flow periods. The use of stream-edge areas may allow quick access to refugia and enable the crayfish to avoid unexpected flood disturbance and predation. These habitat characteristics should therefore be preserved for the conservation of Japanese crayfish, and scale-dependent habitat characteristics should be considered in future conservation plans.