Waterborne Chemical Cues Research Articles

Predatory fish sounds can alter crab foraging behaviour and influence bivalve abundance.

The risk of predation can have large effects on ecological communities via changes in prey behaviour, morphology and reproduction. Although prey can use a variety of sensory signals to detect predation risk, relatively little is known regarding the effects of predator acoustic cues on prey foraging behaviour. Here we show that an ecologically important marine crab species can detect sound across a range of frequencies, probably in response to particle acceleration. Further, crabs suppress their resource consumption in the presence of experimental acoustic stimuli from multiple predatory fish species, and the sign and strength of this response is similar to that elicited by water-borne chemical cues. When acoustic and chemical cues were combined, consumption differed from expectations based on independent cue effects, suggesting redundancies among cue types. These results highlight that predator acoustic cues may influence prey behaviour across a range of vertebrate and invertebrate taxa, with the potential for cascading effects on resource abundance.

Trait-mediated functional responses: predator behavioural type mediates prey consumption.

The predator functional response (i.e. per capita consumption rate as a function of prey density) is central to our understanding of predator-prey population dynamics. This response is behavioural, depending on the rate of attack and time it takes to handle prey. Consistent behavioural differences among conspecific individuals, termed behavioural types, are a widespread feature of predator and prey populations but the effects of behavioural types on the functional response remain unexplored. We tested the effects of crab (Panopeus herbstii) behavioural type, specifically individual activity level, on the crab functional response to mussel (Brachidontes exustus) prey. We further tested whether the effects of activity level on the response are mediated by the presence of toadfish (Opsanus tau) predation threat in the form of waterborne chemical cues known to reduce crab activity level. The effects of crab activity level on the functional response were dependent on crab body size. Individual activity level increased the magnitude (i.e. slope and asymptote) of the type II functional response of small crabs, potentially through an increase in time spent foraging, but had no effect on the functional response of large crabs. Predation threat did not interact with activity level to influence mussel consumption, but independently reduced the slope of the type II functional response. Overall, this study demonstrates size-specific effects of a behavioural type on a predator-prey interaction, as well as a general pathway (modification of the functional response) by which the effects of individual behavioural types can scale up to influence predator-prey population dynamics.

Predator faunas past and present: quantifying the influence of waterborne cues in divergent ecotypes of the isopod Asellus aquaticus

Waterborne chemical cues are an important source of information for many aquatic organisms, in particular when assessing the current risk of predation. The ability to use chemical cues to detect and respond to potential predators before an actual encounter can improve prey chances of survival. We investigated predator recognition and the impact of chemical cues on predator avoidance in the freshwater isopod Asellus aquaticus. This isopod has recently colonised a novel habitat and diverged into two distinct ecotypes, which encounter different predator communities. Using laboratory-based choice experiments, we have quantified behavioural responses to chemical cues from predators typical of the two predator communities (larval dragonflies in the ancestral habitat, perch in the newly colonised habitat) in wild-caught and lab-reared Asellus of the two ecotypes. Individuals with prior experience of predators showed strong predator avoidance to cues from both predator types. Both ecotypes showed similar antipredator responses, but sexes differed in terms of threat-sensitive responses with males avoiding areas containing predator cues to a larger extent than females. Overall, chemical cues from fish elicited stronger predator avoidance than cues from larval dragonflies. Our results indicate that in these isopods, prior exposure to predators is needed to develop antipredator behaviour based on waterborne cues. Furthermore, the results emphasise the need to analyse predator avoidance in relation to waterborne cues in a sex-specific context, because of potential differences between males and females in terms of vulnerability and life history strategies.

Effects of Flow on the Behavior of the Southern Oyster DrillStramonita haemastomain Response to Exudates from Oysters and Oyster Reef Fauna

Stramonita haemastoma, the southern oyster drill, is a predatory gastropod that locates prey using waterborne chemical cues. These cues move by advection and are subjected to hydrodynamic forces such as turbulence, which can have significant effects on both the delivery of cues and on the efficiency and success of organisms that use chemical cues to find prey. We investigated how flow velocity and turbulence would affect oyster drill foraging behavior in a laboratory flume, and found that oyster drills would move upstream toward exudates from fouled oyster clumps but not toward seawater controls. We then measured foraging behavior in a range of flow conditions and did not find significant differences in either foraging success or efficiency among the flow treatments. We also found that a significant number of oyster drills would continue to move upstream even if cue delivery was stopped midway through the trial. Oyster drills placed their siphon near the sediment when oyster reef exudates were delivered through the sediment, and in turbulent flows when greater momentum delivered cues to the sediment. In all flow treatments, oyster drills spent ∼2.5 min motionless before proceeding upstream. Based on these observations, we posit that when first detecting an attractive cue, oyster drills evaluate the cue and flow direction using cues in the sediment and water column before making a decision to move upstream. While moving toward an attractive cue source, oyster drills will continue to move upstream even when the attractive cues are no longer being released, which allows them to find oyster reef habitats successfully in a range of flow conditions.

Contrasting behavioural responses of grazing mayflies and detritivorous caddisflies to predatory fish

Invertebrates living in streams where predatory fish are present are often able to detect them through water-borne chemical cues and respond with behavioural changes that lower predation risk. We hypothesised that behavioural responses to a predatory fish (brown trout, Salmo trutta) would be stronger in grazing mayflies (Baetis sp. and Epeorus sp.) than in detritivorous caddisflies (Potamophylax latipennis and Chaetopteryx sp.) in a montane stream in central Spain, because of differences in their foraging ecology and the presence of a protective case in the latter. Grazing mayflies reduced their rates of movement and entrance into the drift when trout were present, but this response disappeared shortly after trout removal by electrofishing. Mayflies also showed marked drift diel periodicity when trout were present. In contrast, detritivorous caddisflies responded to the potential predation threat by withdrawing into their case. However, their response was the same regardless of the presence of trout, which also had no influence on their movement patterns or drift activity. Our results suggest that effects of predatory fish on stream invertebrates vary with invertebrate traits such as foraging ecology and predator-avoidance strategies.

Embryonic exposure to conspecific chemicals suppresses cane toad growth and survival

Adaptations to suppress the viability of conspecifics may provide novel ways to control invasive taxa. The spread of cane toads (Rhinella marina) through tropical Australia has had severe ecological impacts, stimulating a search for biocontrol. Our experiments show that cane toad tadpoles produce waterborne chemical cues that suppress the viability of conspecifics encountering those cues during embryonic development. Brief (72 h) exposure to these cues in the egg and post-hatching phases massively reduced rates of survival and growth of larvae. Body sizes at metamorphosis (about three weeks later) were almost twice as great in control larvae as in tadpole-exposed larvae. The waterborne cue responsible for these effects might provide a weapon to reduce toad recruitment within the species' invaded range.

Recognition and use of ascidian hosts, and mate acquisition by the symbiotic pea crab Tunicotheres moseri (Rathbun, 1918): the role of chemical, visual and tactile cues

Many crustaceans live in intimate association with larger host animals, mostly for shelter and food. Host recognition and location behaviors by these crustaceans, and other symbionts, are vital in the life history of most symbioses. The pinnotherid crab Tunicotheres moseri (Rathbun, 1918) is a common symbiont with various solitary ascidians throughout its reported range of Jamaica, Venezuela, and West Florida. Sensory cues affecting host recognition, host use, and mate acquisition in the West Florida crab population were the focus of this study. T. moseri responded to host generated and conspecific (males responded to non-gravid females) waterborne chemical cues. Although host generated waterborne chemical cues were recognized by T. moseri, access to direct contact (which could involve chemical, visual and tactile cues) with host ascidians triggered much stronger responses. Results of conditioning trials suggest that T. moseri is a generalist, but prefers Styela plicata even after conditioning with the novel host species Molgula occidentalis and Phallusia nigra. These results show that T. moseri employs the use of multiple senses in establishing symbioses with host tunicates, and the plasticity of the responses allow potentially novel tunicates to serve as hosts. Finally, this study shows that male T. moseri, which typically only enter tunicates for breeding purposes, use waterborne cues to find tunicates housing potential female mates.

Environmental conditions influence the frequency of prey responses to predation risk

Predators can strongly influence prey populations and the structure and function of communities by altering the foraging behavior and/or habitat selection of prey. For these nonlethal predator effects to occur, prey must be able to detect and respond to cues indicating predation risk. The ability of prey to detect and respond to predator signals likely varies with environmental condi- tions. To better understand how the environment can modify nonlethal predator effects by influenc- ing the frequency of prey responses to predators, we examined how hydrodynamic conditions influ- ence predator avoidance behavior in the dogwhelk Nucella lapillus, a carnivorous snail found on rocky intertidal shores. When confronted with predation risk, such as that signaled by water-borne chemical cues released by predatory green crabs, N. lapillus often reduce their movement and forag- ing activity. Using laboratory flumes, we explored how flow velocity and turbulence influenced responses by N. lapillus to predator risk cues. The influence of hydrodynamic conditions on predator avoidance behavior were nonlinear. N. lapillus responded to predators most frequently in intermedi- ate flow velocities but less so in high and low velocities, suggesting that the effects of flow on pre- dator avoidance behaviors are complex. Abiotic factors like flow can strongly influence the behav- ioral responses of intermediate consumers, which may propagate to other trophic levels via trait-mediated trophic cascades.

The role of water-borne chemical cues in mediating social interactions of the Texas blind salamander, Eurycea rathbuni

AbstractAssociation patterns and social interactions of salamanders vary given habitat heterogeneity and behavioural characteristics. Cave ecosystems are generally food limited and encountering mates may be rare. Little is known about the mode of social interactions and preferences in cave-adapted salamanders. We examined social interactions of the caveadapted, federally endangered, Texas blind salamander, Eurycea rathbuni, by examining sex-specific association patterns. We predicted that non-visual (chemical) cues would be an important mode of communication. We found no difference in association patterns between the sexes when presented with a single conspecific and no aggregative behaviours were detected. Interestingly, when given a simultaneous choice between a male or female, females preferred to associate with male conspecifics while males showed no clear preference. The results suggest that females of E. rathbuni use chemical cues to either seek males or avoid females and provide valuable insight into the little known social behaviour of this species and possibly other similar species.

Molecular identification of candidate chemoreceptor genes and signal transduction components in the sensory epithelium ofAplysia

An ability to sense and respond to environmental cues is essential to the survival of most marine animals. How water-borne chemical cues are detected at the molecular level and processed by molluscs is currently unknown. In this study, we cloned two genes from the marine mollusk Aplysia dactylomela which encode multi-transmembrane proteins. We have performed in situ hybridization that reveals expression and spatial distribution within the long-distance chemosensory organs, the rhinophores. This finding suggests that they could be receptors involved in binding water-borne chemicals and coupling to an intracellular signal pathway. In support of this, we found expression of a phospholipase C and an inositol trisphosphate receptor in the rhinophore sensory epithelia and possibly distributed within outer dendrites of olfactory sensory neurons. In Aplysia, mate attraction and subsequent reproduction is initiated by responding to a cocktail of water-borne protein pheromones released by animal conspecifics. We show that the rhinophore contraction in response to pheromone stimulants is significantly altered following phospholipase C inhibition. Overall, these data provide insight into the molecular components of chemosensory detection in a mollusk. An important next step will be the elucidation of how these coordinate the detection of chemical cues present in the marine environment and activation of sensory neurons.

Review of Aquatic Sex Pheromones and Chemical Communication in Anurans

Chemical communication is important in aquatic environments, particularly where visual and acoustical signals are limited. Both larval (tadpole) and adult anurans (frogs and toads) use waterborne chemical signals for many activities. Adult anurans commonly rely on acoustical communication for sex recognition and mating; however, a growing body of evidence suggests that anurans also may use aquatic sex pheromones for localization of potential mates. We provide an overview of how the anuran nasal cavity reorganizes during metamorphosis from the larval to the adult stage. Also, we focus on the behavior of reproductive anurans in response to chemical information detected by olfaction of waterborne chemical cues. Overall, we synthesize the current literature on anuran sex pheromones and chemical communication in the aquatic environment.

NEUROSENSORY ECOLOGY IN THE JEB

It is often difficult to imagine how other people perceive the world, let alone other species, so when Ken Lukowiak was approached by The JEB's Editor in Chief, Hans Hoppeler, to draw together reviews discussing Neurosensory Ecology, he decided to steer clear of the usual sensory topics. Taking an

Settlement of Crassostrea ariakensis Larvae: Effects of Substrate, Biofilms, Sediment and Adult Chemical Cues

The Suminoe oyster (Crassostrea ariakensis) is being considered for introduction into the Chesapeake Bay. However, our current understanding of the biology and ecology of C. ariakensis is insufficient to predict whether an introduction will be successful, provide desired benefits, or have adverse impacts. Behavior of native Eastern oyster (C. virginica) pediveligers has been studied for many years and it is well established that they use a variety of habitat characteristics when selecting a site for colonization. Perhaps the most important of these are chemical cues emitted by adult conspecifics, which can lead to gregarious larval settlement and dense, persistent reef communities. Conversely, almost nothing is known about the mechanisms that regulate larval settlement and metamorphosis for C. ariakensis or how pediveligers might respond to conditions found in Chesapeake Bay. In a comparative study with C. virginica, we examined how environmental factors such as substrate type, natural biofilms, sediment and waterborne chemical cues influence larval settlement for two C. ariakensis strains (''south China'' and ''west coast''). Our results demonstrate many similarities but also potentially important differences. Both species and strains of larvae greatly prefer natural substrates (e.g., shell) covered with biofilms for colonization but the west coast strain of C. ariakensis exhibited greater attachment onto manmade substrates (e.g., fiberglass) than C. virginica. Waterborne chemical cues emitted by adult oysters were also found to enhance substrate attachment for all larval forms but cues do not appear to be species specific. These results provide critical insight to the ability of C. ariakensis larvae to identify and colonize suitable substrates in the Chesapeake Bay, which will have a large impact on recruitment success and their ability to establish self-sustaining populations.

Activity of Sphaerotheca breviceps tadpoles in response to chemical cues of the predaceous tadpoles Hoplobatrachus tigerinus

Tadpoles of Sphaerotheca breviceps raised in the laboratory from the egg stage, and hence lacking prior experience of a predator or its odors, were tested to examine their responses to a predator’s (tadpoles of Hoplobatrachus tigerinus) water-borne chemical cues. The stimulus solution was obtained following 24 h of rearing tadpoles of H. tigerinus (one tadpole per 200 mL water) that were not fed during this period. Upon exposure to the stimulus solution the activity of S. breviceps tadpoles decreased by about 90% within 5 min. Their resting period increased significantly over baseline activity, whereas the swimming period, distance traversed, and swimming spurts declined. However, whenever a test tadpole moved, its swimming velocity was high in response to stimulus solution. The antipredatory responses declined with increase in time of storage of the stimulus solution, indicating decay of the predator’s chemical cues. The findings suggest that (1) antipredator defense strategies of S. breviceps do not require prior experience of predators, (2) the predator’s chemical cues are labile in nature, and (3) the response of prey tadpoles to such cues is similar to reported behavior of anuran tadpoles in response to real predators and alarm cues.

Threat‐Sensitive Behavioral Responses to Concentrations of Water‐Borne Cues from Predation

Aquatic organisms often detect predators via water-borne chemical cues, and respond by showing reduced activity. Prey responses may be correlated with the concentration of predation cues, which would result in graded antipredator behavioral responses that adjust potentially costly behavioral changes to levels that are commensurate with the risk of predation. Larvae of the predatory mosquito Toxorhynchites rutilus prey upon other container-dwelling insects, including larvae of the mosquito Ochlerotatus triseriatus. Previous work has established that O. triseriatus reduce movement, foraging, and time below the surface, and increase the frequency of resting at the surface, in the presence of water-borne cues from predation by T. rutilus. We tested whether these responses by O. triseriatus are threat sensitive by recording behavior of fourth instar larvae in two runs of an experiment in which we created a series of concentrations (100, 10, 1, 0.1, and 0.01% and 100, 70, 40, 20, and 10%) of water that had held either O. triseriatus larvae alone (control) or a T. rutilus larva feeding on O. triseriatus (predation). We also tested whether associated effects on time spent feeding are threat sensitive by determining whether frequencies of filtering or browsing are also related to concentration of cues. The frequencies of resting and surface declined, whereas frequency of filtering (but not browsing) increased more rapidly with a decrease in concentration of predation cues compared with control cues. Thus, O. triseriatus shows a threat sensitive behavioral response to water-borne cues from this predator, adjusting its degree of behavioral response to the apparent risk of predation.

Female choice in response to risk of sperm limitation by the stone crab, Hapalogaster dentata

Mating with males that have recently mated would be risky for females because the males may have limited sperm. Females should prefer males that can provide sufficient sperm for successful fertilization. We investigated whether female stone crabs prefer the larger of two males and which type of cue, visual or chemical, is more important for female mate preference. We then investigated whether females show mate choice in response to the risk of sperm limitation by exposing a receptive female in an aquarium to two males simultaneously: an unmated male with sufficient sperm reserves and a male with depleted sperm reserves. We tethered the males and wrapped their chelae to prevent interference in the females' choice. All females approached and mated with the larger males, indicating that females prefer larger to smaller males. Females located larger males by waterborne chemical cues. Using these cues, females showed a preference for unmated males with sufficient sperm reserves over sperm-depleted males, indicating that sperm limitation occurs in nature, and is a selection pressure in the mating strategy of female stone crabs. Thus, the influence of risk of sperm limitation on female choice should be considered in studies of sexual selection by field observations and laboratory experiments, and in sexual selection models.

Adult fiddler crabs Uca pugnax (Smith) enhance sediment-associated cues for molting of conspecific megalopae

Adult-associated chemical cues can stimulate settlement and metamorphosis of invertebrate larvae into habitats with an enhanced likelihood of juvenile and adult survival. For example, sediments from adult fiddler crab habitat stimulate fiddler crab megalopae to metamorphose (molt) sooner than sediments without adult cues. A similar stimulation of molting occurs after exposure to waterborne chemical cues from adult habitats and to exudates and extracts of adult crabs. We tested whether sediments from habitats without adult Uca pugnax (Smith), which do not stimulate molting of their megalopae, could become stimulatory through brief exposure to adult crabs. Sediments were collected from tidal flats at several distances (∼ 1 m, ∼ 50 m, and ∼ 5.4 km) from adult habitats, and incubated for 24 h with or without adult crabs. Molting rates of laboratory-reared megalopae exposed for 48 h to adult-conditioned sediments were compared to those for untreated controls. Sediments collected in or within 1 m of adult habitat elicited the highest molting rates, and natural sediments from 50 m and 5.4 km had little or no effect on molting. However, incubating sediments collected away from adult habitat with adult crabs produced a higher molting response, and the magnitude of the enhancement increased with distance from adult habitat. Results suggest that the chemical cues that adult crabs release are retained by sediments and consequently stimulate molting of megalopae, regardless of the nature of the sediments themselves. Lack of chemical cues may retard colonization of newly created or heavily disturbed habitats that are otherwise suitable settlement and adult habitat.

Case selection by a limnephilid caddisfly [Potamophylax latipennis (Curtis)] in response to different predators

Some organisms use morphological structures obtained by behavioural processes to lower mortality by predation. We test whether larvae of the limnephilid caddisfly Potamophylax latipennis (Curtis) vary their responses to the presence of different predators (dragonfly naiads, fire salamander larvae or brown trout) by choosing organic or mineral cases. We offered both case types to larvae, and simulated differences in predation risk using water conditioned with chemicals from the different predators. Our results show that Potamophylax larvae detect and discriminate predators using water-borne chemical cues and alter their choice of case type according to the perceived predation risk. Moreover, the distribution of larvae bearing cases of different anti-predator value matches the spatial variation in predation risk in the field.

Water-borne cues from a shell-crushing predator induce a more massive shell in experimental populations of an intertidal snail

Inducible defenses are important in the life strategies of many taxa. In some species of marine gastropods, water-borne chemical cues from potential predators induce defensive changes in shell form and differences in growth rate. We examined such phenotypic plasticity in the direct-developing snail, Littorina subrotundata (Carpenter, 1864). Among experimental field populations of L. subrotundata exposed to differing intensities of predation by the purple shore crab, Hemigrapsus nudus (Dana, 1851), snails collected from predation-intense environments often had more massive shells than closely related snails from adjacent environments where predation was negligible. Snails collected from both environments were raised in tanks containing cages of H. nudus that were feeding on conspecific snails and compared to a control group raised in the absence of this stimulus. Most snails developed significantly more massive shells in the presence of the crabs suggesting that adaptive phenotypic plasticity may account for some of the variation we observed in the field. In one case, snails from a predation-intense environment did not exhibit a statistically significant amount of plasticity, but instead grew a more massive shell irrespective of the laboratory stimulus. We interpret this as evidence for a genetic difference in the plasticity of shell form among experimental populations, caused by intense selection by H. nudus. There was no statistical difference in the growth rates of snails among treatments.

Comment on "Predator classification by the sea penPtilosarcus gurneyi(Cnidaria): role of waterborne chemical cues and physical contact with predatory sea stars"

In their study of behavioural responses of pennatulaceans to physical contact with asteroids in 2002, Weightman and Arsenault claim to be the first to demonstrate that cnidarians have the ability to distinguish predators from nonpredators. In fact, it has been known since at least the 1960s that cnidarians are capable of predator recognition. We briefly describe some of the abundant literature on this topic, especially studies on anthozoans.