Behaviour of juvenile mud crabs Scylla serrata in aquaculture: Response to odours of moulting or injured crabs

Behaviour of juvenile mud crabs, Scylla serrata (70–90 mm carapace width, CW) were observed in response to odours of moulting and injured conspecifics and food (pilchard) under controlled flow conditions using bioassay technique. This study was undertaken to better understand the role that chemical cues have in mediating the attraction of cannibal crabs to moulting crabs in an aquaculture growout facility and thus aid in more successful production. In response to moult odour juvenile S. serrata spent 5.6 ± 1.9% of the time in locomotion but this did not differ significantly (P > 0.05) from that of control odours (seawater, 2.6 ± 1.2%), however a tactile response was observed for moult odour not seen in controls. Juveniles exposed to the odour of injured conspecifics (12.2 ± 2.3% of time in locomotion) and to food (22.7 ± 3.1%) differed significantly from the seawater control (P < 0.05). The possibility that the active agent in moult water is relatively dilute was considered, however varying concentrations of food and crushed conspecific odour failed to demonstrate concentration dependant behavioural results. Variation in the form of size (carapace width) and sex was revealed, so too was preliminary evidence of behavioural differences between crab hatchings. For example, larger crabs (around 80 mm CW) increased tactile investigation of the odour inlet pipe in response to the crab-based odours of moulting (3.5 ± 1.7% of the time) and injured conspecifics (2.6 ± 1.0%), though response to food remained constant over all sizes (10.0% of the time). In another experiment, larger female crabs maintained a high frequency of tactile response to the odour of injured conspecifics. In males, the response was attenuated in larger individuals. Despite no differences being found between moult odour and controls some evidence exists to suggest that a small proportion of crabs were responding to the moult odour and that this still has the potential to cause a dramatic cumulative reduction in growout survival. Variation in size and subsequent behaviour of individuals poses the question of whether behaviour contributes to growth rate and might be a focus of genetic selection for more uniform growth.     

Pattern of integration of conflicting stimuli by the crab Heterozius rotundifrons

When an animal receives several stimuli that could evoke conflicting behaviours they can either show a response to just one stimulus or show a gradation of responses to the multiple stimuli. It has been proposed [Hazlett BA. 2000. Responses to single and multiple sources of chemical cues by New Zealand crustaceans. Mar Freshw Behav Physiol. 34:1–20] that a graded response will be seen if the animals have an alternative response to one behavioural category of stimuli (the alternative-behaviour-gradual-change rule). The crab Heterozius rotundifrons has two alternative patterns of predation avoidance, either assumption of a rigid limb-extended posture for several minutes or a short period of limb extension and then rapid locomotion. We presented crabs with full strength input in one category (food stimulus) and one of seven intensities of input in a conflicting category (either chemical or visual cues associated with increased predation risk). In both cases, as the intensity of the danger signal gradually increased, there was a gradual increase in the duration of the limb-extended posture.     

Anti-predator responses of the intertidal crab Heterozius rotundifrons (Brachyura: Belliidae) in air and water

The intertidal crab Heterozius rotundifrons responds to tactile input, as occurs during a predation attempt, by hyper-extending all of its limbs and remaining in that posture for a variable length of time. We compared the duration of this anti-predator response: (1) in the day versus night (2) in two fluid media (air versus water) (3) after exposure to additional predator cues in one medium (air or water) and testing in the other medium (4) for crabs from different parts of the tidal range and (5) for females with and without eggs on their pleopods.?Crabs showed the posture at night as well as during the day. They also executed the posture when tested in air and extended the duration of the posture in air when they detected an additional predation-risk cue, shadows passing overhead. When crabs experienced input in one medium there was no effect on the duration of behavior shown in the other medium. Crabs from the lower portion of the intertidal showed a markedly longer duration of the limb-extended posture compared to crabs from the higher end of the tidal range of this crab. Berried females responded the same as females without eggs in both air and in water. Thus, crabs show this anti-predator behavior under a wide variety of conditions, but do not appear to transfer information received in one medium to behavior shown in the other media.     

Foraging Trade-offs in Fathead Minnows (Pimephales promelas,Osteichthyes, Cyprinidae): Acquired Predator Recognition in the Absence of an Alarm Response

Pike-naive fathead minnows (Pimephales promelas) were fed ad libitum or deprived of food for 12, 24, or 48 h and then exposed to either conspecific alarm pheromone or distilled water and the odour of a predatory northern pike (Esox lucius). Minnows fed ad libitum or deprived for 12 h showed a stereotypic alarm response to the alarm pheromone (increased time under cover objects and increased occurrence of dashing and freezing behaviour); those deprived of food for 24 h showed a significantly reduced alarm response, while those deprived of food for 48 h did not differ significantly from the minnows exposed to a distilled water control. Upon subsequent testing in an Opto-Varimex activity meter, all groups initially exposed to alarm pheromone and pike odour exhibited an alarm response when exposed to pike odour alone. Those initially conditioned with distilled water and pike odour did nor show an alarm response to pike odour alone. These results demonstrate that there exists a significant trade-off between hunger level and predator-avoidance behaviour in fathead minnows and that minnows can learn the chemical cues of a predatory northern pike through association with alarm pheromone even in the absence of an observable alarm response.     

Predator-induced diapause in Daphnia magna may require two chemical cues

The production of diapausing eggs by Daphnia magna stimulated by fish exudates can be explained as an anti-predator defence ensuring genome protection in periods of high risk from fish predation. The combined effects on the induction of D. magna diapause of an “alarm” chemical originating from injured conspecific prey and fish kairomones were tested. The results of the experiment showed that the cues when present together promote both the production of ephippial eggs and male formation, indicating their role in the synchronization of the entire mode of Daphnia sexual reproduction. Ephippial eggs were only produced in the presence of both fish kairomone and conspecific alarm chemicals, while male offspring occurred in the treatments where both, one or none of the cues were present. However, production of males was the highest when both cues were provided. D. magna responded similarly to the tested cues whether or not the hypothetical alarm substance associated with predator odour came from Daphnia specimens actually eaten by fish or from crushed conspecific individuals. However, chemicals from crushed chironomid larvae combined with fish kairomones did not induce a similar response in D. magna. The relative advantage of utilization of alarm cues or predator kairomones in the induction of defence responses in prey organisms is discussed. Received: 8 June 1998 / Accepted: 11 January 1999     

Cautious cannibals: Behavioral responses of juvenile and adult blue crabs to the odor of injured conspecifics

Blue crabs are cannibalistic, and therefore the scent of injured conspecifics represents both a potential food cue, as well as an indicator of predation risk. We examined the response of blue crabs to conspecific odor alone, as well as in mixtures of attractive cues to determine how animals evaluate and respond to this odor. We explicitly manipulated risk-sensitivity based on either animal size (an indicator of susceptibility to predation) or hunger state (susceptibility to starvation) as ways to evaluate theories of risk-allocation, which suggest that decreases in predation risk, or increases in the risk of starvation, ought to result in diminished responses to sensory cues that signal predator presence or activity. Large and small blue crabs were challenged to locate the source of odor plumes consisting of the scent of injured conspecifics (risk cue), attractive food odors (attractive cue), or their mixture (conflicting cue). Neither large nor small blue crabs tracked aversive cues, but large blue crabs consistently tracked conflicting treatments to their source. Responses to conflicting and aversive treatments also involved diminished movement and reduced tracking speed relative to behaviors displayed in attractive plumes. Thus, even cannibalistic crabs seem to respond more prevalently to the apparent predation risk then to food reward, and risk-sensitive behaviors have a likely cost in terms of reduced food intake. Starved animals were more likely than unstarved animals to track conflicting plumes. Both the ontogenic shift and the response of starved animals support the notion that the cost of risk-aversive behaviors results in this strategy being allocated in proportion to the degree of potential risk. Since risk-aversive responses to chemical cues can produce strong effects in communities, the size-dependent nature of these responses in blue crabs may introduce considerable complexity in interactions between blue crabs, their predators, and their prey.     

Strong behavioural defensive responses of endemic Rana latastei tadpoles induced by a native predator's odour

Prey species must constantly acquire information on predator identity, abundance and dangerousness from the environment. In aquatic habitats, this information is mainly propagated by water-borne chemical signals, either predator-specific odours or prey alarm cues. Anuran larvae innately respond to conspecific alarm cues and are able to associate them to predator cues during their lifetime. In this study, we investigated the anti-predatory responses of endemic Italian agile frog (Rana latastei) tadpoles exposed to either conspecific or heterospecific alarm cues and a native predator's (Anax imperator larvae) odour. Pre-and post-stimulus behaviours of each tadpole were recorded by a digital camera and analysed by a source executable software for image-based tracking. We found that Italian agile frog tadpoles responded to fasted dragonfly odour by strongly reducing their activity, both in terms of the amount of time they spent active and path length covered in comparison to control groups. Contrary to previous studies, predators' diet had a negligible effect on tadpole response and our experiment did not bring any evidence of the phylogenetic-relatedness hypothesis. The innate or early-in-development recognition of dragonfly larvae is clearly adaptive and may increase tadpole survival with relatively low costs, but, at the same time, may increase the risk of ignoring novel potential threats.     

The smell of danger: chemical recognition of fish predators by the invasive crayfish Procambarus clarkii

1. Since avoiding predation can compromise animal fitness, prey are expected to respond to different predator species with an intensity appropriate to the level of risk. In fresh waters, the threat of predation is typically assessed by chemical cues, in particular by odours released by either injured/disturbed conspecifics (conspecific alarm odour) or predators (predator odours). Here, we used the most widely distributed crayfish in the world, the invasive North American Procambarus clarkii, to investigate the relative effectiveness of odours emitted by fish predators compared with conspecific alarm odour. We also tested whether P. clarkii is able to discriminate between fish predators of which it has ‘experience’ (either recent, via introduction to the same water body, or old, by sharing a native range), as well as between fish predators that pose low or high risk. 2. The study was carried out on introduced populations of P. clarkii from two sites, characterised by different fish assemblages: the Malewa River (a tributary of Lake Naivasha, Kenya) and Lake Trasimeno (Italy). Laboratory experiments consisted of three sequential phases (‘water’, ‘food’ and ‘smell’ phases) and five treatments. Treatments differed in the odour presented during the smell phase, i.e. no odour (plain water) and odours from either injured conspecifics or three fish species per site. Crayfish from the Malewa River population were confronted with the odours of largemouth bass (Micropterus salmoides), common carp (Cyprinus carpio) and tilapia (Tilapia zillii) (all introduced to Lake Naivasha but absent from the Malewa River), and those from the Lake Trasimeno population with the odours of the introduced largemouth bass and carp and the native chub (Squalius cephalus). Largemouth bass is the only predator that imposes a high risk to crayfish, and it also shares its native range with P. clarkii. We analysed the time spent by crayfish feeding, in locomotion and in adopting a raised or lowered posture. A reduction in the time spent feeding and in locomotion, and an increase in the time spent in the lowered posture were considered to indicate alarm. 3. Crayfish from both populations responded with a more pronounced reduction in feeding to conspecific alarm odour rather than to predator odours. Crayfish from the Malewa River reacted with the same intensity to the odours of the three fish species tested, whereas, in Lake Trasimeno, the odour of largemouth bass was significantly more threatening than the odours of the other two species. 4. Procambarus clarkii seems to perceive a general fish odour that alerts it to possible predation risk without the need of either a direct recent experience or via sharing a common native range. However, where they coexist with fish, crayfish become able to distinguish among species, adapting the intensity of their response to the effective risk. Our results confirm the relatively high learning capacity of P. clarkii reported in previous studies and suggest the existence of mechanisms that make predator recognition particularly efficient in this extraordinarily successful invader.     

Which Factors Affect Sex Ratio of Spined Loach (genus Cobitis) in Lake Müggelsee?

The distribution and extent of chemical alarm signaling systems among some families of fishes, including the Cottidae, remains unclear. In laboratory experiments, we tested whether reticulate sculpins, Cottus perplexus, respond to chemical alarm signals released by injured conspecifics. Sculpins decreased movement following exposure to skin extracts from conspecifics, but did not respond to cues of syntopic speckled dace, Rhinichthyes osculus, or allotopic swordtails, Xiphophorous helleri. Additional tests demonstrated that the responses of sculpins to alarm cues were dependent on the hunger level of the test fish. Sculpins deprived of food for 2 days failed to respond to conspecific alarm cues, however, the same individuals fed to satiation did respond to alarm cues.     

Innate responses to conspecific and heterospecific alarm cues in the endangered eastern cape redfin Pseudobarbus afer

We examined innate responses to conspecific and heterospecific alarm cues in a small cyprinid minnow, the Eastern Cape redfin Pseudobarbus afer. We found that redfins respond to conspecific skin extract, which contains alarm chemicals, and showed that their preferred response is to hide in refugia. Redfins also respond to skin extract from an allopatric, distantly related minnow species, the chubbyhead barb Enteromius anoplus indicating that neither sympatry nor close phylogenetic relationships are necessary for recognition of heterospecific alarm cues. Although both conspecific and heterospecific alarm cues induced similar responses, the response to heterospecific cues was less intense. This may be explained by a trade-off between selection to maximise threat recognition and selection to avoid the costs of responding to irrelevant cues, or by differences in chemical structures of alarm cues between species. These findings have implications for the conservation of this Endangered fish species and for freshwater fishes throughout Africa.     

Damage released prey alarm substances or predator odours? Risk assessment by an aquatic oligochaete

Although the abilities of prey to detect and respond to chemical substances associated with a predator have been widely reported, the factors promoting the evolution of responses to prey alarm cues vs. predator odours are still vague. In this article, we combined field research with laboratory experiments to explore which chemical substance associated with predator activity (predator odour, conspecific or heterospecific alarm substances) induces defence responses in the aquatic oligochaete Stylaria lacustris, which is vulnerable to common littoral predators. The field results indicated that predators injure the oligochaetes and a great proportion, up to 45% of individuals in the population, were found to be damaged. The results of the laboratory experiments revealed that chemical odours from damselfly larvae feeding on S. lacustris did not induce the defence response in the oligochaetes. On the contrary, oligochaetes detected and responded to alarm substances from damaged conspecifics alone and substances from damaged cladoceran Daphnia magna. We discussed conditions favouring the responses to damage released prey alarm cues instead of predator odours in Stylaria lacustris. Our data suggest that the selection of responses to alarm cues from damaged prey vs. predator odours may be dependent on three factors: (1) non-species-specific predation, (2) divergence of food niche of the different stages of the predator and (3) complex food web with multiple predators. Handling editor: S. Declerk     

Attraction of Flatworms at Various Hunger Levels Toward Cues from an Odonate Predator

Different hunger levels can modify a prey's antipredator behavior in the presence or absence of food. Satiated animals often forego foraging if a predator is nearby, whereas starved animals may risk a predator encounter to search for food. This study evaluated the influence of nutritional state on the behavior of the flatworm Dugesia dorotocephala in the presence of food, predator, and crushed conspecific cues. We found that flatworms are attracted to cues originating from a food source, crushed conspecifics, and a predator (dragonfly larva) compared with control cues. Among the different hunger level treatment groups, levels of satiation had no influence on activity levels but significantly influenced time spent close to and distance from the cue source. Flatworm movement toward predator cues emitted from dragonfly larvae is contrary to our expectations. These results suggest either a unique case of chemical mimicry from the dragonfly larvae or an inherent attraction of planarians to odonate predators that allows them to scavenge the remains of other odonate prey items.     

Antipredator behaviour mediated by chemical cues: the role of conspecific alarm signalling and predator labelling in the avoidance response of a marine gastropod

Gastropods represent a challenge in the understanding of alarm signalling. We studied predator avoidance (climbing behaviour) of the marine snail Tegula funebralis in laboratory experiments. Snails were exposed to crude extract of conspecifics, and to water conditioned by actively feeding or non-feeding predatory crabs. Crabs had previously been maintained on different diets, and were accordingly labelled by chemical cues of various origins. Tegula -extract alone released climbing behaviour in May, but not in June. However, during both these months, snails responded to chemical cues from crabs that were actively feeding on Tegula . Crabs labelled by Tegula -diet, and actively feeding on Tegula , also caused more climbing responses compared to crabs labelled by other diets. Chemical cues derived from crabs actively feeding on another snail species, or from non-feeding crabs, did not induce snail climbing no matter the previous feeding history of the predators. When snails received Tegula -extract combined with water conditioned with a non-feeding, Tegula -labelled crab, no climbing occurred. However, when the non-feeding, Tegula -labelled crab was present in the solution of Tegula -extract, moderate climbing responses were obtained. The results imply that climbing responses of T. funebralis are in general caused by the action of a two-component system. This system seems to be a mixture of chemical cues leaking from the tissue of conspecifics when being eaten, and latent conspecific chemicals that are modified in crabs and presumably released with the urine of chemically labelled predators. The modified chemical labels appear to be fully released by crabs when feeding, and moderately released when detecting food. The responses obtained in May with crude extract alone may result from a seasonal change in alarm signalling properties, or a change in behavioural responsiveness of snails exposed to a variable predator regime.     

Understanding the toad code: Behavioural responses of cane toad (Chaunus marinus) larvae and metamorphs to chemical cues

Abstract Larvae of many anuran taxa display strong behavioural responses to chemical cues, including alarm signals from injured conspecific tadpoles. We exposed tadpoles and metamorphs from an Australian population of the invasive cane toad (Chaunus[Bufo] marinus) to a range of chemical stimuli and quantified their responses both in the laboratory and in the field. Filtered fluids containing scent cues from crushed conspecifics elicited strong avoidance from tadpoles, whereas other cues (e.g. scent of food, of native‐range fish or urodele predators, and thermal stimuli) did not. Apparent aggregation of tadpoles in response to scent cues proved to be an artifact of tank design, and was an indirect consequence of avoidance of those cues. Field trials confirmed that free‐ranging toad tadpoles and metamorphs avoided chemical cues from crushed conspecifics, suggesting that the chemicals inducing this response might provide an opportunity to develop targeted control methods for this invasive species.     

Invasive species of crayfish use a broader range of predation-risk cues than native species

The responses of invasive and native species of crayfish to conspecific and heterospecific alarm odors were recorded in the laboratory. Individuals of the North American invasive Procambarus clarkii responded just as strongly to odors from crushed Austropotomobius pallipes as they did to crushed conspecifics. The North American invasive Orconectes limosus also responded as strongly to P. clarkii odor as to conspecific odor. The native Italian species A. pallipes responded more strongly to conspecific alarm than to heterospecific alarm from P. clarkii. The pattern of invasive species of crayfish using a broader range of danger signals than displaced native species appears to be robust.     

There must be something in the water: assessing the behavioral responses of rusty crayfish (<Emphasis Type="Italic">Orconectes rusticus</Emphasis>) to fish and amphibian predator kairomones

Animals use chemical cues to find food, locate mates, and detect potential predators. Detecting cues in a risky environment can induce behavioral changes to increase survival. Rusty crayfish (Orconectes rusticus) reduce activity, increase refuge use, and make defensive displays after detecting fish predator cues. However, no studies have introduced amphibian cues. We investigated crayfish responses to hellbender salamander (Cryptobranchus alleganiensis, a dominant predator of crayfish) cues and compared these to responses to largemouth bass (Micropterus salmoides) cues. Largemouth bass occur sympatrically with hellbenders and are known to induce distinct responses in rusty crayfish. We randomly assigned crayfish to predator cue and conspecific alarm cue combinations and recorded frozen behavior, appendage movement, locomotion, and refuge use. We found crayfish increased their proportion of time spent frozen and reduced their proportion of time spent active in the tank when exposed to either predator cue. Moreover, these responses were magnified when crayfish were exposed to predator cues in combination with conspecific alarm cues. Our experiment demonstrates evidence in support of the crayfish’s ability to detect and appropriately respond to predator cues alone and in combination with conspecific alarm cues. Future work should investigate the effects of these behavioral changes on trophic dynamics in a natural system.     

Predator (<Emphasis Type="Italic">Carcinus maenas</Emphasis>) nonconsumptive limitation of prey (<Emphasis Type="Italic">Nucella lapillus</Emphasis>) feeding depends on prey density and predator cue type

Predators often have nonconsumptive effects (NCEs) on prey. For example, upon detection of predator cues, prey can reduce feeding activities to hamper being detected by predators. Previous research showed that waterborne chemical cues from green crabs (Carcinus maenas, predator) limit the dogwhelk (Nucella lapillus, prey) consumption of barnacles regardless of dogwhelk density, even though individual predation risk for dogwhelks decreases with conspecific density. Such NCEs might disappear with dogwhelk density if dogwhelks feed on mussels, as mussel stands constitute better antipredator refuges than barnacle stands. Through a laboratory experiment, we effectively found that crab chemical cues limit the per-capita consumption of mussels by dogwhelks at low dogwhelk density but not at high density. The combination of tactile and chemical cues from crabs, however, limited the dogwhelk consumption of mussels at both dogwhelk densities. The occurrence of such NCEs at both dogwhelk densities could have resulted from tactile cues indicating a stronger predation risk than chemical cues alone. Overall, the present study reinforces the notions that prey evaluate conspecific density when assessing predation risk and that predator cue type affects their perception of risk.     

Migratory‐stage sea lamprey Petromyzon marinus stop responding to conspecific damage‐released alarm cues after 4 h of continuous exposure in laboratory conditions

This study investigated the length of avoidance response of migratory‐stage sea lamprey Petromyzon marinus exposed continuously to conspecific damage‐released alarm cues for varying lengths of time in laboratory stream channels. Ten replicate groups of P. marinus, separated by sex, were exposed to either deionized water control or to P. marinus extract for 0, 2 or 4 h continuously. Petromyzon marinus maintained their avoidance response to the conspecific damage‐released alarm cue after continuous exposure to the alarm cue for 0 and 2 h but not 4 h. Beyond being one of the first studies in regards to sensory–olfactory adaptation–acclimation of fishes to alarm cues of any kind, these results have important implications for use of conspecific alarm cues in P. marinus control. For example, continuous application of conspecific alarm cue during the day, when P. marinus are inactive and hiding, may result in sensory adaptation to the odour by nightfall when they migrate upstream.     

Anti‐predator response of naïve and experienced common bully to chemical alarm cues

Histological analysis of the skin of common bully Gobiomorphus cotidianus , a New Zealand native eleotrid fish, revealed the presence of club cells in the epidermis. Epidermal club cells are frequently associated with the production of alarm substance (Schreckstoff). The behavioural responses of perch‐naïve and perch‐experienced common bullies to either conspecific skin extract or chemical cues from an introduced predator, perch Perca fluviatilis , were then examined. Both perch‐naïve and perch‐experienced common bullies exhibited a behavioural response when exposed to conspecific skin extract, indicating the probable presence of an alarm substance. In contrast, only perch‐experienced common bullies recognized and exhibited a subsequent behavioural response to the odour of perch. This study is the first to document the presence of epidermal club cells and a behavioural response to a conspecific chemical alarm signal for fishes in the Eleotridae. The results indicate that common bully can learn to recognize perch odour as a threat, and that this ability may be a result of previous predator labelling involving a conspecific alarm substance.     

Underwater Video Reveals Strong Avoidance of Chemical Alarm Cues by Prey Fishes

A diversity of fishes release chemical cues upon being attacked by a predator. These cues, commonly termed alarm cues, act as sources of public information warning conspecifics of predation risk. Species which are members of the same prey guild (i.e. syntopic and share predators) often respond to one another's alarm cues. The purpose of this study was to discriminate avoidance responses of fishes to conspecific alarm cues and cues of other prey guild members from responses to unknown damaged fish odours and novel odours. We used underwater video to measure avoidance responses of freshwater littoral species, namely fathead minnows (Pimephales promelas), finescale dace (Chrosomus neogaeus), and brook stickleback (Culaea inconstans), to both injured fish cues and novel non‐fish odours. The cyprinids (minnows and dace) showed significant avoidance of minnow cues over swordtail cues, morpholine, and the control of distilled water and tended to avoid fathead cues over cues of known prey guild members (stickleback). Cyprinids also significantly avoided cues of stickleback over unknown heterospecific cues (swordtail) and tended to avoid stickleback cues over morpholine and the distilled water control. Stickleback significantly avoided fathead minnow extract over the distilled water and tended to avoid stickleback and swordtail over distilled water. We conclude that fishes in their natural environment can show dramatic changes in behaviour upon exposure to alarm cues from conspecifics and prey guild members. These responses do not represent avoidance of cues of any injured fish or any novel odour.