The mate pursuit-predation avoidance tradeoff in the virile crayfish, Orconectes virilis

To better understand the tradeoff between mate pursuit and predation risk avoidance, the responses of male virile crayfish (Orconectes virilis) to female sex pheromone and conspecific alarm cue, alone and in combination were tested. Male crayfish were more active and exhibited less antipredator behavior in the pheromone treatment than in either the pheromone + alarm or alarm treatment. The results suggest a tradeoff in favor of risk avoidance when pheromone and risk stimuli are encountered together.     

A Test of Temporal Variation in Risk and Food Stimuli on Behavioral Tradeoffs in the Rusty Crayfish, Orconectes rusticus: Risk Allocation and Stimulus Degradation

The effects of temporal variation in exposure to predation risk on behavioral tradeoffs were tested in the rusty crayfish, Orconectes rusticus. Based on the risk allocation hypothesis, we predicted that increasing the frequency of encounter with predation risk would yield increasing responses to a food stimulus in the presence of both a risk stimulus and a food stimulus. Crayfish were exposed to risk every 12 h, every 6 h, or left undisturbed for 24 h prior to testing. The risk stimuli used were a plain water control, snapping turtle (Chelydra serpentina) cue, and conspecific alarm cue. After 24 h of conditioning, the crayfish were exposed to a combination of risk cue and food cue. The behavioral responses of the crayfish were recorded for 5 min immediately following the introduction of the cues and again for 5 min, 1 h after stimulus exposure. The crayfish were observed at the two times to determine how their responses to the combination of risk and food cues changed over time. The responses of the crayfish were significantly influenced by stimulus treatment, time, and the interaction of time and stimulus treatment. Further analysis indicated that responses to the stimulus treatments changed differently over time. Immediately after exposure, the crayfish were more active in the control and snapping turtle treatments than in the conspecific alarm treatment. The high levels of activity initially observed in the control and snapping turtle treatments waned over time, such that the behaviors recorded 1 h after exposure were not significantly affected by stimulus treatment. Neither frequency nor the interactions of frequency with stimulus and/or time significantly affected crayfish behavior. The results of this study did not support the risk allocation model and contrast with results from similar work on the virile crayfish, Orconectes virilis.     

Multiple predator-avoidance behaviours of the freshwater snail Physella heterostropha pomila: responses vary with risk

• 1 We examined the predator‐avoidance behaviour, exhibited in response to chemical cues, of two populations of the snail Physella heterostropha pomila. Snails were subjected to four treatments simulating different degrees of predation risk: control water (low risk), or water from tanks containing nonforaging crayfish (intermediate risk), crushed conspecifics (high risk) or crayfish consuming conspecifics (high risk). Data were analysed using three‐way ANOVA models (population × predator chemicals × injured conspecific chemicals).
• 2 Physella increased its avoidance behaviour as risk increased. Crayfish cue elicited a significantly greater response than from controls. Cues from injured conspecifics elicited the strongest response.
• 3 Physella exhibited several types of avoidance behaviour, including burial into the substratum, moving to the water surface, and crawling out of the water. The type of cue present influenced response type. Cues from crayfish reduced burial and increased movement to the water surface or out of the water. Cues from injured‐conspecifics significantly increased crawling completely out of the water.
• 4 The two populations differed in the type and degree of response exhibited. One population exhibited significantly greater ‘reactivity’ (i.e. any avoidance behaviour) in response to foraging crayfish, and more burial and crawl‐out behaviours were exhibited in high‐risk treatments.

     

Alate production in an aphid in relation to ant tending and alarm pheromone

1. Winged dispersal is vital for aphids as predation pressure and host plant conditions fluctuate. 2. Ant‐tended aphids also need to disperse, but this may represent a cost for the ants, resulting in an evolutionary conflict of interest over aphid dispersal. 3. The combined effects of aphid alarm pheromone, indicating predation risk, and ant attendance on the production of winged aphids were examined in an experiment with Aphis fabae (Homoptera: Aphididae) (Scopoli 1763) aphids and Lasius niger (Formicidae: Formicinae) (Linné, 1758) ants. 4. This study is the first to investigate the joint effects of alarm pheromone and ant attendance, and also the first to detect an influence of alarm pheromone on the production of winged morphs in A. fabae. 5. After a period of 2 weeks, it was found that aphid colonies exposed to intermittent doses of alarm pheromone produced more winged individuals, whereas ant tending had the opposite effect. The effects were additive on a log scale, and ant attendance had a greater proportional influence than exposure to alarm pheromone. A tentative conclusion is that ants have gained the upper hand in an evolutionary conflict about aphid dispersal.     

Has the Attraction of Predatory Coccinellids to Cornicle Droplets Constrained Aphid Alarm Signaling Behavior?

When attacked by a predator, aphids of many species secrete cornicle droplets, containing an alarm pheromone, that results in the dispersal of nearby conspecifics. As females are parthenogenetic, alarm signaling functions to enhance the survival of clone-mates. Enigmatically, however, aphids are physically able to, but usually do not emit alarm pheromone when initially detecting a predator, but rather signal only when captured by a predator. We hypothesized that cornicle droplets may be attractive to natural enemies and result in an increased risk of predation for the signaler, thereby selecting for prudent alarm signalers. We tested this hypothesis by investigating the olfactory cues that the multicolored Asian ladybird beetle, Harmonia axyridis Pallas, uses to locate pea aphids, Acyrthosiphon pisum. In choice tests, H. axyridis were attracted to odors from pea aphid colonies, whether feeding or not feeding on a host plant leaf, but were not attracted to cornicle droplets containing alarm pheromone. Further, individual pea aphids emitting cornicle droplets were not located more often or in a shorter period of time by beetles than aphids not emitting cornicle droplets. Thus, the cost of emitting early alarm signals is not prohibitively high in regards to the attraction of predators such as H. axyridis.     

Cues of Predation Risk Induce Instar‐ and Genotype‐Specific Changes in Pea Aphid Colony Spatial Structure

Deploying collective antipredator behaviors during periods of increased predation risk is a major determinant of individual fitness for most animal groups. Pea aphids, Acyrthosiphon pisum, which live in aggregations of genetically identical individuals produced via asexual reproduction warn nearby conspecifics of pending attack by secreting a volatile alarm pheromone. This alarm pheromone allows clone‐mates to evade predation by walking away or dropping off the host plant. Here, we test how a single alarm pheromone emission influences colony structure and defensive behavior in this species. Relative to control colonies, groups exposed to alarm pheromone exhibited pronounced escape behavior where many individuals relocated to adjacent leaves on the host plant. Alarm pheromone reception, however, also had subtle instar‐specific effects: The proportion of 1st instars feeding nearest the leaf petiole decreased as these individuals moved to adjacent leaves, while the proportion of 2nd–3rd instars feeding nearest the leaf petiole remained constant. Fourth instars also dispersed to neighboring leaves after pheromone exposure. Lastly, alarm pheromone reception caused maternal aphids to alter their preferred feeding sites in a genotype‐specific manner: Maternal aphids of the green genotype fed further from the petiole, while maternal aphids of the pink genotype fed closer to the petiole. Together, our results suggest that aphid colony responses to alarm pheromone constitute a diversity of nuanced instar‐ and genotype‐specific effects. These behavioral responses can dramatically change the spatial organization of colonies and their collective defensive behavior.     

A blend of formic acid,benzoic acid,and aliphatic alkanes mediates alarm recruitment responses in western carpenter ants,Camponotus modoc

Formicine ants in distress spray alarm pheromone which typically recruits nestmates for help. Studying the western carpenter ant, Camponotus modoc Wheeler (Hymenoptera: Formicidae), our objectives were to (1) determine the exocrine glands that contain alarm recruitment pheromone, (2) identify the key alarm recruitment pheromone components, and (3) ascertain the pheromone components that are discharged by distressed ants. In Y-tube olfactometer experiments, extracts of poison glands, but not of Dufour’s glands, elicited anemotactic responses from worker ants. Gas chromatographic-mass spectrometric analyses of poison gland extracts revealed the presence of (1) aliphatic alkanes (undecane, tridecane, pentadecane, heptadecane), (2) aliphatic alkenes [(Z)-7-pentadecene, (Z)-7- and (Z)-8-heptadecene], (3) two acids (formic, benzoic), and (4) other oxygenated compounds (hexadecan-1-ol, hexadecyl formate, hexadecyl acetate). Testing the responses of worker ants in Y-tube olfactometers to complete and partial synthetic blends of these compounds revealed that the acids and the alkanes are essential alarm pheromone components. In two-choice arena bioassays, micro-locations treated with synthetic alarm pheromone recruited worker ants. Acids and alkanes were abundant in the poison gland and the Dufour’s gland, respectively, suggesting that the alarm pheromone components originate from both glands. Moreover, alarm pheromone sprays of ants differed in that all sprays contained formic acid but only some also contained alkanes, implying that ants can independently discharge the content of either one or both glands in accordance with the type of distress incident they experience.     

The tradeoff between reproductive and food resources in the crayfish Orconectes virilis

The conflict between mating and foraging is one of the many tradeoffs associated with reproduction. The relative attraction to sex pheromone and food stimuli by male virile crayfish (Orconectes virilis) were tested using two experiments. In the first experiment, the responses by males to pheromone and food stimuli alone were assessed. In the second experiment, males were exposed to both pheromone and food stimuli in a choice maze. To determine the effects of feeding motivation, the males in the choice experiment were fed either one day or seven days prior to observation. Male crayfish exhibited similar responses to the pheromone and food stimuli individually. Males exhibited a preference for the pheromone stimulus over the food stimulus in the choice trials, and that preference that was not influenced by starvation.     

Assessment of local predation risk: the role of subthreshold concentrations of chemical alarm cues

The ability to accurately assess local predation risk is criticalto prey individuals, as it allows them to maximize threat-sensitivetrade-offs between predator avoidance and other fitness relatedactivities. A wide range of taxonomically diverse prey (includingmany freshwater fishes) relies on chemical alarm cues (alarmpheromones) as their primary information source for local riskassessment. However, the value of chemical alarm cues has beenquestioned due to the availability of additional sensory inputs(i.e., visual cues) and the lack of an overt antipredator responseunder conditions of low perceived risk. In this paper, we testthe hypothesis that chemical alarm cues at concentrations belowthe point at which they elicit an overt behavioral responsefunction to increase vigilance towards other sensory modalities(i.e., visual alarm cues). Shoals of glowlight tetras (Hemigrammuserythrozonus) exposed to the subthreshold concentration of hypoxanthine-3-N-oxide(the putative Ostariophysan alarm pheromone) did not exhibitan overt antipredator response in the absence of secondary visualcues (not different than the distilled water control). However,when exposed to the sight of a visually alarmed conspecific,they significantly increased the intensity of their antipredatorresponse (not different from shoals exposed to the suprathresholdalarm cue). This study demonstrates that prey may benefit fromresponding to low concentration alarm cues by increasing vigilancetowards secondary cues during local risk assessment, even inthe absence of an overt behavioral response. By increasing vigilancetowards secondary risk assessment cues in the presence of alow risk chemical cue, individuals are likely able to maximizethe threat-sensitive trade-offs between predator avoidance andother fitness related activities.     

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.     

Perception of alarm cues influences the outcome of shelter competition in crayfish20

The effects of predators on prey populations may significantly alter many aspects of prey biology, including spatial distribution, foraging activities, and social interactions. In aquatic habitats, chemosensation is an important mode of communication and has been shown for many taxa, including crayfish, to be used in detection of predator and/or conspecific alarm cues. Here, we report on an experiment to test the hypothesis that detection of alarm cues results in greater individual investment in contests over shelters. We tested this hypothesis through dyadic contests between sex- and size-matched, non-reproductive individuals of Faxonius virilis. We found that crayfish responded to exposure to alarm cues by spending more time inside a shelter. We also report that in contests between pairs in which one crayfish had been exposed to alarm cues and the other had not, exposed individuals were significantly more likely to win ownership of a single shelter. However, we did not detect any differences in the contest parameters we recorded between exposed and unexposed crayfish. These impacts on both individual and social behavior indicate that the presence of predators is likely to have large effects on the distribution and structure of crayfish populations.     

Frequency of Encounter with Risk and the Tradeoff between Pursuit and Antipredator Behaviors in Crayfish: A Test of the Risk Allocation Hypothesis

Prey animals encountering multiple stimuli must often make behavioral tradeoffs. Many environmental cues may influence the tradeoff observed, but recent theoretical work suggests that temporal variation in risk should influence how prey animals behave during any given period of risk. As time spent under risk of predation increases, prey animals will increase their allocation of foraging during periods of risk. This model is known as the risk allocation hypothesis (RAH) ( Lima & Bednekoff 1999 ). We tested the RAH using the crayfish Orconectes virilis. We selected two frequency regimes (exposure to risk every 6 or 12 h) and three cues suggestive of increasing risk (water, snapping turtle cue, and conspecific alarm cue). Test animals were exposed to one of the six frequency × risk combinations for 24 h, followed immediately by the simultaneous introduction of a food and a risk cue. Three behaviors (burrow use, non‐ambulatory motion, and locomotion) were then recorded for 5 min. Responses were significantly influenced by the interaction of risk and frequency. Further analysis indicated that responses were not consistently influenced by frequency alone. While our results do not support the predictions of the RAH for our frequency regimes, qualitative comparison with an earlier, similar study ( Hazlett 1999 ) suggests that risk allocation is occurring in this system. We recommend that frequency of encounter with risk be considered in future studies. Ignoring temporal variation may lead to over‐ or underestimation of the subject's natural responses.     

Predator Recognition and Learned Irrelevance in the Crayfish Orconectes virilis

When individuals of the crayfish Orconectes virilis detect an unlearned danger cue (alarm odor) and a novel cue (goldfish odor) at the same time, they form a learned association and behave as if the novel cue is associated with increased predation risk ( Hazlett et al. 2002 ). This study examined the potential for learned irrelevance in O. virilis and the circumstances under which blockage of the formation of a learned association could occur. If individuals experience a random pattern of alarm odor and goldfish odor over the days prior to the simultaneous detection of those two cues, no learned association is formed (= learned irrelevance). That is, there is no inhibition of responses to a food cue when goldfish odor is added if the crayfish has experienced a random pattern of the two cues. Learning was eliminated if the random pattern of cues was experienced before or after the simultaneous detection. To present the two cues (alarm and goldfish odors) to crayfish independently on separate days, the water containing goldfish odor had to be removed from the aquaria as the odor persisted at least 24 h. The importance of the learned irrelevance phenomenon on predator–prey interactions is discussed.     

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.     

Context‐dependent alarm signalling in an insect

Animals often respond to danger by raising alarm to inform others. Alarm signals come in many different forms, such as visual or mechanical display, sound or odour. Some animals produce vocal alarm signals that vary with the level of danger. For chemical alarm signals, virtually nothing is known about such context‐dependent signalling due to a general notion that alarm pheromones have fixed compositions. Here, we show that larvae of the Western Flower Thrips (Frankliniella occidentalis) produce an alarm pheromone whose composition varies with the level of danger they face: the presence of a relatively harmless predator or a very dangerous predator, that is either actually attacking or not. The frequency of alarm pheromone excretion increases with the level of danger. Moreover, the composition of excreted alarm pheromone varies in the relationship between total and relative amount of the putative two components, decyl acetate (DAc) and dodecyl acetate (DDAc). When pheromone is excreted with a predator present but not attacking, the percentage DDAc increases with the total amount of pheromone. When a predator does attack, however, the relationship between percentage DDAc and total amount of pheromone is reversed. Taken together, the alarm signal of thrips larvae appears to be context dependent, which to our knowledge is the first report of context‐dependent composition of an alarm pheromone.     

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.     

Preference-avoidance reactions of crayfish to sublethal concentrations of cadmium

The preference-avoidance reactions of the crayfish, Cambarus acuminatus, exposed to nominal cadmium concentrations of 125.0, 12.5, and 1.25 µCd⁺⁺/1 are examined. Pooled data from five trials at each treatment concentration demonstrate a statistically significant avoidance of the highest concentration, and preference for middle and lowest concentrations. Additional observations of behavior indicate that crayfish sense sublethal cadmium concentrations and respond to them with a general decrease in activity. Therefore, the use of crayfish locomotor activity as a potential parameter for continuous biological monitoring systems appears feasible.     

繁殖期4种淡水鱼类化学预警行为及其与性腺指数的关联

化学预警信息（Chemical alarm cue,CAC）在鱼类捕食者-猎物关系中发挥重要作用,并与二者生存适合度密切关联。繁殖期鱼类的繁殖生理投入和化学预警响应均具有较高的能量需求,因而可能存在某种程度上的生存-繁殖的权衡（Trade-off）。选取高体鳑鲏（Rhodeus ocellatus,卵生,繁殖投入较低）、斑马鱼（Danio rerio,卵生,繁殖投入较高）、孔雀鱼（Poecilia reticulata,卵胎生,繁殖投入较高）和皮球鱼（Poecilia latipinna,卵胎生,繁殖投入很高）等繁殖方式各异、能量投入不同的4种淡水鱼类为实验对象,测定了繁殖IV期实验鱼对不同浓度的化学预警信息（Damage-released chemical alarm cues,DCAC）的行为响应模式,并探究了4种实验鱼的化学预警响应与其性腺指数（Gonadosomatic index,GSI）的关联。结果表明：（1）DCAC对4种实验鱼的空间分布、活跃状态、逃逸行为等大部分化学预警响应参数均有不同程度的影响（P<0.05）;（2）4种实验鱼GSI与其化学预警响应参数的变化无显著相关性（P>0.05）（除高浓度DCAC处理组皮球鱼GSI与底栖时间的变化负相关外）。研究回答了长期以来有关繁殖期鱼类化学预警通讯是否缺失的问题,证实了繁殖期不同繁殖生理投入/繁殖对策的4种淡水鱼类均有显著的化学预警响应,提示鱼类GSI与其化学预警响应程度通常不相关（仅高风险环境下繁殖生理投入很高的物种中可能呈现负相关）。     

The behavioural responses of juvenile signal crayfish Pacifastacus leniusculus to stimuli from perch and eels

• 1 Experiments were designed to determine the relative importance of chemical and visual stimuli in eliciting predator avoidance behaviour in juvenile freshwater crayfish Pacifastacus leniusculus (Dana).
• 2 Crayfish placed in visual and/or chemical contact with one of two predators exhibited marked avoidance behaviour, spending less time walking and climbing and more time within shelters.
• 3 The combined effects of both visual and chemical stimuli increased crayfish shelter use and reduced walking and climbing activity to a greater degree than either stimulus when presented alone.
• 4 Crayfish exhibited avoidance behaviour in response to chemical stimuli during periods of light and darkness. Visual detection of predators elicited avoidance behaviour during the day.
• 5 It is suggested that the behavioural response of P. leniusculus to chemical stimuli reduces the likelihood of being detected by visual predators, and that chemical stimuli lower the response threshold for avoidance behaviour in crayfish reacting to visual stimuli. The adaptiviry of using chemical cues to detect predators is emphasized.

     

Food supplementation and predation risk in harsh climate: interactive effects on abundance and body condition of tit species

Food availability and predation risk can have drastic impacts on animal behaviour and populations. The tradeoff between foraging and predator avoidance is crucial for animal survival and will strongly affect individual body mass, since large fat reserves are beneficial to reduce starvation but may increase predation risk. However, two‐factor experiments simultaneously investigating the interactive effects of food and predation risk, are still rare. We studied the effects of food supplementation and natural predation risk imposed by pygmy owls Glaucidium passerinum on the abundance and fat reserves of tit species in boreal forests of north Europe, from January to March in 2012 and in 2013. Food supplementation increased the number of individuals present in a given forest patch, whereas the level of predation risk had no clear impact on the abundance of tit species. The stronger impact of food supply respect to predation risk could be the consequence of the harsh winter conditions in north Europe, with constant below‐zero temperatures and only few (5–7 h) daylight hours available for foraging. Predation risk did not have obvious effects on tit abundance but influenced food consumption and, together with food supplementation, affected the deposition of subcutaneous fat in great tits Parus major. High owl predation risk had detrimental effects on body fat reserves, which may reduce over‐winter survival, but the costs imposed by pygmy owl risk were compensated when food was supplemented. The starvation–predation tradeoff faced by great tits in winter may thus be mediated through variation in body fat reserves. In small species living in harsh environment, this tradeoff appeared thus to be biased towards avoidance of starvation, at the cost of increasing predation risk.