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     

Sublethal predation on Stylaria lacustris: a study of regenerative capabilities

Research on predator–prey interaction has generally ignored the possibility of prey injury by predator. Although injured prey usually constitute a minor group in a population, sublethal predation can play an important role in some aquatic assemblages. In a laboratory experiment, I tested the effect of attack by larvae of the damselfly Ischnura elegans and tanyponid Clinotanypus nervosus on the oligochaete Stylaria lacustris. Predation by these insect larvae caused damage to the prey which then are able to escape and survive. More than 50% of the worms used in the experiment were damaged by C. nervosus. Results of predation by I. elegans larvae of different lengths showed that the number of damaged worms decreased with the length of predatory larvae. Small predators injured more worms than large ones, which killed and totally consumed most of the prey. Damage to S. lacustris usually involves the loss of anterior, posterior or both these fragments (middle part preserved). An analysis of the survival of worms revealed that individuals which lost anterior, posterior, or both fragments survived equally well as control ones, with the exception of worms that lost 70% of the body length posteriorly amputated. It should be noted that these worms were the least numerous in all worms damaged by predators. The laboratory experiment on the regenerative capability of S. lacustris showed that after amputation, all worms regenerated the lost structures and started to increase in length. The small individuals after amputation of both anterior and posterior fragments achieved their initial length in the course of the experiment. It is likely that the regenerative capability in S. lacustris is an adaptation to sublethal effects of predation, which seems to play an important role in littoral assemblages dominated by oligochaetes.     

Influence of Body Size on the Responses of Fathead Minnows, Pimephales promelas, to Damselfly Alarm Cues

A wide diversity of aquatic organisms release chemical alarm cues upon encountering or being attacked by a predator. These alarm cues can be used by nearby individuals to assess local predation risk. Receivers warned by chemical alarm cues gain a survival benefit when encountering predators. Animals that are in the same prey guild (i.e. that co‐occur and share the same predators) may learn to recognize each others’ chemical alarm cues. This ability may confer an adaptive advantage if the prey animals are vulnerable to the same predators. However, if the prey grow to different sizes and as a consequence are no longer vulnerable to the same suite of predators, then there should no longer be an advantage for the prey to respond to each others’ alarm cues. In this study, we exposed small and large fathead minnows (Pimephales promelas) to cues from syntopic injured damselfly larvae (Enallagma boreale), cues from injured mealworm larvae (Tenebrio molitor) and to distilled water. Small minnows exhibited antipredatory behaviour and increased shelter use in response to injured damselfly cues but not to the controls of injured mealworm or distilled water. On the contrary, large minnows exhibited no significant change in shelter use in response to any of the injured cues. These data demonstrate that fathead minnows exhibit an antipredator response to damselfly alarm cues, but only when minnows are small and members of the same prey guild as damselfly larvae. These results demonstrate the considerable flexibility in the responses to heterospecific alarm cues.     

Effects of Chemical Cues on Foraging in Damselfly Larvae, <Emphasis Type="Italic">Enallagma antennatum</Emphasis>

Animals experiencing a trade-off between predation risk and resource acquisition must accurately predict ambient levels of predation risk to maximize fitness. We measure this trade-off explicitly in larvae of the damselfly Enallagma antennatum, comparing consumption rates in the presence of chemical cues from predators and injured prey. Damselflies distinguished among types of chemical cues based on species of prey injured or eaten. Injured coexisting heterospecific and unknown heterospecific chemical cues did not reduce foraging relative to starved predator cues, while cues arising from predators eating a coexisting heterospecific did decrease foraging. This study shows a cost in terms of reduced foraging in response to chemical cues and further defines the ability of prey to respond discerningly to chemical cues.     

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.     

Field Response of Tadpoles to Conspecific and Heterospecific Alarm

Many organisms use chemical cues from a variety of sources to mediate predator avoidance. Response to heterospecific alarm cues has been demonstrated for tadpoles within but not among taxa and alarm response behavior has seldom been examined under field conditions. This study examined the response of three sympatric amphibian larvae and predaceous larval Dytiscus sp. (diving beetle) to damage-release signals in natural ponds by using capture rates from treated funnel traps as an index of larval behavior. Hyla regilla (Pacific tree frog) tadpoles avoided traps treated with either crushed conspecifics or with Rana aurora (red-legged frog) tadpoles but the larger ranids and Ambystoma macrodactylum (long-toed salamander) did not respond to either treatment. H. regilla tadpoles were likely susceptible to any potential predators of ranid tadpoles in these ponds and this result is consistent with the hypothesis that a response to heterospecific alarm occurs in sympatric prey with shared predators.     

Anti-predator behaviour in response to conspecific chemical alarm cues in an esociform fish, <Emphasis Type="Italic">Umbra limi</Emphasis> (Kirtland 1840)

When a predators attack prey, damaged prey tissue releases chemical information that reliably indicates an actively foraging predator. Prey use these semiochemicals to cue anti-predator behaviour and reduce their probability of predation. Here, we test central mudminnows, Umbra limi (Kirtland 1840), for anti-predator behavioural responses to chemical cues in conspecific skin extract. In a field experiment, traps scented with mudminnow skin extract (alarm cue) caught fewer mudminnows than traps scented with water (control). Under controlled laboratory conditions, mudminnows showed a significant reduction in activity and movement to the bottom in response to alarm cues relative to water controls. Reduced activity and increased time on the bottom of the tank are both known components of an anti-predator response. Thus, based on field and lab data, mudminnows exhibited anti-predator behavioural responses to chemical alarm cues released by damaged epidermal tissue. Histological preparations of epidermal tissue did not reveal the presence of specialised “alarm substance” cells for the production of chemical alarm cues. This is the first report of an alarm reaction in an esociform, an order with a long evolutionary history of piscivory.     

The Effects of Density on the Learned Recognition of Heterospecific Alarm Cues

Numerous species, both aquatic and terrestrial, use alarm cues to mediate predation risk. These cues may be either intentionally or inadvertently released, and may be received by either conspecifics or heterospecifics. In aquatic systems, alarm cues are often chemical in nature and are released when an organism is disturbed or damaged by a predator. In some cases the recognition of alarm cues from conspecifics, or closely related heterospecifics, is innate, while the recognition of alarm cues from distantly related species must be learned. Many studies have documented the use of heterospecific alarm cues, but few have explored the manner in which these cues come to be recognized as an indication of predation. In the current study, we examined the fathead minnow (Pimephales promelas)/brook stickleback (Culaea inconstans) alarm system. We tested the effect of density on the ability of minnows to learn to recognize stickleback alarm cues as a threat. We hypothesized that the ability of minnows to learn to recognize stickleback alarm cues should increase with increasing stickleback density because there would be more opportunity for minnows to associate the heterospecific alarm cue with the threat. To test this hypothesis we stocked minnows into large outdoor pools with no stickleback, low numbers of stickleback, or high numbers of stickleback. All pools contained a predator (pike, Esox lucius) known to the minnows. Following a 14 d conditioning period, minnows were tested for a response to skin extract from stickleback, minnow, and an unknown heterospecific (swordtail, Xiphophorus helleri). Minnows from pools with large numbers of stickleback learned to respond to stickleback alarm cues while minnows from pools with low numbers of stickleback, or no stickleback, did not.     

Predator induced life-history shifts in a freshwater cladoceran

Summary Life-history theory predicts that maturity and resource allocation patterns are highly sensitive to selective predation. Under reduced adult survival, selection will favour genotypes capable of reproducing earlier, at a smaller size and with a higher reproductive effort. When exposed to water that previously held fish, (size selective predators which prefer larger Daphnia), individuals of Daphnia hyalina reproduced earlier, at a smaller size and had a higher reproductive investment. Hence the prey was able to switch its life history pattern in order to become less susceptible to predation by a specific predator. The cue that evokes the prey response is a chemical released by the predator.     

Chemical cues from multiple predator-prey interactions induce changes in behavior and growth of anuran larvae

Chemical signals are used as information by prey to assess predation risk in their environment. To evaluate the effects of multiple predators on prey growth, mediated by a change in prey activity, I exposed small and large bullfrog (Rana catesbeiana) larvae (tadpoles) to chemical cues from different combinations of bluegill sunfish (Lepomis macrochirus) and larval dragonfly (Anax junius) predators. Water was regularly transferred from predation trials (outdoor experiment) to aquaria (indoor experiment) in which activity and growth of tadpoles was measured. The highest predation mortality of small bullfrog larvae in the outdoor experiment was due to Anax, and it was slightly lower in the presence of both predators, probably resulting from interactions between predators. There was almost no mortality of prey with bluegill. The activity and growth of small bullfrog larvae was highest in the absence of predators and lowest in the presence of Anax. In the presence of bluegill only, or with both predators, the activity and growth of small bullfrog tadpoles was intermediate. Predators did not affect large tadpole activity and growth. Regressing mortality of small bullfrog tadpoles against activity and growth of bullfrog tadpoles revealed a significant effect for small bullfrog larvae but a non-significant effect for large bullfrog larvae. This shows that the response of bullfrog tadpoles to predators is related to their own body size. The experiment demonstrates that chemical cues are released both as predator odor and as alarm substances and both have the potential to strongly alter the activity and growth of prey. Different mechanisms by which chemical cues may be transmitted to species interactions in the food web are discussed. Received: 28 June 1999 / Accepted: 15 November 1999     

Cue reliability, risk sensitivity and inducible morphological defense in a marine snail

Reliable cues that communicate current or future environmental conditions are a requirement for the evolution of adaptive phenotypic plasticity, yet we often do not know which cues are responsible for the induction of particular plastic phenotypes. I examined the single and combined effects of cues from damaged prey and predator cues on the induction of plastic shell defenses and somatic growth in the marine snail Nucella lamellosa. Snails were exposed to chemical risk cues from a factorial combination of damaged prey presented in isolation or consumed by predatory crabs (Cancer productus). Water-borne cues from damaged conspecific and heterospecific snails did not affect plastic shell defenses (shell mass, shell thickness and apertural teeth) or somatic growth in N. lamellosa. Cues released by feeding crabs, independent of prey cue, had significant effects on shell mass and somatic growth, but only crabs consuming conspecific snails induced the full suite of plastic shell defenses in N. lamellosa and induced the greatest response in all shell traits and somatic growth. Thus the relationship between risk cue and inducible morphological defense is dependent on which cues and which morphological traits are examined. Results indicate that cues from damaged conspecifics alone do not trigger a response, but, in combination with predator cues, act to signal predation risk and trigger inducible defenses in this species. This ability to “label” predators as dangerous may decrease predator avoidance costs and highlights the importance of the feeding habits of predators on the expression of inducible defenses.     

Friends in Low Places: Responses of a Benthic Stream Fish to Intra‐Prey‐Guild Alarm Cues

Many aquatic species produce chemical alarm cues that serve as a warning to nearby conspecifics. In mixed‐species aggregations, individuals may also benefit by ‘eavesdropping’ on the chemical alarm cues of other species that are in the same prey guild. Rainbow Darters (Etheostoma caeruleum) are benthic fish that co‐occur with native Ozark Minnows (Notropis nubilus), recently introduced Western Mosquitofish (Gambusia affinis), and native Oklahoma Salamanders (Eurycea tyrnerensis), all of whom are vulnerable to the same predators. We tested the responses of darters to the damage‐released alarm cues of conspecifics (positive control), minnows, and mosquitofish; alarm cues from Bumblebee Gobies (Brachygobius doriae) served as a negative (allopatric) control. We also tested the response of sympatric and allopatric darters to the damage‐released alarm cues of Oklahoma Salamander. Darters exhibited a fright response to conspecific and minnow alarm cues, but not to cues from mosquitofish or gobies. Lack of response to mosquitofish cues could be because they are introduced or because they typically occur higher in the water column than darters. Darters that were sympatric with the salamander exhibited a fright response to the alarm cues of the salamander, while allopatric darters did not. Rainbow Darters can develop responses to the alarm cues of syntopic species (minnows and Oklahoma Salamander) within their prey guild.     

水生生态环境中捕食信息素的生态学效应

捕食信息素是捕食者释放的,能够引发猎物反捕食反应的化学信号。在水生生态系统中,捕食信息素在捕食者和猎物之间信息传递及协同进化过程中发挥着重要的作用,其生态学效应在国际上受到广泛关注。捕食信息素的来源有多种形式,研究中常使用养殖过捕食者的水溶液作为捕食信息素的来源。捕食信息素的作用效果受到捕食者和猎物的种类、信息素的浓度、观察的指标等多方面因素的影响。捕食信息素可以对水生生物的行为、形态和生活史特征等方面造成影响。水生生物通过感知捕食信息素来提前预知潜在的被捕食风险,并作出适应性调整,以降低被捕食的风险。在某些情况下,捕食信息素可以与污染物产生交互作用,从而干扰污染物对水生生物的毒性。对水生环境中捕食信息素的研究现状做了综述,介绍了当前对捕食信息素来源和理化性质等本质问题的认识,总结捕食信息素对水生生物行为、形态和生活史特征的影响,以及捕食信息素对污染物毒性的干扰,并分析了这一研究领域尚存在的困难和今后的研究方向。加强对捕食信息素的研究,将为解析水生环境中捕食者和猎物的生态关系提供新依据。     

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     

Predators marked with chemical cues from one prey have increased attack success on another prey species

1. To reduce the risk of being eaten by predators, prey alter their morphology or behaviour. This response can be tuned to the current danger if chemical or other cues associated with predators inform the prey about the risks involved. 2. It is well known that various prey species discriminate between chemical cues from predators that fed on conspecific prey and those that fed on heterospecific prey, and react stronger to the first. It is therefore expected that generalist predators are more successful in capturing a given prey species when they are contaminated with chemical cues from another prey species instead of cues from the same prey species. 3. Here, a generalist predatory mite was studied that feeds on thrips larvae as well as on whitefly eggs and crawlers. Mites were marked with cues (i.e. body fluids) of one of these two prey species and were subsequently offered thrips larva. 4. Predators marked with thrips cues killed significantly fewer thrips than predators marked with whitefly cues, even though the predator's tendency to attack was the same. In addition, more thrips larvae sought refuge in the presence of a predatory mite marked with thrips cues instead of whitefly cues. 5. This suggests that generalist predators may experience improved attack success when switching prey species.     

Avoidance behavior in two sympatric planaria species: effects of conspecific and heterospecific chemical alarm cues

In many aquatic animals, predator avoidance can be stimulated by chemical cues, including those released by injured prey (alarm cues). Alarm cues of both conspecific and heterospecific origin have been identified within several fish taxa, where phylogenetic conservation of the cue-response complex is common. Turbellarian flatworms (planaria) are among the simplest animals known to respond to chemical cues released by injured conspecifics. We examined how two locally sympatric planaria species respond to conspecific and heterospecific chemical cues using macerated tissue suspensions. Brown (Girardia tigrina) and black (Dugesia dorotocephala) planaria both exhibited avoidance behavior when presented conspecific cues. Despite a significant twofold difference in body size (black > brown), stimulus prepared from a single (1×) individual of either species elicited avoidance. Increasing brown planaria cue concentration by macerating two individuals (2×) produced a significant increase in conspecific avoidance. Heterospecific stimuli produced asymmetric results. Black planaria avoided the brown planaria stimulus, but only in the higher concentration (2×) trials. Brown planaria did not consistently exhibit avoidance of the black planaria stimulus and some brown subjects approached and consumed black planarian tissues. Our results expand the demonstrated occurrence of alarm cues among planaria and suggest that avoidance behavior can be mediated by multiple environmental and intrinsic factors in freshwater Turbellaria.     

The Diel Activity of Crucian Carp, Carassius Carassius, in Relation to Chemical Cues from Predators

Chemical cues from piscivorous fish and prey alarm substances often cause rapid fright responses in prey. However little is known of how piscivore-related chemical cues affect prey behaviour over periods longer than a few hours. Here we have investigated how chemical cues from piscivorous northern pike, Esox lucius, affect habitat choice and diel activity of crucian carp, Carassius carassius, over an extended period 11 days. At the beginning of the experiment control fish were nocturnal while fish in the pike cue treatment were aperiodic. After 11 days, control fish had become more strongly nocturnal and displayed two activity peaks during early and late night whereas fish in the pike cue treatment were still aperiodic with no activity peaks. Habitat choice was aperiodic in both treatments throughout the experiment. In both treatments, more fish were found in the vegetation zone than in the open habitat. This was most pronounced when pike cues were present. These results demonstrate that short-term anti-predator responses to chemical cues from predators can translate into long-term adjustments of diel periodicity. Further, the results did not support the idea that crucian carp should switch to nocturnal activity in response to visually hunting predators. Control fish were nocturnal and chemical cues from pike did not make this pattern more pronounced.     

Costs of Predator Avoidance Reduce Competitive Ability of Daphnia

Large-sized Daphnia hyalina×galeata hybrid and small-sized Ceriodaphnia reticulata were raised together for 3 weeks in thermally stratified flow-through tubes ('plankton organ'), in the presence and the absence of fish kairomone, and their relative performance was monitored, as indicated by the populations' growth rates (r). In the kairomone-free medium, D. hyalina grew faster than C. reticulata; the presence of kairomone reversed this ratio, producing relatively higher r in C. reticulata. The simulated fish presence reduced growth in D. hyalina population also when it was separated from the competitor, while growth in C. reticulata was altered by the kairomone only in the presence of Daphnia. It is suggested that costs of surface avoidance in Daphnia can reduce its competitive superiority to small-sized cladocerans, permanently dwelling at the surface.     

Evidence for the Predator Attraction Hypothesis in an amphibian predator–prey system

Many species possess damage-released chemical alarm cues that function in alerting nearby individuals to a predator attack. One hypothesis for the evolution and/or maintenance of such cues is the Predator Attraction Hypothesis, where predators, rather than prey, are the “intended” recipients of these cues. If a predator attack attracts additional predators, these secondary predators might interfere with the predation event, providing the prey with a better chance to escape. In this study, we conducted two experiments to explore this hypothesis in an amphibian predator/prey system. In Experiment 1, we found that tiger salamanders (Ambystoma mavortium) showed a foraging attraction to chemical cues from wood frog (Lithobates sylvaticus) tadpoles. Salamanders that were experienced with tadpole prey, in particular, were strongly attracted to tadpole alarm cues. In Experiment 2, we observed experimental encounters between a tadpole and either one or two salamanders. The presence of the second predator caused salamanders to increase attack speed at the cost of decreased attack accuracy (i.e., increasing the probability that the tadpole would escape attacks). We also found that the mere presence of visual and chemical cues from a second predator did not affect this speed/accuracy trade-off but did cause enough of a distraction to increase tadpole survival. Thus, our findings are consistent with the Predator Attraction Hypothesis for the evolution and/or maintenance of alarm cues.     

Identifying century-old long-spined <Emphasis Type="Italic">Daphnia</Emphasis>: species replacement in a mountain lake characterised by paleogenetic methods

Mountain lakes often harbour morphologically or genetically unique populations of zooplankton species, including cladocerans. Daphnia lacustris Sars, predominantly found in Fennoscandia but also known from two Central European lakes in the Tatra Mountains, is one of such taxa. This Daphnia species often forms morphotypes with extremely long tailspines. Historical literature from a century ago documented similar morphs from another lake in the Tatra mountain range, presently inhabited by the phenotypically very different D. galeata. Using a paleogenetic approach (partial sequencing of the mitochondrial gene for 12S rRNA from preserved ephippial eggs in the lake sediment), we tested the hypothesis that Daphnia species composition changed in the lake due to anthropogenic disturbances, and that long-spined morphs were actually another relict population of currently extinct D. lacustris. Ephippia with extremely long spines were successfully retrieved from sediment cores. Despite being morphologically very well preserved, intact eggs were found in less than 2% of analysed ephippia. Genetic analyses, benefiting in most cases from amplification of short 12S fragments using internal primers, proved that long-spined ephippia belonged to D. longispina, which apparently coexisted with D. galeata in the mid-twentieth century. Our results confirm that paleogenetic methods are useful for studying the recent population structures of zooplankton species forming dormant egg banks but lacking reliably identifiable remains in sediments, and show that the extreme development of tailspines in mountain-lake Daphnia is associated with as-yet unclear environmental factors rather than taxonomic status.