Threat-sensitive generalization of predator recognition by larval amphibians

Despite the importance of acquired predator recognition in mediating predator–prey interactions, we know little about the specific characteristics that prey use to distinguish predators from non-predators. Recent experiments with mammals and fish indicate that some prey lacking innate predator recognition have the ability to display anti-predator responses upon their first encounter with those predators if they are similar to predators that the prey has recently learned to recognize. This phenomenon is referred to as generalization of predator recognition. In this experiment, we documented for the first time that larval amphibians (woodfrog, Rana sylvatica) have the ability to generalize the recognition of known predators to closely related novel predators. Moreover, we demonstrated that this ability is dependent on the level of risk associated with the known predator. When red-bellied newt, Cynops pyrrhogaster (known predator), was paired with simulated low risk, tadpoles displayed fright responses to newts and novel tiger salamanders, Ambystoma tigrinum, but not to novel African clawed frogs, Xenopus laevis. However, when the newt was paired with simulated high risk, tadpoles generalized their responses to both tiger salamanders and African clawed frogs. Larval anurans seem to have a wider generalization frame than other animals.     

Effects of relaxed predation pressure on visual predator recognition in the guppy

Many prey species have a genetic predisposition to recognise and respond to predators and can fine-tune their anti-predator behaviour following appropriate experience. Although the Trinidadian guppy ( Poecilia reticulata) has become a model species for the investigation of adaptive behaviour, the extent to which experience mediates predator recognition remains unclear. In this study, we examined the effects of relaxed predation pressure on patterns of anti-predator behaviour in populations differing in evolutionary history. The anti-predator behaviour of wild- and laboratory-born guppies from high- and low-predation localities in Trinidad were compared using three models resembling Crenicichla alta, a dangerous guppy predator, Aequidens pulcher, a less dangerous piscivore, and a snake. Snakes are not known to prey on guppies in Trinidad. Specifically, the following predictions were tested: (1) wild caught fish from the high-predation localities (where guppies co-occur with C. alta and A. pulcher) would respond to the three models according to their perceived level of threat, whereas guppies from the low-predation site would show a reduced response to all of the predator models; (2) high-predation laboratory-reared fish would display a reduced but qualitatively similar response to their wild counterparts; and (3) there would be no behavioural differences between wild- and laboratory-reared low-predation fish. In accordance with these predictions, the results revealed that wild fish originating from high-predation sites responded more strongly to the models than fish from low-predation sites. When reared in the laboratory, guppies from the high-predation population showed a reduced response compared to their wild-caught counterparts, but there was no difference in the behaviour of wild- and laboratory-reared low-predation fish. Model type affected predator inspection behaviour but not schooling tendency, and both wild- and laboratory-reared guppies were more wary of the fish models than the snake. These results suggest that early experience differentially mediates the anti-predator responses of fish from high-risk localities.     

Patterns of shell repair in articulate brachiopods indicate size constitutes a refuge from predation

The cost of overcoming prey defenses relative to the value of internal tissues is a key criterion in predator/prey interactions. Optimal foraging theory predicts: (1) specific sizes of prey will result in the best returns to predators, and (2) there will often be a size at which the cost/benefit balance is low enough to effectively exclude predation. Data presented here on styles of repaired shell damage and size at which injury had been sustained was collected from samples of terebratulide brachiopods from the Antarctic Peninisula (Liothyrella uva), Falkland Islands (Magellania venosa and Terebratella dorsata) and Chile (M. venosa). The predominant form of damage on shells was indicative of predators attacking the valve margins. The modal size for repaired damage was more than 10 mm smaller than the modal size for the overall size distribution in each species and there were no repaired attacks in the largest size classes of any species. These data suggest that size forms a refuge from predation, as would be predicted by optimal foraging theory. The optimal sizes that predators appeared to attack vary between species, as do the sizes that provided a refuge from predation. High levels of multiple repairs (19% of the M. venosa population from the Falkland Islands sampled had 2 or more repairs) suggest that the mortality following attack is low, suggesting that many predators abandon their attacks.     

Pyrrolizidine alkaloids on three trophic levels – evidence for toxic and deterrent effects on phytophages and predators

Summary. Pyrrolizidine alkaloids (PAs) present a model system in the investigation of tritrophic interactions mediated by plant secondary compounds. However, their toxicity for insect herbivores has never been experimentally proven. Here, we demonstrate the toxic effects of a PA on growth and survival of the eri silk moth Philosamia ricini. In a feeding experiment, larvae of this generalist herbivore fed with an artificial PA diet gained weight significantly slower than control animals, and died as pupae. We suggest that derivatives of the ingested PA N-oxide damage developmental functions during metamorphosis. A tracer test with [¹⁴C]senecionine N-oxide revealed that the caterpillars lack adaptations that would prevent conversion of the chemical into the pro-toxic free base. In contrast, the PA adapted leaf beetle Longitarsus anchusae accumulates PAs as N-oxides. We tested the purpose of sequestration in this species as defence against predators. Through a series of prey choice experiments with three carabid predator species, chemically non-protected bark beetle pupae were chosen almost uniformly over L. anchusae pupae. In a following choice test with one of these predators, artificially PA-treated mealworm segments deterred the predator from feeding. Overall the study corroborates the immediate toxic effect of PAs on non-adapted herbivores and the protective effect that adapted insects may gain by sequestering them. It thereby underlines the potential for PAs to play a central role in multitrophic interactions between plants, phytophages and their predators.     

The peculiar case of an insectivorous iguanid lizard that detects chemical cues from prey

Summary. Ecological and phylogenetic factors determine which sensory modalities organisms use in their day-to-day activities. Among lizards, empirical studies indicate a tight association between foraging strategies and the ability to detect chemical cues from prey. Consequently, ambush insectivores do not detect food chemicals and these differences have a phylogenetic basis, as ambush lizards mainly belong to the Iguania clade. These data contrast, however, with the widespread uses of chemoreception in the Iguania genus Liolaemus, which are mostly insectivorous ambush predators. Moreover, observations from different Liolaemus species suggest a capability to find prey through chemoreception. In order to clarify the abilities of Liolaemus to detect chemical cues from prey, the chemoreceptive behavior of the insectivorous ambush predator, L. lemniscatus, was studied. Lizards were given the choice between areas with and without chemical cues from a food item (mealworms). Results show that test animals stayed for longer, moved more, and did more chemical exploration (tongue flicks) in the area where chemical cues from mealworms were present. Furthermore, in this area, more individuals displayed behaviors that suggest maintenance and defense of the prey patch. Thus, L. lemniscatus is the first insectivorous Iguania reported to be able to detect chemical cues from prey. Although I propose a mechanism for acquiring chemical detection of prey cues in Liolaemus, I also remark that it is necessary to reanalyze both the abilities to detect and use chemical foraging cues in Iguania at large, and the methodologies traditionally used to study these issues.     

Defence effectiveness of easy bleeding sawfly larvae towards invertebrate and avian predators

Summary. Easy bleeding is a phenomenon discovered in some tenthredinid insects which possess a particularly low mechanical resistance of the integument, leading under mechanical stress to haemolymph exudation. It has a defensive effect against ants and wasps through harmful plant compounds which are sequestered in the haemolymph. Here we describe etho-ecological and some chemical aspects of the defence of easy bleeders and specify the range of predators to which easy bleeding might be effective. Beside a high haemolymph deterrence associated with low integument resistance across sawfly species, we also detected toxicity of the haemolymph of some species to workers of the ant Myrmica rubra. The behaviour of easy bleeders is to move slowly and, once disturbed, to become motionless, thereby probably impeding the tendency of a predator to attack. This behaviour had no beneficial effect for easy bleeders when attacked by the predatory bug Podisus maculiventris. Bugs could successfully and without harm prey on sawfly larvae without evoking easy bleeding. For the easy bleeder Athalia rosae, host plants with different secondary metabolite profiles, and, consequently, changes in haemolymph chemistry only slightly affected the feeding behaviour of the bugs. To test the effectiveness of easy bleeding towards a vertebrate predator, easy bleeders were offered to birds, Sturnus vulgaris. The body colouration of the sawfly larvae was of prime importance in determining the predators response when testing birds in a group. It is likely that easy bleeding is a defence strategy directed primarily towards foraging insects with biting-chewing mandibles and that it is much less active towards predatory insects with piercing-sucking mandibles as well as birds. The involvement of chemical and/or physical cues in the strategy is discussed with respect to these types of predators.     

Threat-sensitive learning of predators by larval mosquitoes <Emphasis Type="Italic">Culex restuans</Emphasis>

A prerequisite for prey to show adaptive behavioural responses to predators is that the prey has the ability to recognise predators as threats. While predator recognition can be innate in many situations, learning is often essential. For many aquatic species, one common way to learn about predators is through the pairing of a novel predator odour with alarm cues released from injured conspecifics. One study with fish demonstrated that this mode of learning not only allows the prey to recognise the predatory cues as a threat, but also mediates the level of threat associated with the predator cues (i.e. threat-sensitive learning). When the prey is exposed to the novel predator with a high concentration of alarm cues, they subsequently show a high intensity of antipredator response to the predator cues alone. When exposed to the predator with a low concentration of alarm cues, they subsequently show a low-intensity response to the predator cues. Here, we investigated whether larval mosquitoes Culex restuans have the ability to learn to recognise salamanders as a threat through a single pairing of alarm cues and salamander odour and also whether they would learn to respond to salamander cues in a threat-sensitive manner. We conditioned individual mosquitoes with water or a low, medium or high concentration of crushed conspecific cues (alarm cues) paired with salamander odour. Mosquitoes exposed to salamander odour paired with alarm cues and subsequently exposed to salamander odour alone responded to the salamander as a threat. Moreover, the intensity of antipredator response displayed during the conditioning phase matched the response intensity during the testing phase. This is the first demonstration of threat-sensitive learning in an aquatic invertebrate.     

An overlooked side effect of nest-scattering behavior to decrease predation risk (Acari: Tetranychidae,Stigmaeidae)

The number of nests containing egg masses a female makes over her lifetime and the pattern of scattering nests vary among species in a genus of nest-weaving spider mites (Stigmaeopsis). We hypothesized that the scattered nests of small nest builders have a previously overlooked indirect effect in that the void nests created after predation take on a new role as hindering devices that effectively decrease predator searching efficiency. First, we demonstrated that the experimental design used in this study is a good reflection of the nest distribution pattern of Stigmaeopsis takahashii (an intermediate-sized nest builder) in the field. Using this species as a model, we tested how different nest-scattering patterns affect the predator to examine how scattering may indirectly provide an anti-predation strategy by increasing a predators searching time. Next, we observed how artificially arranged void nests disturb predatory behavior in both starved and fully fed predator females and showed that void nests have a strong hindering effect on predators. Thus, we concluded that the nesting behavior of this mite species not only has anti-predator effects but must also have a stabilizing effect on predator–prey interaction systems at the population level.     

Species-specific antipredatory behaviours: effects on prey choice in different habitats

Summary Prey species may use many different behaviours to avoid predation. In this study, the antipredator behaviours of juvenile roach (Rutilus rutilus) and juvenile perch (Perca fluviatilis) were studied in wading pools with three kinds of structural complexity: no structure, structure simulating vegetation and structure simulating bottom crevices. Predation experiments with piscivorous perch and habitat choice experiments with the prey were performed, and the foraging success and prey choice of the predators were related to the type of structure. Predator foraging success was lower in the vegetation than in the other treatments. In the absence of structure and with vegetation structure, predators preferred perch over roach, while the preference was reversed in the crevice treatment. Roach and perch differed in their antipredatory behaviours. Roach responded to the presence of predators by schooling, moving fast and remaining at the surface, and escaped from attacks by jumping out of the water. In contrast, perch moved more slowly, dispersed after attacks and tried to hide at the bottom. Perch always preferred the vegetation structure to the non-structured part of the pool, while roach showed preference for the vegetation structure only when predators were present. Roach never occurred in crevices, whereas perch used crevices when predators where present. Predator pursuit speed was lower in the vegetation structure than in the non-structured treatment, but prey escape speed was unaffected. The results suggest that both the quantity and quality of structural complexity interacting with species-specific antipredator behaviours are important for predator-prey dynamics. It is also suggested that the presence of structure can have substantial effects on the structure of North Eurasian fish communities, by affecting relative and absolute predation pressures from piscivorous perch on prey species. Correspondence to: B. Christensen     

Escape take-off strategies in birds: the significance of protective cover

Avian escape strategy is highly dependent on the ability to fly, and the success rate of raptor attacks is reduced if the prey gets fully airborne. Therefore, when escaping from predator attacks, the initial take-off is crucial and a rapid take-off, high velocity, and high angle of ascent maximize the chance of survival. However, due to the laws of gravity, birds face a trade-off between maximizing its linear acceleration and maximizing its rate of climb when taking off. The optimal policy between velocity and angle of ascent when a bird escapes from an attacking predator might depend on the detailed nature of the predator’s attack, the proximity to cover, and the presence of conspecifics. Many small birds rely on a quick dash to protective cover. In this study, we examine how the availability of protective cover affects take-off strategy in birds. Male great tits (Parus major) were subjected to a surprise attack by a model predator either in the presence or absence of protective cover. When attacked by the predator, great tits took off and perched in the cover when it was available. Birds subjected to the predator attack in the absence of cover took off in 10° higher angle of ascent and flew faster in the start of the take-off, compared to birds that took off in the presence of cover. Thus, this study for the first time shows that a bird do trade off speed with angle of ascent in an adaptive way, depending on the presence of protective cover.     

The interplay between foraging mode, habitat structure, and predator presence in antlions

Antlion larvae are sand-dwelling insect predators, which ambush small arthropod prey while buried in the sand. In some species, the larvae construct conical pits and are considered as sit-and-wait predators which seldom relocate while in other species, they ambush prey without a pit but change their ambush site much more frequently (i.e., sit-and-pursue predators). The ability of antlion larvae to evade some of their predators which hunt them on the sand surface is strongly constrained by the degree of sand stabilization or by sand depth. We studied the effect of predator presence, predator type (active predatory beetle vs. sit-and-pursue wolf spider), and sand depth (shallow vs. deep sand) on the behavioral response of the pit building Myrmeleon hyalinus larvae and the sit-and-pursue Lopezus fedtschenkoi larvae. Predator presence had a negative effect on both antlion species activity. The sit-and-wait M. hyalinus larvae showed reduced pit-building activity, whereas the sit-and-pursue L. fedtschenkoi larvae decreased relocation activity. The proportion of relocating M. hyalinus was negatively affected by sand depth, whereas L. fedtschenkoi was negatively affected also by the predator type. Specifically, the proportion of individual L. fedtschenkoi that relocated in deeper sand was lower when facing the active predator rather than the sit-and-pursue predator. The proportion of M. hyalinus which constructed pits decreased in the presence of a predator, but this pattern was stronger when exposed to the active predator. We suggest that these differences between the two antlion species are strongly linked to their distinct foraging modes and to the foraging mode of their predators. Reut Loria and Inon Scharf contributed equally to the paper.     

Defensive secretions from the larvae ofApatania fimbriata (Pictet) (Trichoptera: Limnephilidae)

Summary When the larvae of the caddis flyApatania fimbriata (Pictet) are threatened, drops of fluid appear on their head capsules. The secretions are produced in a gland in the dorsal part of the prothorax. The neck region contains an eversible sac with numerous single setae, groups of 3 setae, or rows of setae on the surface. The secretion is released through two paris of orifices on the lateral sides of the sac. For the most part the secretion is composed of some 30 fatty acids, with the major components having 12–14 carbon atoms and up to 4 double bonds (approx. 1–2 µg secretion per specimen). Biotests with synthetic saturated acids (C₆–C₁₂) in a stream and in the laboratory demonstrated a paralysing effect on small invertebrate predators (Rhyacophila sp.,Plectrocnemia conspersa, Hydropsyche sp., larvae, all Trichoptera). In choice experiments,Rhyacophila sp. larvae preferred larvae ofAgapetus fuscipes andDrusus annulatus (Trichoptera) as food as compared withApatania fimbriata larvae. Larger predators, such asDinocras cephalotes (Insecta, Plecoptera) and the fishCottus gobio, did not discriminate betweenApatania fimbriata and other prey species. The use of fatty acids in defensive secretions is interpreted as an adaptation to the running water environment. They are effective repellents againstRhyacophila sp. larvae, the most important predator in the natural environment ofApatania larvae.     

Predation risk assessment by green frog (<Emphasis Type="Italic">Rana clamitans</Emphasis>) tadpoles through chemical cues produced by multiple prey

Many prey assess predation risk through predator chemical cues. Numerous studies have shown that (1) prey sometimes respond to chemical cues produced by heterospecifics and (2) that many species are capable of associative learning. This study extends this research by focusing on predation risk assessment and antipredator behavior in environments containing chemical cues produced by multiple prey species. The results show that green frog (Rana clamitans) tadpoles (1) assess risk from the chemical cue produced during predation by a heterospecific (gray tree frog, Hyla versicolor, tadpoles) and (2) can exhibit similarly strong behavioral responses to a mix of conspecific and heterospecific cues compared to conspecific cue alone, depending on their conditioning environment. I then discuss how the prey choice of the predators and the relative abundances of the prey species should influence the informational value of heterospecific cues.     

Background level of risk determines the intensity of predator neophobia in juvenile convict cichlids

Behavioural ecology is rife with examples of prey animals that are able to adjust the intensity of their anti-predator response to match background risk levels. Often, preys need experience with predators before they will invest in costly anti-predator responses. This means that prey animals often fail to respond to predators during their first encounter. Recently, we have shown that prey raised under high-risk conditions may exhibit avoidance of potential predation cues independent of experience (neophobia). Such phenotypically plastic neophobic predator responses may reduce the initial costs of learning ecologically relevant threats while maintaining sufficient behavioural plasticity to respond to variation in local conditions. Here, we test if induced neophobia results in threat-sensitive behavioural trade-offs in response to a novel chemosensory cue. Our first experiment shows that while juvenile convict cichlids (Amatitlania nigrofasciata) pre-exposed to high (but not low) risk conditions exhibited predator avoidance to a novel odour (rainbow trout, Oncorhynchus mykiss), the response intensity was not influenced by the concentration of trout odour detected. Our second experiment demonstrated that the intensity of anti-predator response towards a novel predator cue was dependent upon the level of background risk. Convict cichlids pre-exposed to high-risk conditions showed stronger responses than those pre-exposed to low-risk conditions, while cichlids pre-exposed to intermediate-risk conditions exhibited intermediate response intensities. Together, these data demonstrate that background levels of risk and not the concentration of novel cues detected shape the induced neophobic response pattern of juvenile convict cichlids.     

Hunted hunters? Effect of group size on predation risk and growth in the Australian subsocial crab spider Diaea ergandros

A reduced predation risk is considered to be a major adaptive advantage of sociality. While most studies are concerned with non-predatory prey species, group-living predators are likely to face similar threats from higher-order predators. We studied the relationship between group size and predation risk in the subsocial crab spider Diaea ergandros by testing predictions from theoretical models including attack abatement as well as the formation of protective retreats. In a field survey, we found predatory clubionid spiders in 35 % of the D. ergandros nests and as predicted, nest size did not correlate with predator presence. In a subsequent laboratory experiment, we observed survival probability, nest construction activity and feeding behaviour including weight development between groups of different sizes as well as in the absence or presence of a predator. Large groups had an advantage in terms of survival and growth compared to smaller groups or single individuals. They also built significantly larger nests than smaller groups, supporting the idea of protective retreat formation being an adaptive benefit to group living. Even though clubionids did attack D. ergandros, they did not significantly affect overall mortality of D. ergandros. The feeding experiment showed that spiders fed on a larger proportion of flies in the presence of a predator. However, these groups gained significantly less weight compared to the control groups, indicating that the potential predators not only act as predators but also as food competitors, constituting a twofold cost for D. ergandros.     

Disturbance cues in freshwater prey fishes: do juvenile convict cichlids and rainbow trout respond to ammonium as an ‘early warning’ signal?

Summary.  Several freshwater invertebrate and vertebrate prey species rely on chemosensory cues, including non-injury released disturbance cues, to assess and avoid local predation threats. The prevailing hypothesis is that a pulse of ammonia released by disturbed or stressed prey functions as the disturbance cue. Here, we test this hypothesis in two phylogenetically distant freshwater prey fishes, convict cichlids and rainbow trout. In our first experiment, we measured NH₄ ⁺ concentration in tanks containing shoals of cichlid or trout before and after exposure to a realistic model predator (or left undisturbed). We failed to find an increase in ambient NH₄ ⁺ concentration for either cichlids or trout. In our second experiment, we exposed cichlids or trout to NH₄ ⁺ at 0.1 or 0.5 mg L⁻¹ (or a distilled water control) and measured the change in antipredator behaviour (time moving, foraging rate and area use). We found no consistent increase in antipredator behaviour in response to NH₄ ⁺. In our third study, we exposed cichlids and trout to the disturbance cues of cichlids or trout (versus the odour of undisturbed donors). We found significant increases in antipredator behaviour, regardless of donor species, for both cichlids and trout. Thus, the results of our first two experiments do not support the hypothesis that ammonium functions as a disturbance cue in prey fishes. However, the results of our final experiment do confirm the use of disturbance cues in convict cichlids and rainbow trout and support that hypothesis that the disturbance cue is indeed some generalized metabolic byproduct.     

Do mountain log skinks (<Emphasis Type="Italic">Pseudemoia entrecasteauxii</Emphasis>) modify their behaviour in the presence of two predators?

Prey often adopt antipredator strategies to reduce the likelihood of predation. In the presence of predators, prey may use antipredator strategies that are effective against a single predator (specific) or that are effective against several predators (nonspecific). Most studies have been confined to single predator environments although prey are often faced with multiple predators. When more than one predator is present, specific antipredator behaviours can conflict and avoidance of one predator may increase vulnerability to another. To test how prey cope with this dilemma, I recorded the behaviours of lizards responding to the nonlethal cues of a bird and snake presented singly and simultaneously. Lizards use specific and conflicting antipredator tactics when confronted with each predator, as evidenced by refuge use. However, when both predators were present, lizards refuge use was the same as in the predator-free environment, indicating that they abandoned refuge use as a primary mechanism for predator avoidance. In the presence of both predators, they reduced their overall movement and time spent thermoregulating. This shift in behaviour may represent a compromise to minimize overall risk, following a change in predator exposure. This provides evidence of plasticity in lizard antipredator behaviour and shows that prey responses to two predators cannot be accurately predicted from what is observed when only one predator is present.Communicated by W. Cooper     

The paradox of risk assessment: comparing responses of fathead minnows to capture-released and diet-released alarm cues from two different predators

Summary. Many aquatic prey are known to use chemical alarm cues to assess their risk of predation. In fishes, such alarm cues can be released either through damage of the epidermis during a predatory attack (capture-released) or through release from the predator feces (diet-released). In our study, we compared the importance of capture- versus diet-released alarm cues in risk assessment by fathead minnows (Pimephales promelas) that were na?ve to fish predators. We utilized two different fish predators: a specialized piscivore, the northern pike (Esox lucius) and a generalist predator, the brook trout (Salvelinus fontinalis). Handling time of pike consuming minnows was much shorter than for trout consuming minnows, likely resulting in less epidermal damage to the minnows during attacks by pike. In accordance with this, minnows showed a less intense antipredator response to capture-released cues from pike than capture-released cues from trout. This represents a paradox in risk assessment for the minnows as they respond to the specialized piscivore, the more dangerous predator, with a less intense antipredator response. In contrast, the minnows showed a stronger antipredator response to the specialized piscivore than to the generalist when given diet cues. This work highlights the need for researchers to carefully consider the nature of the information available to prey in risk assessment.     

Nest-size variation reflecting anti-predator strategies in social spider mites of<Emphasis Type="Italic"> Stigmaeopsis</Emphasis> (Acari: Tetranychidae)

The social spider mites (Acari: Tetranychidae) of Stigmaeopsis weave dense nests on the underside of host leaves. Four species occur on the leaves of bamboo in Japan: Stigmaeopsis longus, S. celarius, S. takahashii and S. saharai. We initially reconfirmed the occurrence of distinct variation in nest size among the species. Based on the hypothesis that this variation plays a role in protecting the spider mites from predators, we looked at the behavior of the natural enemies that occur on the host plants along with members of Stigmaeopsis. We found considerable variation in the ability of nests to protect the spider-mite eggs. The smallest nests protected the eggs against three predators, whereas the largest nests protected the eggs against only one predator species. So, decreases in nest size increased egg defense. Thus we concluded that nest-size variation reflects a strategy for reducing predation.Communicated by D. Gwynne