Sensory exploitation of prey: manipulation of the initial direction of prey escapes by a conspicuous "rare enemy"

The painted redstart (Myioborus pictus) represents a group of non-cryptic predators, the flush pursuers, who visually trigger prey escapes by spreading and pivoting their conspicuously patterned tails and wings. The prey are then chased in aerial pursuits. Such an exploitation of prey may be possible because the predation risk from redstarts is smaller than that from the predatory guild of insectivores and their neural pathways are adapted to helping prey avoid common predators rather than "rare enemies". I propose that the pivoting movements of flush pursuers direct insect escapes across the central field of vision of a predator, where it is easier to track and intercept the prey. Eighty per cent of chases by wild redstarts were in a direction suggesting that prey were entering the birds' area of stereoscopic vision. The redstart's fanned and raised tail creates a stronger visual stimulus than a redstart's head. Flies escaped away from the section of the fly's field of vision in which the model's tail was located and towards the area where the predator's stereoscopic vision is likely to be located, in front of a bird's forehead. The experiments suggested that redstarts may not only exploit the sensitivity of typical neural escape pathways, which are non-directionally sensitive, but that they may also exploit the sensitivity of some directionally sensitive neural pathways in prey.     

Prey Escape Direction is Influenced by the Pivoting Displays of Flush-Pursuing Birds

Painted redstart, Myioborus pictus, and its congeners in Central and South America, belong to a small fraction of insectivorous flush‐pursuing birds. Unlike most of the small insectivorous birds, which glean prey from substrates, the flush pursuers spread and pivot their conspicuously patterned tails and wings. This display triggers prey escape flights which are hypothesized to occur through visual stimulation of prey escape circuits [giant descending neuron cluster (GDNC) in Diptera] sensitive to the looming motion of an approaching bird, translational motion of a pivoting body with widely spread tail and contrast of the white‐black plumage pattern. In this paper, data from field observations of redstarts and experiments with bird models show an increase in the frequency of prey escapes away from the strong visual stimulation of an open tail, and in the direction opposite to that of the horizontal translational motion present in the pivots. We discuss how the effect on prey escape direction may enhance prey interception capabilities of redstarts during aerial pursuits. Combined with an earlier study the results show that, unlike the movements of typical gleaner–foragers, the flush displays by redstarts affect prey escape direction in a manner that may facilitate prey tracking and capture by birds. Because the GDNs, which mediate escape initiation, are not sensitive to motion direction, we hypothesize that other neurons, in addition to the GDNs, are involved in influencing the direction of escape responses.     

Evolutionary significance of geographic variation in a plumage-based foraging adaptation: an experimental test in the slate-throated redstart (Myioborus miniatus)

Geographic variation in the plumage pattern of birds is widespread but poorly understood, and in very few cases has its evolutionary significance been investigated experimentally. Neotropical warblers of the genus Myioborus use their contrasting black-and-white plumage to flush insect prey during animated foraging displays. Although previous experimental work has demonstrated that white plumage patches are critical to flush-pursuit foraging success, the amount of white in the plumage shows considerable interspecific and intraspecific geographic variation. We investigated the evolutionary significance of this geographic variation by experimentally decreasing or increasing the amount of white in the tail of slate-throated redstarts (Myioborus miniatus comptus) from Monteverde, Costa Rica, to mimic the natural extremes of tail pattern variation in this species. In addition to measuring the effects of plumage manipulation on foraging performance, we performed field experiments measuring the escape response of a common insect prey species (an asilid fly) using model redstarts representing four different Myioborus plumage patterns. Our experiments were designed to test four hypotheses that could explain geographic variation in plumage pattern. Compared to controls, experimental birds with reduced-white tails that mimic the plumage pattern of M. miniatus hellmayri of Guatemala showed significant reductions in flush-pursuit foraging performance. In contrast, the addition of white to the tail to mimic the plumage pattern of M. miniatus verticalis of Bolivia had no significant effect on foraging performance of Costa Rican redstarts. In field experiments with asilid flies, model redstarts simulating the plumage of M. miniatus comptus of Costa Rica and M. miniatus verticalis of Bolivia elicited greater responses than did models of other Myioborus taxa with either less or more white in the plumage. The results of our experiments with both birds and insects allow us to reject two hypotheses for geographic variation in plumage pattern: (1) that geographic variation is a nonadaptive result of genetic drift, and (2) that selection for enhanced flush-pursuit foraging performance generally favors increased white in the plumage, but evolutionary trade-offs constrain the evolution of extensive patches of white in some geographic regions. Instead, our results suggest that geographic variation in the plumage pattern of Myioborus redstarts reflects adaptation to regional habitat characteristics that enhances flush-pursuit foraging performance.     

Adaptation of prey and predators between patches

Mathematical models are proposed to simulate migrations of prey and predators between patches. In the absence of predators, it is shown that the adaptation of prey leads to an ideal spatial distribution in the sense that the maximal capacity of each patch is achieved. With the introduction of co-adaptation of predators, it is proved that both prey and predators achieve ideal spatial distributions when the adaptations are weak. Further, it is shown that the adaptation of prey and predators increases the survival probability of predators from the extinction in both patches to the persistence in one patch. It is also demonstrated that there exists a pattern that prey and predators cooperate well through adaptations such that predators are permanent in every patch in the case that predators become extinct in each patch in the absence of adaptations. For strong adaptations, it is proved that the model admits periodic cycles and multiple stability transitions.     

Habitat-specific sensory-exploitative signals in birds: propensity of dipteran prey to cause evolution of plumage variation in flush-pursuit insectivores

Sensory exploitation occurs when signals trigger behavioral reactions that diminish the receiver's fitness. Research in this area focuses on the match between the signal's form and the receiver's sensitivity, but the effect of habitat on interspecific sensory exploitation is rarely addressed. Myioborus redstarts use conspicuous wing and tail displays of contrasting black-and-white plumage patches to flush dipteran insects, which are then pursued and captured in flight. Previous studies have shown that by increasing the distance at which insects perform an escape response, conspicuous visual displays improve the birds' foraging performance. We tested the hypothesis that selection for a visual signal that maximizes prey escape distance under local habitat conditions can lead to the evolution of geographic variation in plumage pattern among Myioborus redstarts. Using models of foraging birds, we recorded the escape responses of Dipterous insects to a range of plumage patterns and background tones (from light to dark) to determine whether the plumage pattern that maximizes prey flushing is dependent upon that habitat (background) against which birds are viewed by their prey. Our results indicate that the effectiveness of a particular plumage pattern in flushing dipteran prey depends strongly on the background against which that plumage pattern is displayed, and darker habitat (background) conditions generally favor plumages with more extensive patches of white in the tail. However, the addition of white wing patches that imitate the plumage of the painted redstart (Myioborus pictus) generally increases insect escape responses but reduces the effect that tail pattern variation and background tone have on escape behavior. These experiments support the hypothesis that habitat-specific natural selection to enhance sensory exploitation of prey escape responses could produce geographic variation in plumage patterns of flush-pursuers.     

Tail flicking in the black redstart (<Emphasis Type="Italic">Phoenicurus ochruros</Emphasis>) and distance to cover

Tail flicking is a common behavior in many bird species, but its function is often unknown. Apart from intraspecific communication, tail flicking could be used during predator–prey communication, e.g., as a signal of prey vigilance or quality. We studied this behavior in the black redstart (Phoenicurus ochruros), a species that frequently shows tail flicking and is prone to attacks by ambushing predators that hide in cover. Hence, cover might be perceived as dangerous by this species. We hypothesized that flicking should increase with decreasing distance to cover. We counted the number of tail flicks of individuals and measured their distance to the nearest cover for an ambushing predator. We found that distance to cover had a significant effect on tail flicking behavior, as flicking increased with decreasing distance, but found no difference in flicking frequency between adults and juveniles or between sexes. Consequently, tail flicking is unlikely to signal submission or to be sexually selected in the black redstart. Since tail flicking also occurred in the absence of predators, we consider tail flicking in black redstarts to display vigilance and to be directed towards ambushing predators.     

Dragonfly larvae and tadpole frog space use games in varied light conditions

Predators and prey often engage in a game where predators attemptto be in areas with higher prey densities and prey attempt tobe in areas with lower predator densities. A few models havepredicted the resulting distributions of predators and prey,but little empirical data exist to test these predictions andto examine how abiotic and biotic factors shape the distributions.Thus, we observed how Anax dragonfly nymphs and Pacific treefrog tadpoles (Pseudacris regilla) either together or separatelydistributed themselves in an arena with a high- and a low-preyresource patch. Trials were conducted in high- and low-lightconditions to manipulate predation risk and to view the effectsof this abiotic factor. Counter to the model predictions, wefound that predators were not more abundant in high-resource(HR) patches, and they thus did not force prey toward beinguniformly distributed. Using a model selection approach to assesswhat factors affected predator and prey patch-switching movement,we found that prey more often left patches that had more predatorspresent, but predators surprisingly more often left patcheswith more prey present. Light levels did not affect predationrisk; however, in the dark with the associated reduction invisual information predators preferred HR patches. This causeda lower coincidence of prey and predators in patches. Predatorsalso switched patches less often when they occupied the samepatch as the other predator. This suggests that predator distributions,and indirectly prey distributions, are affected by the riskof intraguild predation.     

Predatory behavior of the praying mantis,Tenodera aridifolia II. Combined effect of prey size and predator size on the prey recognition

Predatory behavior of the praying mantis,Tenodera aridifolia, as a function of the combined effect of its size and the size of the prey was investigated by using prey models. Behavioral responses were almost identical through the nymphal development in the predator. As the mantis grew, it attacked larger prey models, suggesting that it recognizes the prey's size in accordance with its own body size. Regression analyses demonstrate that the ratio of the prey's volume to the cube and the square of the predator's length is a more important parameter for prey recognition than are the one-dimensional parameters of the prey's and the predator's sizes.     

Flight initiation distance and escape behavior in the black redstart (Phoenicurus ochruros)

There are many anti‐predatory escape strategies in animals. A well‐established method to assess escape behavior is the flight initiation distance (FID), which is the distance between prey and predator at which an animal flees. Previous studies in various species throughout the animal kingdom have shown that group size, urbanization, and distance to refuge and body mass affect FID. In most species, FID increases if body mass, group size or distance to refuge decreases. However, how age and sexual dimorphism affect FID is rather unknown. Here, we assess the escape behavior and FID of the black redstart (Phoenicurus ochruros), a small turdid passerine. When approached by a human, males initiated flights later, that is allowing a closer approach than females. Males of this species are more conspicuous, and therefore, may exhibit aposematism to deter potential predators or are less fearful than females. Additionally, juveniles fled at shorter distances and fled to lower heights than adults. Lastly, concerning escape strategy, black redstarts, unless other passerine birds, fled less often into cover, but rather onto open or elevated spots. Black redstarts are especially prone to predation by ambushing predators that might hide in cover. Hence, this species most likely has a higher chance of escaping by fleeing to an open spot rather than to a potentially risky cover.     

Reactions of hand-reared and wild-caught predators toward warningly colored, gregarious, and conspicuous prey

Recently there has been debate over the importance of innateavoidance of aposematic prey by predators, particularly birds.There is evidence that the predators have innate or unlearned,thus, inherited avoidance against certain colors, but whetherthere is any innate avoidance against gregariousness or conspicuousnessis unclear. Previously predator behavior toward these charactersof aposematic prey have been tested in separate experiments.We designed an experiment to separate inheritance toward color,gregariousness, and conspiucuosness. We simultaneously offeredthe predators warningly colored and nonwarningly colored preyitems, both aggregated and solitary, on white (conspicuous)or brown (cryptic) backgrounds. The predators we used were naive (handraised), wild-caught yearling and adult great tits (Parus major L.).The results confirm previous results regarding the innate avoidanceof color. Naive predators seemed to have a genetically or culturallytransmitted avoidance of yellow and black prey compared to brownprey. Surprisingly, yearling wild-caught great tits were moreselective than adults, which did not show as strong avoidanceof yellow and black prey. More importantly, birds did not findgregarious prey more aversive than single prey, which indicatesthat grouping alone does not serve as an innate avoidance signal.Conspicuousness itself was not aversive to the predators. Ourresults suggest that the avoidance against a particular colorpattern probably has an inherited basis, whereas gregariousand conspicuous characters of prey presumably aid the avoidancelearning.     

Conspecific alarm cues, but not predator cues alone, determine antipredator behavior of larval southern marbled newts, Triturus pygmaeus

Predation imposes selection on the ability of prey to recognize and respond to potential threats. Many prey species detect predators via chemoreception, particularly in aquatic environments. Also, chemical cues from injured prey are often perceived as an indication of predation risk. However, because antipredatory behavior can be costly, prey responses should depend on the current level of risk that each predator poses, which may depend on the type of chemical cues detected. We exposed larval newts, Triturus pygmaeus, to chemical cues from predator larval beetles or to alarm cues from conspecific larval newts and examined the behavioral changes of larval newts. Results showed that larval newts reduced activity levels when conspecific alarm cues were present but not when the predator cues alone were present. These results might suggest that larval newts are unable to recognize predator chemicals. To avoid costs of unnecessary antipredatory behaviors, larval newts may benefit by avoiding only predators that represent a current high level of threat, showing only antipredatory responses when they detect conspecific alarm cues indicating that an actual predatory attack has occurred.     

Effect of sex and bright coloration on survival and predator‐induced wing damage in an aposematic lantern fly with startle display

1. Aposematic coloration in prey promotes its survival by conspicuously advertising unpalatability to predators. Although classical examples of aposematic signals involve constant presentation of a signal at a distance, some animals suddenly display warning colours only when they are attacked. 2. Characteristics of body parts suddenly displayed, such as conspicuous coloration or eyespot pattern, may increase the survival of the prey by startling the predator, and/or by signalling unpalatability to the predators at the moment of attack. 3. The adaptive value of such colour patterns suddenly displayed by unpalatable prey has not been studied. We experimentally blackened the red patch in the conspicuous red–white–black hindwing pattern displayed by an unpalatable insect Lycorma delicatula White (Hemiptera: Fulgoridae) in response to predator's attack. 4. There was no evidence that the presence of the red patch increased prey survival over several weeks. We hypothesise that predators generalised from the red–white–black patches on the hindwings of unpalatable L. delicatula to any similar wing display as a signal of unpalatability. Because a higher proportion of males than females stay put at their resting sites, displaying their wings in response to repeated attacks by predators, wing damage was more frequent in males than in females. 5. To our knowledge, this is the first experimental test of an adaptive role of aposematic signals presented by unpalatable prey during sudden displays triggered by direct predatory attack.     

Use of prey hotspots by an avian predator: purposeful unpredictability?

The use of space by predators in relation to their prey is a poorly understood aspect of predator-prey interactions. Classic theory suggests that predators should focus their efforts on areas of abundant prey, that is, prey hotspots, whereas game-theoretical models of predator and prey movement suggest that the distribution of predators should match that of their prey's resources. If, however, prey are spatially anchored to one location and these prey have particularly strong antipredator responses that make them difficult to capture with frequent attacks, then predators may be forced to adopt alternative movement strategies to hunt behaviorally responsive prey. We examined the movement patterns of bird-eating sharp-shinned hawks (Accipiter striatus) in an attempt to shed light on hotspot use by predators. Our results suggest that these hawks do not focus on prey hotspots such as bird feeders but instead maintain much spatial and temporal unpredictability in their movements. Hawks seldom revisited the same area, and the few frequently used areas were revisited in a manner consistent with unpredictable returns, giving prey little additional information about risk.     

Habitat choice in predator-prey systems: spatial instability due to interacting adaptive movements

The role of habitat choice behavior in the dynamics of predator-prey systems is explored using simple mathematical models. The models assume a three-species food chain in which each population is distributed across two or more habitats. The predator and prey adjust their locations dynamically to maximize individual per capita growth, while the prey's resource has a low rate of random movement. The two consumer species have Type II functional responses. For many parameter sets, the populations cycle, with predator and prey "chasing" each other back and forth between habitats. The cycles are driven by the aggregation of prey, which is advantageous because the predator's saturating functional response induces a short-term positive density dependence in prey fitness. The advantage of aggregation in a patch is only temporary because resources are depleted and predators move to or reproduce faster in the habitat with the largest number of prey, perpetuating the cycle. Such spatial cycling can stabilize population densities and qualitatively change the responses of population densities to environmental perturbations. These models show that the coupled processes of moving to habitats with higher fitness in predator and prey may often fail to produce ideal free distributions across habitats.     

Spatial dynamics of communities with intraguild predation: the role of dispersal strategies

I investigate the influence of dispersal strategies on intraguild prey and predators (competing species that prey on each other). I find an asymmetry between the intraguild prey and predator in their responses to each other's dispersal. The intraguild predator's dispersal strategy and dispersal behavior have strong effects on the intraguild prey's abundance pattern, but the intraguild prey's dispersal strategy and behavior have little or no effect on the intraguild predator's abundance pattern. This asymmetry arises from the different constraints faced by the two species: the intraguild prey has to acquire resources while avoiding predation, but the intraguild predator only has to acquire resources. It leads to puzzling distribution patterns: when the intraguild prey and predator both move away from areas of high density, they become aggregated to high-density habitats, but when they both move toward areas of high resource productivity, they become segregated to resource-poor and resource-rich habitats. Aggregation is more likely when dispersal is random or less optimal, and segregation is more likely as dispersal becomes more optimal. The crucial implication is that trophic constraints dictate the fitness benefits of using dispersal strategies to sample environmental heterogeneity. A strategy that affords greater benefits to an intraguild predator can lead to a more optimal outcome for both the intraguild predator and prey than a strategy that affords greater benefits to an intraguild prey.     

Dome-shaped functional response induced by nutrient imbalance of the prey

Nutritional ecological theory predicts that predators should adjust prey capture and consumption rates depending on the prey's nutritional composition. This would affect the predator's functional response, at least at high prey densities, i.e. near predator satiation. Using a simple fruitfly-wolf spider laboratory system in Petri dishes, we found that functional responses changed from day to day over a 7 day period. After 1 to 2 days of feeding, dome-shaped functional responses (i.e. reduced predation at highest prey densities) appeared in spiders fed nutritionally imbalanced prey, compared with steadily increasing or asymptotic functional responses with nutritionally near-optimal prey. Later again (days 5-7), the difference disappeared as the level of the functional response was reduced in both treatments. Experiments with adult females in spring and subadult spiders in autumn revealed opposite patterns: a dome-shaped response with high-lipid prey for reproductive females, for which protein-rich prey are optimal, and a dome-shaped (or simply reduced) response with high-protein prey for pre-winter subadults, for which high-lipid flies are the optimal prey. Our results have implications for predation theory and models of biological control that have, so far, neglected nutritional aspects; in particular, the dynamic nutritional state of the predators should be incorporated.     

Predator-prey interactions between ectoparasites

Vertebrates represent a resource frequently exploited by ectoparasites. But the ectoporosites themselves also represent a resource that can be exploited by specialized predators. Some o f these predators have been classified as ectoparasites, but in some cases the vertebrate blood in their crops comes from their blood-sucking prey. In fact, as Lance Durden explains, the assemblage o f arthropods that inhabit the vertebrate skin surface, or pelage, seems to show a complete spectrum of adaptations from predators to facultative and obligate blood-suckers, together with those feeding on other materials in this special habitat. The dynamics of their interactions are further complicated by responses of the host to the arthropods, and much further study is needed before the role o f predators in controlling ectoparasites can be clarified.     

Habitat and body condition influence American Redstart foraging behavior during the non‐breeding season

Insectivorous birds may adjust their foraging strategies to exploit changes in resource distributions. Arthropod prey strongly influence habitat‐specific persistence of long‐distance migrant passerines in their wintering areas, and arthropods are strongly affected by rainfall. However, the effect of drought on the dynamics of avian foraging ecology as resources shift is not well understood. We captured female American Redstarts (Setophaga ruticilla) and studied their foraging behavior in high‐quality (evergreen black mangrove) and low‐quality (deciduous scrub) habitat in Jamaica during the winter of 1995–1996. As is typical in southwestern Jamaica, conditions became drier as spring approached and many trees in scrub lost most of their leaves; mangrove trees maintained most of their leaf cover. Birds in scrub lost more mass than those in mangrove, and scrub birds shifted to using more aerial (and fewer near‐perch) maneuvers. In scrub, but not in mangrove, the proportion of wing‐powered movements and aerial foraging maneuvers was positively correlated with mass corrected by body size. In both habitats, attack rate was negatively correlated with body condition. Therefore, redstarts in scrub that maintained body condition were likely better able to use energetically expensive aerial maneuvers and wing‐powered search movements to exploit large, calorie‐rich flying arthropods. As the scrub dried over the course of the winter, the shift in foraging tactic may have allowed some birds to forage more efficiently (i.e., lower attack rate), likely facilitating maintenance of good body condition.     

Frequency-dependent taste-rejection by avian predation may select for defence chemical polymorphisms in aposematic prey

Chemically defended insects advertise their unpalatability to avian predators using conspicuous aposematic coloration that predators learn to avoid. Insects utilize a wide variety of different compounds in their defences, and intraspecific variation in defence chemistry is common. We propose that polymorphisms in insect defence chemicals may be beneficial to insects by increasing survival from avian predators. Birds learn to avoid a colour signal faster when individual prey possesses one of two unpalatable chemicals rather than all prey having the same defence chemical. However, for chemical polymorphisms to evolve within a species, there must be benefits that allow rare chemical morphs to increase in frequency. Using domestic chicks as predators and coloured crumbs for prey, we provide evidence that birds taste and reject proportionally more of the individuals with rare defence chemicals than those with common defence chemicals. This indicates that the way in which birds attack and reject prey could enhance the survival of rare chemical morphs and select for chemical polymorphism in aposematic species. This is the first experiment to demonstrate that predators can directly influence the form taken by prey's chemical defences.     

Multitrait aposematic signal in Batesian mimicry

Batesian mimics can parasitize Müllerian mimicry rings mimicking the warning color signal. The evolutionary success of Batesian mimics can increase adding complexity to the signal by behavioral and locomotor mimicry. We investigated three fundamental morphological and locomotor traits in a Neotropical mimicry ring based on Ithomiini butterflies and parasitized by Polythoridae damselflies: wing color, wing shape, and flight style. The study species have wings with a subapical white patch, considered the aposematic signal, and a more apical black patch. The main predators are VS‐birds, visually more sensitive to violet than to ultraviolet wavelengths (UVS‐birds). The white patches, compared to the black patches, were closer in the bird color space, with higher overlap for VS‐birds than for UVS‐birds. Using a discriminability index for bird vision, the white patches were more similar between the mimics and the model than the black patches. The wing shape of the mimics was closer to the model in the morphospace, compared to other outgroup damselflies. The wing‐beat frequency was similar among mimics and the model, and different from another outgroup damselfly. Multitrait aposematic signals involving morphology and locomotion may favor the evolution of mimicry rings and the success of Batesian mimics by improving signal effectiveness toward predators.