Viewing distance affects how the presence of inedible models influence the benefit of masquerade

Masquerading prey closely resemble inedible objects found in the same locality. These animals gain protection from their predators by causing their predators to misclassify them as the inedible ‘models’ that they appear to resemble. We recently demonstrated that predators are more likely to misclassify masquerading prey as their models when masqueraders are viewed in isolation from their models than when they are viewed simultaneously with examples of their models. Using domestic chicks (Gallus gallus domesticus) as predators and the twig-mimicking caterpillars of the Early Thorn Moth (Selenia dentaria) as prey, we tested whether this effect was influenced by the relative orientations of models and masqueraders; and the distance from which models and masqueraders could be viewed simultaneously. We found no effect of orientation, but that the cost to masqueraders of being viewed simultaneously with an example of the model declined as the distance between the model and masquerader increased. These results are interpreted in terms of animal cognition, and their implications for the evolutionary ecology of masquerade.     

Predators are less likely to misclassify masquerading prey when their models are present

Masquerading animals have evolved striking visual resemblances to inanimate objects. These animals gain protection from their predators not simply by avoiding detection, but by causing their predators to misclassify them as the ‘models’ that they appear to resemble. Using domestic chicks as predators and twig-mimicking caterpillars as prey, we demonstrated that masquerading prey were more likely to be misclassified as their models when viewed in isolation from their models than when viewed alongside examples of their model, although they benefitted from masquerade to some extent in both conditions. From this, we predict a selection pressure on masqueraders to use microhabitats that reduce the risk of them being viewed simultaneously with examples of their model, and/or to more closely resemble their model in situations where simultaneous viewing is commonplace.     

Masquerade is associated with polyphagy and larval overwintering in Lepidoptera

Masquerading animals benefit from the difficulty that predators have in differentiating them from the inedible objects, such as twigs, that they resemble. The function of masquerade has been demonstrated, but how it interacts with the life history of organisms has not yet been studied. Here, we report the use of comparative analyses to test hypotheses linking masquerade to life‐history parameters. We constructed a phylogenetic tree of the British species of the lepidoptera families Geometridae and Drepanidae, and compiled life history and coloration data from the literature. We found that masquerade is associated with the exploitation of a greater diversity of host plants whether measured by the number of families or genera. We found a positive relationship between body size and polyphagy among masquerading species, and no relationship among cryptic species. Among those species predominantly found on woody host plants, masquerading species are more likely to overwinter as larvae while cryptic species mostly overwinter as pupae. Polyphenism was associated with multivoltinism in masquerading species but not cryptic species. Taken together, our results show that masquerade must be viewed as a strategy distinct to crypsis and hence may provide insights into the evolution of both defensive strategies. Our study further demonstrates the utility of broad‐scale between‐species comparisons in studying associations between diverse life‐history parameters and sensory aspects of predator‐prey interactions. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 90–103.     

Prey Luring Coloration of A Nocturnal Semi‐Aquatic Predator

Body coloration serves a variety of purposes in animals. Diurnal and nocturnal predators such as spiders may use their body coloration to lure prey. We predicted here that the white patches on the forelegs on females of the nocturnal semi‐aquatic spider Dolomedes raptor lure prey, explaining why they are primarily displayed when the spider forages along the water edge. To test our prediction, we developed a color vision model assessing whether the patches are visible to pygmy grasshoppers, the spider's primary prey. We conducted a field experiment using cardboard dummies that resemble D. raptor in size, shape, and color, but with half of them lacking leg patches, and we staged interactions between pygmy grasshoppers and D. raptor with and without leg patches in a greenhouse. We found the white patches to be visible to grasshoppers. The dummies with white patches attracted more grasshopper prey than the dummies without the patches. Moreover, grasshoppers were more attracted to spiders when their white patches were present. Our results supported the hypothesis that the white patches of D. raptor lure prey. Our findings, nevertheless, could not be explained as the spider's body coloration acting as a sensory trap but it should not be ruled out. More studies on a wider range of predators and prey will give more meaningful insights into the co‐evolution of predatory lures and prey sensory modalities.     

The Relationship between Sympatric Defended Species Depends upon Predators' Discriminatory Behaviour

Toxic prey species living in the same environment have long been thought to mutually benefit from having the same warning signal by sharing the education of naïve predators. In contrast, ‘saturation theory’ predicts that predators are physiologically limited by the amount of toxin that they can eat in a given time period. Therefore, sympatric species that contain the same toxin should mutually benefit from reduced predation even when they are visually distinct, reducing the benefits to visual mimicry. For the first time, we found that mutualism can occur between unequally defended prey that are visually distinct, although the benefits to each prey type depends on the predators'' abilities and/or motivation to visually discriminate between them. Furthermore, we found that this variability in predatory behaviour had a significant impact on the benefits of mimicry for unequally defended prey. Our results demonstrate that variability in the foraging decisions of predators can have a significant effect on the benefits of shared toxicity and visual mimicry between sympatric species, and highlights the need to consider how predators exert selection pressures on models and mimics over their entire lifetimes.     

Predators target rare prey in coral reef fish assemblages

Predation can result in differing patterns of local prey diversity depending on whether predators are selective and, if so, how they select prey. A recent study comparing the diversity of juvenile fish assemblages among coral reefs with and without predators concluded that decreased prey diversity in the presence of predators was most likely caused by predators actively selecting rare prey species. We used several related laboratory experiments to explore this hypothesis by testing: (1) whether predators prefer particular prey species, (2) whether individual predators consistently select the same prey species, (3) whether predators target rare prey, and (4) whether rare prey are more vulnerable to predation because they differ in appearance/colouration from common prey. Rare prey suffered greater predation than expected and were not more vulnerable to predators because their appearance/colouration differed from common prey. Individual predators did not consistently select the same prey species through time, suggesting that prey selection behaviour was flexible and context dependent rather than fixed. Thus, selection of rare prey was unlikely to be explained by simple preferences for particular prey species. We hypothesize that when faced with multiple prey species predators may initially focus on rare, conspicuous species to overcome the sensory confusion experienced when attacking aggregated prey, thereby minimizing the time required to capture prey. This hypothesis represents a community-level manifestation of two well-documented and related phenomena, the “confusion effect” and the “oddity effect”, and may be an important, and often overlooked, mechanism by which predators influence local species diversity.     

The cost of migratory prey: seasonal changes in semi‐domestic reindeer distribution influences breeding success of Eurasian lynx in northern Norway

Migratory prey is a widespread phenomenon that has implications for predator–prey interactions. By creating large temporal variation in resource availability between seasons it becomes challenging for carnivores to secure a regular year‐round supply of food. Some predators may respond by following their migratory prey, however, most predators are sedentary and experience strong seasonal variation in resource availability. Increased predation on alternative prey may dampen such seasonal resource fluctuations, but reduced reproduction rates in predators is a predicted consequence of migratory primary prey behavior that has received little empirical attention. We used data from 23 GPS collared Eurasian lynx Lynx lynx monitored during 2007–2013 in northern Norway, to examine how spatio‐temporal variation in the migratory behavior of semi‐domestic reindeer Rangifer tarandus influences lynx spatial organization and reproductive success using estimates of seasonal home range overlap and breeding success. We found that lynx of both sexes maintained seasonally stable home ranges and exhibited site fidelity across years, independent of whether they had access to reindeer throughout the year or experienced a scarcity of reindeer in winter due to migration. However, lynx without access to reindeer in winter showed a decreased probability of reproducing and a tendency for lowered kitten survival into their first winter, when compared to female lynx with reindeer available year around. This supports the hypothesis that sedentary predators experience demographic costs in systems with migratory primary prey. Changes in the migratory behavior of ungulates, including disrupted migrations, is therefore likely to have bottom–up effects on the population dynamics of sedentary predators as well as the previously documented consequences for ungulate population dynamics.     

Constitutive exposure to the volatile methyl salicylate reduces per‐capita foraging efficiency of a generalist predator to learned prey associations

Understanding the factors that influence the ability of predators to find and kill herbivores is central to enhancing their impact on prey populations, but few studies have tested the impact of these factors on predation rates in realistic foraging environments. Using the tri‐trophic system consisting of tomato, Solanum lycopersicum L. (Solanaceae), hornworm caterpillars, Manduca sexta L. (Lepidoptera: Sphingidae), and the predaceous stink bug Podisus maculiventris (Say) (Hemiptera: Pentatomidae), we measured the effects of associative learning and plant volatile camouflage on predator behavior and foraging efficiency in field enclosures. To do so, we compared experienced vs. naive individuals under varying environmental contexts. Experienced predators were those with prior exposure to induced volatiles from the tomato–caterpillar association, whereas naive predators had not experienced tomato, only prey (caterpillars). We varied their environmental foraging matrix using either (1) tomato surrounded by basil (Ocimum basilicum L.; Lamiaceae) or (2) tomato exposed to the synthetic volatile, methyl salicylate (MeSA). We found that (1) experienced predators were more efficient than naive predators, capturing 28% more prey; (2) the tomato–basil combination did not affect predator–prey interactions; and (3) constitutive emission of synthetic MeSA caused a 22% reduction in P. maculiventris predation rate. These differences corresponded with distinct shifts in predator foraging; for example, experienced individuals were less stationary and exhibited unique behaviors such as stylet extension. Taken together, these results suggest that it is possible to improve the function of generalist predators in suppressing prey by coupling odors with food. However, constitutive emission of volatiles to attract natural enemies may ultimately camouflage neighboring plants, reducing the benefits of orientation to learned stimuli such as induced volatiles.     

Effects of chlorogenic acid-and tomatine-fed caterpillars on the behavior of an insect predator

If generalist insect predators are a selective force contributing to patterns of feeding specialization by insect herbivores, then predators should be deterred from eating allelochemical-fed prey. The attack and feeding behaviors of naive predators (Podisus maculiventris stinkbugs) reared on control caterpillars (Manduca sexta) fed plain diet were compared to experienced predators reared on caterpillars fed tomato allelochemicals. Tomatine-fed prey were found more quickly by both naive and tomatine-experienced predators, and chlorogenic acid-experienced predators were more stimulated to begin searching for prey. However, experienced predators were less likely to attack both chlorogenic acidfed and tomatine-fed caterpillars than were naive predators. These results indicate that allelochemical-fed prey were easier for predators to locate, but allelochemical-containing prey often deterred predation by experienced predtors.     

The evolution and ecology of masquerade

Many organisms appear to mimic inanimate objects such as twigs, leaves, stones, and bird droppings. Such adaptations are considered to have evolved because their bearers are misidentified as either inedible objects by their predators, or as innocuous objects by their prey. In the past, this phenomenon has been classified by some as Batesian mimicry and by others as crypsis, but now is considered to be conceptually different from both, and has been termed ‘masquerade’. Despite the debate over how to classify masquerade, this phenomenon has received little attention from evolutionary biologists. Here, we discuss the limited empirical evidence supporting the idea that masquerade functions to cause misidentification of organisms, provide a testable definition of masquerade, and suggest how masquerade evolved and under what ecological conditions. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 1–8.     

Foraging responses of predators to novel toxic prey: effects of predator learning and relative prey abundance

Learning to avoid toxic prey items may aid native predators to survive the invasion of highly toxic species, such as cane toads Bufo marinus in tropical Australia. If the predators’ initial aversion is generalized, native prey that resemble the toxic invader may receive a benefit through accidental mimicry. What ecological factors influence the acquisition of learned avoidance (and hence, the impact of invasion on both predators and native prey)? We conducted laboratory experiments to evaluate how the relative abundance of toad tadpoles compared to palatable native tadpoles (Litoria caerulea and L. rubella) affected the ability of native aquatic predators to discriminate between these two prey types. Both fish (northern trout gudgeon, Mogurnda mogurnda) and frogs (Dahl's aquatic frog, Litoria dahlii) learned to discriminate between toads and frogs within an eight‐day period. Higher abundance of toad tadpoles relative to frog tadpoles enhanced rates of predator learning, and thus reduced predation on toads and increased predation on native tadpoles. In the field, spatial and temporal variation in the relative abundance of cane toads compared to native frogs may influence the rates at which these novel toxic items are deleted from predator diets, and the duration of predator protection afforded to natives that resemble the invader.     

Can experienced birds select for Mullerian mimicry?

Field experiments have shown that avian predators in the wildcan select for similarity of warning signals in aposematic prey(Müllerian mimicry) because a common signal is better protectedthan a signal that is novel and rare. The original theory ofMüllerian mimicry assumes that the mechanism promotingmimicry is predator learning; by sharing a signal, the comimicspecies share the mortality that is due to sampling by inexperiencedpredators. Predation events have not been observed in the wild,and learning experiments with naive bird predators in a laboratoryhave not unambiguously shown a benefit of a uniform signal comparedwith different signals. As predators in the field experimentsare likely to be more experienced compared with previous laboratoryexperiments, we studied selection by experienced predators ona novel imperfect mimic. We trained great tits Parus major toavoid artificial aposematic models and subsequently introducedperfect and imperfect mimics at different frequencies. Birdswith prior experience on the models selected against the imperfectmimics that were at a disadvantage also in a memory test conducteda week after their introduction. Selection against the imperfectmimics was antiapostatic. However, the imperfect mimics alsobenefited from some signal generalization to the models andpossibly gained protection because the birds were familiar withthe alternative cryptic prey that was also present. Our resultssuggest that experienced predators might be more important tothe evolution of mimicry than the learning-based theory assumes.     

Predator hunting modes and predator–prey space games

Predators and prey are often engaged in a game where their expected fitnesses are affected by their relative spatial distributions. Game models generally predict that when predators and prey move at similar temporal and spatial scales that predators should distribute themselves to match the distribution of the prey's resources and that prey should be relatively uniformly distributed. These predictions should better apply to sit-and-pursue and sit-and-wait predators, who must anticipate the spatial distributions of their prey, than active predators that search for their prey. We test this with an experiment observing the spatial distributions and estimating the causes of movements between patches for Pacific tree frog tadpoles (Pseudacris regilla), a sit-and-pursue dragonfly larvae predator (Rhionaeschna multicolor), and an active salamander larval predator (Ambystoma tigrinum mavortium) when a single species was in the arena and when the prey was with one of the predators. We find that the sit-and-pursue predator favors patches with more of the prey's algae resources when the prey is not in the experimental arena and that the prey, when in the arena with this predator, do not favor patches with more resources. We also find that the active predator does not favor patches with more algae and that prey, when with an active predator, continue to favor these higher resource patches. These results suggest that the hunting modes of predators impact their spatial distributions and the spatial distributions of their prey, which has potential to have cascading effects on lower trophic levels.     

Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey

We investigated how the plant‐inhabiting, anthocorid predator, Anthocoris nemoralis, copes with variation in prey, host plant and associated herbivore‐induced plant volatiles and in particular whether the preference for these plant odours is innate or acquired. We found a marked difference between the olfactory response of orchard‐caught predators and that of their first generation reared on flour moth eggs in the laboratory, i.e. under conditions free of herbivory‐induced volatiles. Whereas the orchard‐caught predators preferred odour from psyllid‐infested pear leaves, when offered against clean air in a Y‐tube olfactometer, the laboratory‐reared first generation of (naive) predators did not. The same difference was found when a single component (methyl salicylate) of the herbivore‐induced plant volatiles was offered against clean air. After experiencing methyl salicylate with prey, however, the laboratory‐reared predators showed a pronounced preference for this volatile. This acquired preference did not depend on whether the volatile had been experienced in the juvenile period or in the adult phase, but it did depend on whether it had been offered in presence or absence of prey. In the first case, they were attracted to the plant volatile in subsequent olfactometer experiments, but when the volatile had been offered during a period of prey deprivation, the predators were not attracted. We conclude that associative learning is the most likely mechanism underlying acquired odour preference.     

Do native predators benefit from non‐native prey?

Despite knowledge on invasive species’ predatory effects, we know little of their influence as prey. Non‐native prey should have a neutral to positive effect on native predators by supplementing the prey base. However, if non‐native prey displace native prey, then an invader's net influence should depend on both its abundance and value relative to native prey. We conducted a meta‐analysis to quantify the effect of non‐native prey on native predator populations. Relative to native prey, non‐native prey similarly or negatively affect native predators, but only when studies employed a substitutive design that examined the effects of each prey species in isolation from other prey. When native predators had access to non‐native and native prey simultaneously, predator abundance increased significantly relative to pre‐invasion abundance. Although non‐native prey may have a lower per capita value than native prey, they seem to benefit native predators by serving as a supplemental prey resource.     

Predation pressure on an imperfect Batesian micicry complex in the presence of alternative prey

Summary Differential predation pressure and the probability of predation on a Batesian mimicry complex and on alternative prey were estimatedin a field experiment. The mimicry complex was composed of a noxious model (Eleodes obscura (Say)) and a palatable mimic (Stenomorpha marginata (LeConte)). House crickets (Acheta domesticus) (Linn.) were used as alternative prey. The experiment was conducted for 23 nights in August and September to approximate the peak seasonal activity time period during which both models and mimics normally are exposed to predation while foraging and depositing eggs. Each night thirty prey in ratios of 16 models: 7 mimics: 7 crickets were exposed for 2.5 h to a suite of predators consisting of pallid bats (Antrozous pallidus), striped skunks (Mephitis mephitis) and ringtails (Bassariscus astutus) that had free access to the prey. The model-mimic ratio was similar to that found in nature. Predators obtained prey on 11 of the 23 nights and preferred the alternative prey (crickets) in proportions higher than was expected from a predation rate that was equal on all species of prey. Mimics were taken by predators at a rate proportional to their abundance, while models were taken at a rate considerably lower than their relative abundance. This suggests that at least some of the predators could distinguish between models and mimics and were willing to eat the mimics at higher frequencies than they were willing to eat the models. However, although the mimicry is not perfect with respect to the entire predator suite, the mimics still gain an advantage by resembling the models, compared to the predation levels on the alternate prey.     

Mechanisms of group-hunting in vertebrates

Group-hunting is ubiquitous across animal taxa and has received considerable attention in the context of its functions. By contrast much less is known about the mechanisms by which grouping predators hunt their prey. This is primarily due to a lack of experimental manipulation alongside logistical difficulties quantifying the behaviour of multiple predators at high spatiotemporal resolution as they search, select, and capture wild prey. However, the use of new remote-sensing technologies and a broadening of the focal taxa beyond apex predators provides researchers with a great opportunity to discern accurately how multiple predators hunt together and not just whether doing so provides hunters with a per capita benefit. We incorporate many ideas from collective behaviour and locomotion throughout this review to make testable predictions for future researchers and pay particular attention to the role that computer simulation can play in a feedback loop with empirical data collection. Our review of the literature showed that the breadth of predator:prey size ratios among the taxa that can be considered to hunt as a group is very large (<10⁰ to >10²). We therefore synthesised the literature with respect to these predator:prey ratios and found that they promoted different hunting mechanisms. Additionally, these different hunting mechanisms are also related to particular stages of the hunt (search, selection, capture) and thus we structure our review in accordance with these two factors (stage of the hunt and predator:prey size ratio). We identify several novel group-hunting mechanisms which are largely untested, particularly under field conditions, and we also highlight a range of potential study organisms that are amenable to experimental testing of these mechanisms in connection with tracking technology. We believe that a combination of new hypotheses, study systems and methodological approaches should help push the field of group-hunting in new directions.     

Resource-Dependent Giving-Up Time of the Predatory Mite, Phytoseiulus persimilis

We examined the effect of prey (Tetranychus urticae) egg density on leaving rate of the predatory mite, Phytoseiulus persimilis, from leaf disks using predators with different feeding experiences and levels of external volatile cues related to their prey. Predators stayed longer on disks with prey eggs than on those without prey eggs. However, at each prey egg density predators stayed longer in the absence of prey-related volatiles from an external source. Starved predators stayed longer in a prey patch than those that had not experienced starvation. At each prey density, starved P. persimilis consumed a greater proportion of prey eggs than satiated predators. The total prey consumption of starved predators appears to be related to their longer residence time on source disks compared to satiated predators and also the per capita consumption rate was greater for starved predators compared to satiated predators.     

Habitat context influences predator interference interactions and the strength of resource partitioning

Despite increasing evidence that habitat structure can shape predator–prey interactions, few studies have examined the impact of habitat context on interactions among multiple predators and the consequences for combined foraging rates. We investigated the individual and combined effects of stone crabs (Menippe mercenaria) and knobbed whelks (Busycon carica) when foraging on two common bivalves, the hard clam (Mercenaria mercenaria) and the ribbed mussel (Geukensia demissa) in oyster reef and sand flat habitats. Because these species co-occur across these and other estuarine habitats of varying physical complexity, this system is ideal for examining how habitat context influences foraging rates and the generality of predator interactions. Consistent with results from previous studies, consumption rates of each predator in isolation from the other were higher in the sand flat than in the more structurally complex oyster reef habitat. However, consumption by the two predators when combined surprisingly did not differ between the two habitats. This counterintuitive result probably stems from the influence of habitat structure on predator–predator interactions. In the sand-flat habitat, whelks significantly reduced their consumption of their less preferred prey when crabs were present. However, the structurally more complex oyster reef habitat appeared to reduce interference interactions among predators, such that consumption rates when the predators co-occurred did not differ from predation rates when alone. In addition, both habitat context and predator–predator interactions increased resource partitioning by strengthening predator dietary selectivity. Thus, an understanding of how habitat characteristics such as physical complexity influence interactions among predators may be critical to predicting the effects of modifying predator populations on their shared prey.     

Foraging behavior of an estuarine predator, the blue crab Callinectes sapidus in a patchy environment

To define general principles of predator‐prey dynamics in an estuarine subtidal environment, we manipulated predator density (the blue crab, Callinectes sapidus) and prey (the clam, Macoma balthica) patch distribution in large field enclosures in the Rhode River subestuary of the central Chesapeake Bay. The primary objectives were to determine whether predators forage in a way that maximizes prey consumption and to assess how their foraging success is affected by density of conspecifics. We developed a novel ultrasonic telemetry system to observe behavior of individual predators with unprecedented detail. Behavior of predators was more indicative of optimal than of opportunistic foraging. Predators appeared responsive to the overall quality of prey in their habitat. Rather than remaining on a prey patch until depletion, predators appeared to vary their patch use with quality of the surrounding environment. When multiple (two) prey patches were available, residence time of predators on a prey patch was shorter than when only a single prey patch was available. Predators seemed to move among the prey patches fairly regularly, dividing their foraging time between the patches and consuming prey from each of them at a similar rate. That predators more than doubled their consumption of prey when we doubled the number of prey (by adding the second patch) is consistent with optimizing behaviors ‐ rather than with an opportunistic increase in prey consumption brought about simply by the addition of more prey. Predators at high density, however, appeared to interfere with each other's foraging success, reflected by their lower rates of prey consumption. Blue crabs appear to forage more successfully (and their prey to experience higher mortality) in prey patches located within 15–20 meters of neighboring patch, than in isolated patches. Our results are likely to apply, at least qualitatively, to other crustacean‐bivalve interactions, including those of commercial interest; their quantitative applicability will depend on the mobility of other predators and the scale of patchiness they perceive.