Cryptic Prey Research Articles

In paired preference tests, domestic chicks innately choose the colour green over red, and the shape of a frog over a sphere when both stimuli are green

Many animals express unlearned colour preferences that depend on the context in which signals are encountered. These colour biases may have evolved in response to the signalling system to which they relate. For example, many aposematic animals advertise their unprofitability with red warning signals. Predators’ innate biases against these warning colours have been suggested as one of the potential explanations for the initial evolution of aposematism. It is unclear, however, whether unlearned colour preferences reported in a number of species is truly an innate behaviour or whether it is based on prior experience. We tested the spontaneous colour and shape preferences of dark-hatched, unfed, and visually naive domestic chicks (Gallus gallus). In four experiments, we presented chicks with a choice between either red (a colour typically associated with warning patterns) or green (a colour associated with palatable cryptic prey), volume-matched spheres (representing a generalised fruit shape) or frogs (representing an aposematic animal’s shape). Chicks innately preferred green stimuli and avoided red. Chicks also preferred the shape of a frog over a sphere when both stimuli were green. However, no preference for frogs over spheres was present when stimuli were red. Male chicks that experienced a bitter taste of quinine immediately before the preference test showed a higher preference for green frog-shaped stimuli. Our results suggest that newly hatched chicks innately integrate colour and shape cues during decision making, and that this can be augmented by other sensory experiences. Innate and experience-based behaviour could confer a fitness advantage to novel aposematic prey, and favour the initial evolution of conspicuous colouration.

The effect of anthropogenic noise on foraging and vigilance in zoo housed pied tamarins

The phenomenon of human-induced rapid environmental change (HIREC) is a great challenge in the modern world that presents a threat to all species. Research on the effect of anthropogenic noise on free-living wildlife is increasing but the effect of anthropogenic noise on the behaviour and welfare of captive wildlife has received limited attention, even though captive settings are full of human activity and a wide range of sounds. Moreover, studies in captivity tend to classify noise subjectively by volume according to human hearing and as part of the overall ‘visitor effect’ rather than a stressor in its own right. Research on free-living wildlife suggests that anthropogenic noise can negatively impact foraging behaviour; similar impacts in captive species could have a detrimental effect on their health and welfare if animals cannot perform functional feeding behaviours and access adequate nutrition. In the current study, we designed a forage box experiment for captive pied tamarins, a Critically Endangered callitrichid primate species that is prone to poor physical health and breeding success in captivity. Ten pairs of tamarins housed at Jersey Zoo were provided with a forage box containing cryptic (hidden) prey items (waxworms). Using a within-subjects design, tamarins were provided access to the forage box in noise and non-noise conditions of anthropogenic noise (machinery used for gardening in the zoo). Both active (foraging with the hands) and observational (looking into the forage box) foraging were significantly less frequent in the presence of anthropogenic noise; however, there was no difference in the duration of these behaviours or in foraging success. Furthermore, the presence of anthropogenic noise did not significantly affect vigilance behaviour. We found no sex differences in the effect of noise, and our results suggest that the anthropogenic noise we tested was only a minimal distractor for tamarins. However, large individual differences in foraging suggest that other factors may have a larger impact on foraging than the anthropogenic noise used in this experiment. More research into how captive animals may respond to the presence of anthropogenic noise is needed.

Artificial fruits and nuts for studying predation of cryptic prey: a case of 3D‐printed coffee berries for studying predation of coffee berry borer by flat bark beetles

AbstractStudying the effects of predation in cryptic herbivorous insects is difficult because many spend all or most of their life cycle inside their host plant. Here, we designed and 3D‐printed artificial coffee berries to study predation of coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae, Scolytinae), by the flat bark beetle, Cathartus quadricollis (Guerin‐Meneville) (Coleoptera: Silvanidae). The 3D‐printed berries were tested under laboratory and field conditions and the results confirmed the usefulness of 3D‐printed materials to create life‐like models for studying predation.

Selfish herd effects depend on prey crypsis

Determining why some animals form groups while others remain solitary is a longstanding goal in behavioural ecology. Group formation can help mitigate predation risk through various mechanisms, including risk dilution and group vigilance. The selfish herd hypothesis proposes that prey can reduce their risk by minimizing the area around which all points in that area are closer to them than to another conspecific (i.e. by minimizing their ‘domain of danger’ (DOD)). This hypothesis assumes that an individual's predation risk is proportional to the size of its DOD; however, the relationship between risk and proximity to conspecifics may depend on additional factors. Specifically, approaching conspecifics may be costly for prey that rely on crypsis because group formation increases detectability. Using plasticine model prey, we experimentally manipulated prey coloration as well as the DOD, and then tracked their ‘survival’ under natural field conditions. We found that an individual's predation risk increased with their DOD for conspicuous (red) prey, but decreased with the DOD in cryptic (green) prey. Our results are consistent with patterns in natural systems and indicate that the relationship between predation risk and DOD depends on additional factors like prey coloration.

Social context affects camouflage in a cryptic fish species.

Crypsis, or the ability to avoid detection and/or recognition, is an important and widespread anti-predator strategy across the animal kingdom. Many animals are able to camouflage themselves by adapting their body colour to the local environment. In particular, rapid changes in body colour are often critical to the survival of cryptic prey which rely on evading detection by predators. This is especially pertinent for animals subject to spatio-temporal variability in their environment, as they must adapt to acute changes in their visual surroundings. However, which features of the local environment are most relevant is not well understood. In particular, little is known about how social context interacts with other environmental stimuli to influence crypsis. Here, we use a common cryptic prey animal, the goby (Pseudogobius species 2) to examine how the presence and body colour of conspecifics influence the rate and extent to which gobies change colour. We find that solitary gobies change colour to match their background faster and to a greater extent than gobies in pairs. Further, we find that this relationship holds irrespective of the colour of nearby conspecifics. This study demonstrates the importance of social context in mediating colour change in cryptic animals.

Anatomy of the sense of touch in sea otters: Cutaneous mechanoreceptors and structural features of glabrous skin.

Sea otters (Enhydra lutris) demonstrate rapid, accurate tactile abilities using their paws and facial vibrissae. Anatomical investigations of neural organization in the vibrissal bed and somatosensory cortex coincide with measured sensitivity, but no studies describe sensory receptors in the paws or other regions of glabrous (i.e., hairless) skin. In this study, we use histology to assess the presence, density, and distribution of mechanoreceptors in the glabrous skin of sea otters: paws, rhinarium, lips, and flipper digits, and we use scanning electron microscopy to describe skin-surface texture and its potential effect on the transduction of mechanical stimuli. Our results confirm the presence of Merkel cells and Pacinian corpuscles, but not Meissner corpuscles, in all sea otter glabrous skin. The paws showed the highest density of Merkel cells and Pacinian corpuscles. Within the paw, relative densities of mechanoreceptor types were highest in the distal metacarpal pad and digits, which suggests that the distal paw is a tactile fovea for sea otters. In addition to the highest receptor density, the paw displayed the thickest epidermis. Rete ridges (epidermal projections into the dermis) and dermal papillae (dermal projections into the epidermis) were developed across all glabrous skin. These quantitative and qualitative descriptions of neural organization and physical features, combined with previous behavioral results, contribute to our understanding of how structure relates to function in the tactile modality. Our findings coincide with behavioral observations of sea otters, which use touch to maintain thermoregulatory integrity of their fur, explore objects, and capture visually cryptic prey.

Seasonal variations in bird selection pressure on prey colouration

The direction and strength of selection for prey colouration by predators vary in space and time and depend on the composition of the predator community. We tested the hypothesis that bird selection pressure on prey colouration changes through the season due to changes in the proportion of naïve juvenile individuals in the bird community, because naïve and educated birds differ in their responses to prey colours. Bird predation on caterpillar-shaped plasticine models in two boreal forest sites increased sevenfold from early summer to mid-summer, and the time of this increase coincides with the fledging of juvenile birds. In early summer, cryptic (black and green) models were attacked at fivefold higher rates compared with conspicuous (red and yellow) models. By contrast, starting from fledging time, cryptic and conspicuous models were attacked at similar rates, hinting at a lower selectivity by naïve juvenile birds compared with educated adult birds. Cryptic models exposed in a group together with conspicuous models were attacked by birds at a threefold lower rate than cryptic models exposed singly, thus supporting the aposematic commensalism hypothesis. However, this effect was not observed in mid- and late summer, presumably due to the lack of avoidance of conspicuous prey by the juvenile birds. We conclude that selection pressure on prey colouration weakens considerably when naïve birds dominate in the community, because the survival advantages of aposematic colouration are temporarily lost for both the conspicuous and their neighbouring cryptic prey.

A procedural analogue of prey detection and applied signal detection

Researchers have employed a variety of laboratory analogues of cryptic prey detection and applied signal detection to study factors influencing learning and performance in these ethological and applied scenarios. However, these procedural analogues do not appear to map closely onto their “real-world” counterparts, particularly with respect to the role of the “yes” (i.e., “attack”) response and the payoff for this response (or its absence) on signal-present and signal-absent trials. Using domestic hens, we developed a procedural analogue in which a “yes” response requires some time to emit; such responses were reinforced only in the presence of a signal. In Experiment 1, we evaluated the influence of the “yes” response requirement by manipulating the number of responses required to qualify as a “yes” response. As the “yes” response requirement was increased, bias toward responding “no” increased, revealing that this is a critical factor controlling accuracy in this procedure. In Experiment 2, we evaluated the influence of signal probability and reinforcement rate on signal detection accuracy and found that neither of these factors significantly influenced accuracy or bias. These findings suggest that this procedural analogue may represent a valuable alternative for studying behaviour in relevant signal detection scenarios.

Size-dependent predation risk in cryptic prey

Visual crypsis of prey is determined by the interaction between an individual’s physical appearance to their predators and visual aspects of their environment. Physical size will impact visual appearance and thus potentially influence crypsis. However, research on this topic is limited, leaving the effect of size in cryptic prey largely unexplored. To identify if the success of cryptic phenotypes is size-dependent, we conducted a series of field experiments in which we exposed two types of cryptic artificial prey (uniform colored and disruptively patterned) of different sizes to free-living avian predators and recorded attack rate. Despite similar statistical power and methodology, we found increasing predation risk with increasing size only for disruptive phenotypes. Our results suggest that large sizes may break down ability for disruptive patterns to effectively break up the body outline. However, further research in more controlled conditions would be needed to distinguish the effects of initial detection and post-detection preferences on attack rates.

Predator personality and prey detection: inter-individual variation in responses to cryptic and conspicuous prey

Limited attention constrains predators from engaging in cognitively demanding tasks such as searching for cryptic prey at the same time as remaining vigilant towards threats. Since finite attention can result in negative correlations between foraging and vigilance, the tendency of individual predators to focus attention on searching for cryptic prey may be correlated with other behavioural traits which reflect risk-reward trade-offs, such as consistent inter-individual variation in boldness (a personality trait describing risk-taking, defined in this study as the time taken to leave a refuge). We investigated the importance of personality in prey detection by comparing inter-individual variation in the response of three-spined sticklebacks (Gasterosteus aculeatus) to conspicuous and cryptic prey. Fish were slower to attack cryptic prey than conspicuous prey, consistent with cryptic prey being harder to detect. Despite the greater challenge involved in detecting cryptic prey, inter-individual variation in the time taken to detect prey was similar in the cryptic and conspicuous prey treatments, and was uncorrelated with boldness, which was repeatable between individuals. We also observed a positive association between the rate of attack on conspicuous prey and whether individual fish attacked cryptic prey in other trials. Our findings suggest that boldness is not related to prey detection or attention in this context. Instead, consistent differences in motivation once exploration has begun between individual predators may explain inter-individual variation in the time taken to attack both prey cryptic and conspicuous prey.Significance statementUsing an experimental approach to manipulate the conspicuousness of prey, we show that individual fish consistently differ in their rates of attacking prey. This demonstrates that fish show “personality variation” in predatory behaviour, but these inter-individual differences were not related to the boldness of each fish (their tendency to engage in risky behaviours).

The signal detection problem of aposematic prey revisited: integrating prior social and personal experience.

Ever since Alfred R. Wallace suggested brightly coloured, toxic insects warn predators about their unprofitability, evolutionary biologists have searched for an explanation of how these aposematic prey evolve and are maintained in natural populations. Understanding how predators learn about this widespread prey defence is fundamental to addressing the problem, yet individuals differ in their foraging decisions and the predominant application of associative learning theory largely ignores predators' foraging context. Here we revisit the suggestion made 15 years ago that signal detection theory provides a useful framework to model predator learning by emphasizing the integration of prior information into predation decisions. Using multiple experiments where we modified the availability of social information using video playback, we show that personal information (sampling aposematic prey) improves how predators (great tits, Parus major) discriminate between novel aposematic and cryptic prey. However, this relationship was not linear and beyond a certain point personal encounters with aposematic prey were no longer informative for prey discrimination. Social information about prey unpalatability reduced attacks on aposematic prey across learning trials, but it did not influence the relationship between personal sampling and discrimination. Our results suggest therefore that acquiring social information does not influence the value of personal information, but more experiments are needed to manipulate pay-offs and disentangle whether information sources affect response thresholds or change discrimination. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Anthropogenic noise impairs foraging for cryptic prey via cross-sensory interference.

Anthropogenic noise levels are globally rising with profound impacts on ecosystems and the species that live in them. Masking or distraction by noise can interfere with relevant sounds and thereby impact ecological interactions between individuals of the same or different species. Predator-prey dynamics are particularly likely to be influenced by rising noise levels, with important population- and community-level consequences, as species may differentially adapt to noise disturbance. Acoustic noise can, however, also impair the use of visual information by animals through the process of cross-sensory interference, possibly impacting species interactions that have so far been largely ignored by noise impact studies. Here, we assessed how noise affected the performance of great tit (Parus major) foraging on cryptic prey. Birds trained individually to search for paper moths differing in the level of camouflage with the test background were tested in the presence and absence of noise. We found that noise significantly increased approach and attack latencies, but that the effect depended on the level of crypsis. Noise increased latencies for cryptic prey targets, but not for conspicuous and colour-matched prey targets. Our results show that noise can interfere with the processing of visual information, particularly in difficult tasks such as separating objects from a similar looking background. These results have important ecological and evolutionary implications as they demonstrate how globally rising anthropogenic noise levels can influence the arms race between predators and prey across sensory domains.

In the corner of the eye: camouflaging motion in the peripheral visual field.

Most animals need to move, and motion will generally break camouflage. In many instances, most of the visual field of a predator does not fall within a high-resolution area of the retina and so, when an undetected prey moves, that motion will often be in peripheral vision. We investigate how this can be exploited by prey, through different patterns of movement, to reduce the accuracy with which the predator can locate a cryptic prey item when it subsequently orients towards a target. The same logic applies for a prey species trying to localize a predatory threat. Using human participants as surrogate predators, tasked with localizing a target on peripherally viewed computer screens, we quantify the effects of movement (duration and speed) and target pattern. We show that, while motion is certainly detrimental to camouflage, should movement be necessary, some behaviours and surface patterns reduce that cost. Our data indicate that the phenotype that minimizes localization accuracy is unpatterned, having the mean luminance of the background, does not use a startle display prior to movement, and has short (below saccadic latency), fast movements.

Transparency improves concealment in cryptically coloured moths.

Predation is a ubiquitous and strong selective pressure on living organisms. Transparency is a predation defence widespread in water but rare on land. Some Lepidoptera display transparent patches combined with already cryptic opaque patches. A recent study showed that transparency reduced detectability of aposematic prey with conspicuous patches. However, whether transparency has any effect at reducing detectability of already cryptic prey is still unknown. We conducted field predation experiments with free avian predators where we monitored and compared survival of a fully opaque grey artificial form (cryptic), a form including transparent windows and a wingless artificial butterfly body. Survival of the transparent forms was similar to that of wingless bodies and higher than that of fully opaque forms, suggesting a reduction of detectability conferred by transparency. This is the first evidence that transparency decreases detectability in cryptic terrestrial prey. Future studies should explore the organization of transparent and opaque patches in animals and their interplay on survival, as well as the costs and other potential benefits associated with transparency on land.

Consistent Associations between Body Size and Hidden Contrasting Color Signals across a Range of Insect Taxa.

While there have been a number of recent advances in our understanding of the evolution of animal color patterns, much of this work has focused on color patterns that are constantly displayed. However, some animals hide functional color signals and display them only transiently through behavioral displays. These displays are widely employed as a secondary defense following detection when fleeing (flash display) or when stationary (deimatic display). Yet if displays of hidden colors are so effective in deterring predation, why have not all species evolved them? An earlier study suggested that the hidden antipredatory color signals in insects are more likely to have evolved in species with large size because either (or both) (i) large cryptic prey are more frequently detected and pursued or (ii) hidden color signals in large prey are more effective in deterring predation than in small prey. These arguments should apply universally to any prey that use hidden signals, so the association between large size and hidden contrasting color signals should be evident across diverse groups of prey. In this study, we tested this prediction in five different groups of insects. Using phylogenetically controlled analysis to elucidate the relationship between body size and color contrast between forewings and hind wings, we found evidence for the predicted size-color contrast associations in four different groups of insects, namely, Orthoptera, Phasmatidae, Mantidae, and Saturniidae, but not in Sphingidae. Collectively, our study indicates that body size plays an important role in explaining variation in the evolution of hidden contrasting color signals in insects.

Anuran predators overcome visual illusion: dazzle coloration does not protect moving prey.

Predators everywhere impose strong selection pressures on the morphology and behavior of their prey, but the resulting antipredator adaptations vary greatly among species. Studies of adaptive coloration in prey species have generally focused on cryptic or aposematic prey, with little consideration of color patterns in palatable mobile prey. Complex color patterns have been proposed to decrease the ability of visual predators to capture moving prey (motion dazzle effect). Most support for this hypothesis, however, comes from experiments with human subjects and simulated prey. We tested the motion dazzle effect using, for the first time, natural predators (cane toads, Rhinella marina) and live prey (house crickets, Acheta domesticus) with altered color patterns. We found no support for the motion dazzle effect as striped crickets did not fare better than solid colored ones. Crickets that spent more time moving, however, were more likely to be eaten. Our results suggest that motion specialized visual predators such as toads overcome the motion dazzle effect and impose stronger selection pressure on prey behavior than on coloration. These findings emphasize the importance of sensory specializations of predators in mediating antipredator strategies.

Flash behavior increases prey survival

Flash behavior, in which otherwise cryptic prey exhibit conspicuous coloration or noise when fleeing from potential predators, has been postulated to hinder location of prey once they become stationary. Here, using artificial computer-generated prey and humans as visual predators, we show that human subjects are more likely to abandon their search for prey that flash, compared to continuously cryptic fleeing controls. Survivorship of flashing prey was an additional 20% higher than the survivorship of continuously cryptic prey, depending on the background against which it was depicted. This survivorship advantage was consistent regardless of whether prey showed flash colors continuously or intermittently during flight. The advantage over continuously cryptic prey was highest when the flashing prey was presented first. Likewise, the more search areas containing no prey that the volunteers had initially viewed, the more likely they were to give up when there was a cryptic prey present. Collectively, these 3 findings indicate that volunteers inferred the flashing prey was absent from the search area when they failed to see a prey in the same form as they saw it move. Our results demonstrate first proof of concept: flash behavior, widely seen in taxa from insects to mammals, is an effective antipredator escape mechanism.

Social transmission of avoidance among predators facilitates the spread of novel prey.

Warning signals are an effective defence strategy for aposematic prey, but only if they are recognized by potential predators. If predators must eat prey to associate novel warning signals with unpalatability, how can aposematic prey ever evolve? Using experiments with great tits (Parus major) as predators, we show that social transmission enhances the acquisition of avoidance by a predator population. Observing another predator's disgust towards tasting one novel conspicuous prey item led to fewer aposematic than cryptic prey being eaten for the predator population to learn. Despite reduced personal encounters with unpalatable prey, avoidance persisted and increased over subsequent trials. Next we use a mathematical model to show that social transmission can shift the evolutionary trajectory of prey populations from fixation of crypsis to fixation of aposematism more easily than was previously thought. Therefore, social information use by predators has the potential to have evolutionary consequences across ecological communities.

First Observation of a Disturbance Foraging Association between Obligate Ant-following Birds and a Tamandua Anteater in Central Panama

ABSTRACT.— Disturbance foraging – the use of disturbances created by other animals to locate cryptic or sedentary prey – is a widespread phenomenon, particularly in birds. In the Neotropics, a prominent example of disturbance foraging in birds is their relationship with army ants (Eciton burchellii). Numerous bird species attend army ant swarms and forage on the prey that the ants flush from the leaf litter. Here, I document a previously undescribed disturbance foraging association between two species of obligate ant-following birds and a small anteater, the northern tamandua (Tamandua mexicana). I observed both bird species approach and forage on fallen termites underneath the anteater, which was excavating a termite nest. The foraging association appeared to be a commensal relationship – the antbirds obtained a foraging benefit from the anteater, which was in turn unaffected by the birds. My observation suggests that ant-following birds may respond to other disturbances in addition to army ant swarms to...

Body size affects the evolution of hidden colour signals in moths.

Many cryptic prey have also evolved hidden contrasting colour signals which are displayed to would-be predators. Given that these hidden contrasting signals may confer additional survival benefits to the prey by startling/intimidating predators, it is unclear why they have evolved in some species, but not in others. Here, we have conducted a comparative phylogenetic analysis of the evolution of colour traits in the family Erebidae (Lepidoptera), and found that the hidden contrasting colour signals are more likely to be found in larger species. To understand why this relationship occurs, we present a general mathematical model, demonstrating that selection for a secondary defence such as deimatic display will be stronger in large species when (i) the primary defence (crypsis) is likely to fail as its body size increases and/or (ii) the secondary defence is more effective in large prey. To test the model assumptions, we conducted behavioural experiments using a robotic moth which revealed that survivorship advantages were higher against wild birds when the moth has contrasting hindwings and large size. Collectively, our results suggest that the evolutionary association between large size and hidden contrasting signals has been driven by a combination of the need for a back-up defence and its efficacy.