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.     

Age‐dependent responses to alarm calls depend on foraging activity in Willow Tits Poecile montanus

Survivorship in animals depends on both foraging activities and avoidance of predation, and thus behavioural decisions often reflect a trade‐off between predation risk and foraging efficiency. In this experimental study, we compared behavioural responses of free‐living adult and juvenile Willow Tits Poecile montanus to a conspecific alarm call in two treatments. The alarm call was played back when a focal bird was either not feeding, or feeding on a sunflower seed on the middle part of a spruce branch. When feeding at the time of the alarm call, juveniles more often stayed motionless or moved shorter distances than adults. Our results suggest that in hierarchical groups, juveniles are forced to take greater risks to maintain access to food or lack experience to optimize between food and safety.     

Acoustic stimuli from predators trigger behavioural responses in aggregate caterpillars

Prey detect their predators through predator signals and cues and, consequently, respond with anti‐predatory behaviours to inhibit the action of their aggressors. Lepidopterans can intercept signals emitted by predators and may defend themselves through chemical, morphological or behavioural responses. In this study, we investigated the effect of acoustic stimuli of different predators on defensive behaviour of gregarious caterpillars. Our results demonstrated that Hylesia nigricans (Lepidoptera, Saturniidae) caterpillars alter their behaviour (i.e. abruptly raising the head) in response to the acoustic stimulus of the predators (i.e. predation risk signals from birds and wasps). The magnitude of this response depended on predator identity and caterpillar body size. Larger caterpillars responded more strongly to predatory stimuli than smaller caterpillars. However, regardless of the size of the caterpillars, they responded more strongly to the stimuli of wasps. In addition, we identified that H. nigricans caterpillars emit ultrasonic noise after detecting the stimuli of the predators – this noise seems to function as an alert about the risk of predation during the early stages of development (second and fifth instars). The duration of ultrasonic emission (i.e. milliseconds) increases with the number of repetitions of the stimuli (i.e. wing‐beat sounds of the wasps and insectivorous birds). These results provide novel information about predation risk in interactions among caterpillars and their predators, and indicate possible communication among invertebrates mediated by the risk of predation.     

Greater energy stores enable flightless moulting geese to increase resting behaviour

Many species of waterfowl undergo a post‐breeding simultaneous flight feather moult (wing moult) which renders them flightless and vulnerable to predation for up to 4 weeks. Here we present an analysis of the correlations between individual time‐budgets and body mass states in 13 captive Barnacle Geese Branta leucopsis throughout an entire wing moult. The daily percentage of time spent resting was positively correlated with initial body mass at the start of wing moult. Behaviour of individual birds during wing moult is dependent on initial physiological state, which may in turn be dependent on foraging ability; the storage of energy before the start of wing moult will help birds to reduce exposure to the dangers of predation.     

Visual cues contribute to predator detection in anuran larvae

The ability of prey to detect predators directly affects their probability of survival. Chemical cues are known to be important for predator detection in aquatic environments, but the role of other potential cues is controversial. We tested for changes in behaviour of Rana temporaria tadpoles in response to chemical, visual, acoustic, and hydraulic cues originating from dragonfly larvae (Aeshna cyanea) and fish (Gasterosteus aculeatus). The greatest reduction in tadpole activity occurred when all cues were available, but activity was also significantly reduced by visual cues only. We did not find evidence for tadpoles lowering their activity in response to acoustic and hydraulic cues. There was no spatial avoidance of predators in our small experimental containers. The results show that anuran larvae indeed use vision for predator detection, while acoustic and hydraulic cues may be less important. Future studies of predator‐induced responses of tadpoles should not only concentrate on chemical cues but also consider visual stimuli. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

The key role of behaviour in animal camouflage

Animal camouflage represents one of the most important ways of preventing (or facilitating) predation. It attracted the attention of the earliest evolutionary biologists, and today remains a focus of investigation in areas ranging from evolutionary ecology, animal decision‐making, optimal strategies, visual psychology, computer science, to materials science. Most work focuses on the role of animal morphology per se, and its interactions with the background in affecting detection and recognition. However, the behaviour of organisms is likely to be crucial in affecting camouflage too, through background choice, body orientation and positioning; and strategies of camouflage that require movement. A wealth of potential mechanisms may affect such behaviours, from imprinting and self‐assessment to genetics, and operate at several levels (species, morph, and individual). Over many years there have been numerous studies investigating the role of behaviour in camouflage, but to date, no effort to synthesise these studies and ideas into a coherent framework. Here, we review key work on behaviour and camouflage, highlight the mechanisms involved and implications of behaviour, discuss the importance of this in a changing world, and offer suggestions for addressing the many important gaps in our understanding of this subject.     

Larvae of cryptic species of Anopheles gambiae respond differently to cues of predation risk

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Trait flexibility of generalist invertebrates exposed to contrasting predation and drying stressors

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Variability in the area,energy and time costs of wintering waders responding to disturbance

Birds’ responses to human disturbance are interesting due to their similarities to anti‐predator behaviour, and understanding this behaviour has practical applications for conservation management by informing measures such as buffer zones to protect priority species. To understand better the costs of disturbance and whether it will impact on population size, studies should quantify time‐related responses as well as the more commonly reported flight initiation distance (FID). Using waders wintering on an estuarine area, we experimentally disturbed foraging birds on the Wash Embayment, UK, by walking towards them and recording their responses (FID, alert time, time spent in flight, time taken to resume feeding, and total feeding time lost). We present data for 10 species of conservation concern: Curlew Numenius arquata, Oystercatcher Haematopus ostralegus, Bar‐tailed Godwit Limosa lapponica, Grey Plover Pluvialis squatarola, Redshank Tringa totanus, Knot Calidris canutus, Turnstone Arenaria interpres, Ringed Plover Charadrius hiaticula, Sanderling Calidris alba and Dunlin Calidris alpina. Larger species responded more strongly, response magnitude was greater under milder environmental conditions, and responses varied over both small and large spatial scales. The energetic costs of individual responses, however, were low relative to daily requirements and disturbance events were unlikely to be frequent enough to seriously limit foraging time. We suggest, therefore, that wintering wader populations on the Wash are not currently significantly negatively impacted by human disturbance during the intertidal foraging period. This is also likely to be the case at other estuarine sites with comparable access levels, visitor patterns, invertebrate food availability and environmental conditions.     

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

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

Losing anti‐predatory behaviour: A cost of translocation

Translocation of endangered species to habitats where exotic predators have been removed is now a common conservation practice around the world. Many of these translocated populations have thrived, and they are often used as sources for the harvesting of individuals for translocations to sites where exotic predators still exist, albeit at reduced densities. This study investigates how isolation from exotic predators affects the ability of individuals to recognize such predators using the North Island robin (Petroica longipes) as a model. The study was carried out in three robin populations in the North Island, New Zealand: a translocated population on Tiritiri Matangi Island, where exotic mammalian predators are absent; a population reintroduced from Tiritiri Matangi Island to Wenderholm Regional Park, a mainland site where these mammals are controlled to low densities; and a mainland population at Benneydale where exotic predatory mammals are common. The response intensity of robins to a model stoat was high at Benneydale and low at Tiritiri Matangi and Wenderholm. This result indicates that isolation from mammalian predators on Tiritiri Matangi has suppressed the ability of North Island robins to recognize these predators. It is possible that the low predatory mammal densities at Wenderholm have reduced robin contact with stoats, therefore reduced the opportunity for robins to learn to recognize stoats. Thus, translocation of individuals from populations without predators to places where key predators still exist could be unsuccessful if translocated individuals fail to perform appropriate anti‐predator behaviours.     

Basal metabolic rate and risk‐taking behaviour in birds

Basal metabolic rate (BMR) constitutes the minimal metabolic rate in the zone of thermo‐neutrality, where heat production is not elevated for temperature regulation. BMR thus constitutes the minimum metabolic rate that is required for maintenance. Interspecific variation in BMR in birds is correlated with food habits, climate, habitat, flight activity, torpor, altitude, and migration, although the selective forces involved in the evolution of these presumed adaptations are not always obvious. I suggest that BMR constitutes the minimum level required for maintenance, and that variation in this minimum level reflects the fitness costs and benefits in terms of ability to respond to selective agents like predators, implying that an elevated level of BMR is a cost of wariness towards predators. This hypothesis predicts a positive relationship between BMR and measures of risk taking such as flight initiation distance (FID) of individuals approached by a potential predator. Consistent with this suggestion, I show in a comparative analysis of 76 bird species that species with higher BMR for their body mass have longer FID when approached by a potential predator. This effect was independent of potentially confounding variables and similarity among species due to common phylogenetic descent. These results imply that BMR is positively related to risk‐taking behaviour, and that predation constitutes a neglected factor in the evolution of BMR.     

Habitat heterogeneity and mammalian predator–prey interactions

• 1 In predator–prey theory, habitat heterogeneity can affect the relationship between kill rates and prey or predator density through its effect on the predator's ability to search for, encounter, kill and consume its prey. Many studies of predator–prey interactions include the effect of spatial heterogeneity, but these are mostly based on species with restricted mobility or conducted in experimental settings.
• 2 Here, we aim to identify the patterns through which spatial heterogeneity affects predator–prey dynamics and to review the literature on the effect of spatial heterogeneity on predator–prey interactions in terrestrial mammalian systems, i.e. in freely moving species with high mobility, in non‐experimental settings. We also review current methodologies that allow the study of the predation process within a spatial context.
• 3 When the functional response includes the effect of spatial heterogeneity, it usually takes the form of predator‐dependent or ratio‐dependent models and has wide applicability.
• 4 The analysis of the predation process through its different stages may further contribute towards identifying the spatial scale of interest and the specific spatial mechanism affecting predator–prey interactions.
• 5 Analyzing the predation process based on the functional response theory, but separating the stages of predation and applying a multiscale approach, is likely to increase our insight into how spatial heterogeneity affects predator–prey dynamics. This may increase our ability to forecast the consequences of landscape transformations on predator–prey dynamics.

     

Foraging and Calling Behavior of Carolina chickadees (Poecile carolinensis) in Response to the Head Orientation of Potential Predators

When animals detect predators they modify their behavior to avoid predation. However, less is known about whether prey species modify their behavior in response to predator body and behavioral cues. Recent studies indicated that tufted titmice, a small songbird, decreased their foraging behavior and increased their calling rates when they detected a potential predator facing toward a feeder they were using, compared to a potential predator facing away from that feeder. Here, we tested whether related Carolina chickadees, Poecile carolinensis, were also sensitive not just to the presence of a predator model, but to its facial/head orientation. Although chickadees are closely related to titmice, recent studies in different populations suggest chickadees respond to risky contexts involving predators differently than titmice. We conducted two field studies near feeders the birds were exploiting. In Study One, a mask‐wearing human observer stood near the feeder. In Study Two, a model of a domestic cat was positioned near the feeder. In both studies, the potential threatening stimulus either faced toward or faced away from the feeder. Chickadees avoided the feeder more in both studies when the potential predator was present, and showed strongest feeder avoidance when the potential predator faced toward the feeder. Chickadee calling behavior was also affected by the facial orientation of the potential predator in Study 1. These results suggest that, like titmice, chickadees exhibit predation‐risk‐sensitive foraging and calling behavior, in relation to facial and head orientation of potential threats. These small birds seem to attend to the likely visual space of potential predators. Sensitivity to predator cues like behavior and body posture must become more central to our theories and models of anti‐predator behavioral systems.     

Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues

While ocean acidification is predicted to threaten marine biodiversity, the processes that directly impact species persistence are not well understood. For marine species, early life history stages are inherently vulnerable to predators and an innate ability to detect predators can be critical for survival. However, whether or not acidification inhibits predator detection is unknown. Here, we show that newly hatched larvae of the marine fish Amphiprion percula innately detect predators using olfactory cues and this ability is retained through to settlement. Aquarium-reared larvae, not previously exposed to predators, were able to distinguish between the olfactory cues of predatory and non-predatory species. However, when eggs and larvae were exposed to seawater simulating ocean acidification (pH 7.8 and 1000 p.p.m. CO₂) settlement-stage larvae became strongly attracted to the smell of predators and the ability to discriminate between predators and non-predators was lost. Newly hatched larvae were unaffected by CO₂ exposure and were still able to distinguish between predatory and non-predatory fish. If this impairment of olfactory preferences in settlement-stage larvae translates to higher mortality as a result of increased predation risk, there could be direct consequences for the replenishment and the sustainability of marine populations.
Ecology Letters (2010) 13: 68–75     

Temporal variation in behavioral responses to dietary cues from a gape‐limited predator in tadpole prey: A test of the phylogenetic relatedness hypothesis

The ability of prey to recognize and adequately respond to predators determines their survival. Predator‐borne, post‐digestion dietary cues represent essential information for prey about the identity and the level of risk posed by predators. The phylogenetic relatedness hypothesis posits that prey should respond strongly to dietary cues from closely related heterospecifics but respond weakly to such cues from distantly related prey, following a hierarchical pattern. While such responses have mostly been observed in prey at their first encounter with predators, whether prey maintain such hierarchical levels of investment through time remains unclear. We investigated this question by exposing Rhacophorus arboreus tadpoles to the non‐consumptive effect of gape‐limited newt predators Cynops pyrrhogaster that were fed one of five prey diets across a gradient of phylogenetic relatedness: frog tadpoles (Rhacophorus arboreus, Rhacophorus schlegelii, Pelophylax nigromaculatus, and Hyla japonica) and medaka fish (Oryzias latipes). Predators’ diet, time, and their interaction significantly influenced tadpole activity level. We found support for the phylogenetic relatedness hypothesis: Investments in defense were stronger to cues from tadpole diets than to cues from fish diet. However, such a hierarchical response was recorded only in the first four days following predator exposure, then gradually disappear by day 8 on which the tadpoles exhibited similar activity level across all predator treatments. The findings suggest that, at least under the threat of gape‐limited predators, prey use phylogenetic information to evaluate risk and appropriately invest in defense during early encounters with predators; however, energy requirements may prevent prey from maintaining a high level of defense over long exposure to predation risk.     

Non‐pathogenic aquatic bacteria activate the immune system and increase predation risk in damselfly larvae

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