Prey Colour Research Articles

Exploration correlates with dietary choosiness and avoidance learning style in a generalist predator

Abstract The hypothesis of slow-fast syndromes predicts a correlation between personality type and learning style; fast explorers would have a more proactive (fast but inflexible) learning style whereas slow explorers would be more reactive (slow but flexible) learners. Empirical evidence for this personality-cognition coupling remains inconclusive and heavily biased towards birds. Moreover, most studies did not examine the personality-cognition correlation when the cognitive task is discerning food quality, a scenario directly related to energy acquisition that underpins the evolution of slow-fast syndromes. In this study, we examined the exploration-cognition correlation in the context of avoidance learning in an opportunistic predator - the common sun skink Eutropis multifasciata. We quantified exploration tendencies of individuals in an unfamiliar environment and compared foraging behaviors when lizards associated prey color and taste during the initial learning trials and subsequent reverse learning trials, where the color-taste associations were switched. We found that fast explorers were less choosy and modified their foraging behaviors less with experience, conforming to a more proactive cognitive style. In contrast, slow explorers were reactive learners and were able to change foraging behaviors in both learning and reverse learning phases, even though the ability to do so depended on the color-taste treatment. Contrary to conventional predictions, the proactive-reactive learning styles in our focal species was not differentiated by a learning speed-flexibility trade-off. Our findings offer nuanced support to the slow-fast syndromes and suggest that the two types of exploration-cognition correlations could be different responses to fast-changing environmental predictability.

Habitat heterogeneity limits prey colour polymorphism maintained via negative frequency-dependent selection.

The persistence of non-neutral trait polymorphism is enigmatic because stabilizing selection is expected to deplete variation. In cryptically coloured prey, negative frequency-dependent selection due to search image formation by predators has been proposed to favour rare variants, promoting polymorphism. However, in a heterogeneous environment, locally varying disruptive selection favours patch type-specific optima, resulting in spatial segregation of colour variants. Here, we address whether negative frequency-dependent selection can overcome selection posed by habitat heterogeneity to promote local polymorphism using an individual-based model. In addition, we compare how prey and predator mobility may modify the outcome. Our model revealed that frequency-dependent predation could strongly promote local prey polymorphism, but only when differences between morphs in patch-specific fitness were small. The effect of frequency-dependent predation depended on the predator adjustment of search image and was hampered by the prey population structure. Gene flow due to prey movement counteracted local selection, promoted local polymorphism to some extent, and relaxed the conditions for polymorphism due to frequency-dependent predation. Importantly, abrupt spatial changes in morph frequencies decreased the probability that mobile frequency-dependent predators could maintain local prey polymorphism. Overall, our study suggests that in a spatially heterogeneous environment, negative frequency-dependent selection may help maintain local polymorphism but only under a limited range of conditions.

Intricate covariation between exploration and avoidance learning in a generalist predator

Abstract Many predators avoid unprofitable prey by learning to use visual features of the prey as reliable indicators of quality. However, individual variation in avoidance learning is rarely examined in detail. It has been hypothesized that better avoidance learning ability might correlate with faster exploration tendency, but available data are limited in both quantity and scope. In this study, we examined the covariation between exploration, foraging decisions, and avoidance learning in a generalist lizard Eutropis multifasciata to test the prediction that faster explorers are also better avoidance learners. We also examined how sex, population, and color of unpalatable prey might mediate the exploration-avoidance learning covariation. We collected data on exploration and foraging behavior in individuals from two allopatric populations and quantified changes in foraging decisions over five daily learning trials, in which individuals were presented with normal- and bitter-tasting prey that differed consistently in color. Even though bitter prey elicited strong negative responses, lizards overall did not avoid consuming fewer such prey with learning. Instead, they learned to prioritize on palatable prey as the experiment progressed. In concordance with our prediction, we found that faster explorers were generally better avoidance learners, even though sex, population, and prey color were also important. Our study represents a rare experimental test of the exploration-avoidance learning covariation, especially in non-avian systems. Our results suggest that unpalatability might be an ineffective defense against generalist predators such as E. multifasciata and that faster explorers might impose stronger selection for the evolution of warning signals in unprofitable prey.

Evidence for frequency-dependent selection in House Wrens, but not Eastern Bluebirds

Frequency-dependent selection occurs when predators alter their prey choice to target abundant prey. We tested whether two species of insectivorous songbirds exhibited similar frequency-dependent selection behavior. House Wren (Troglodytes aedon) and Eastern Bluebird (Sialia sialis) routinely occupy nest boxes established over 700 acres at Missouri Western State University. During the 2018 breeding season from April through July, House Wrens consumed more sentinel prey from the color station that had previously appeared in higher frequency after four days of training. Eastern Bluebirds did not consume more of the previously abundant prey color stations and neither species showed a preference when the abundant color was reversed for the second half of the experiment which may be explained by latency in switching previously learned behaviors. Consequently, House Wrens demonstrated an initial frequency-dependent foraging strategy, but the Eastern Bluebirds did not. These results indicate how generalist insectivores that nest in the same habitat differ in their foraging strategies and behaviors.

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.

Detectability and predator strategy affect egg depredation rates: Implications for mitigating nest depredation in farmlands

Predation is a major evolutionary force in animal ecology. Mechanisms by which prey coloration provides camouflage has been widely studied. However, predator response to prey camouflage and concealment has received less attention. Understanding vegetation structure effect on depredation success could help managers design strategies to mitigate the depredation of managed species (e.g., threatened or hunted). We aimed to investigate the relationship between depredation rate, nest camouflage and concealment in ground-nesting birds of farmlands, and their predators. We set up an experiment of 2576 artificial ground nests to assess the role of egg coloration (white, light green, and dark green), egg size (small, medium, and large), and vegetation structure (vegetation height and land use) in nest survival rates. We also explored the role of predator searching strategies by analysing clumped depredation and multiple depredation events. Of the nests, 34.0% were depredated, with corvids as the predators 78.5% of the time. Corvid depredation decreased by 40–60% in grasslands and spring crops above a vegetation height of 30 cm. In contrast, vegetation height and land use may be of far less importance in avoiding depredation by other predators. The probability of depredation was spatially clumped, suggesting that predators increase search effort in areas where a nest was previously encountered. Neighboring depredation and depredation repetition were more frequent in corvids than in other predators. Our study indicates that nests in vegetation higher than 30 cm had a drastic reduction in depredation rates by corvids. Management of vegetation structure is a key tool to mitigate depredation risk, and improving the availability of alternative food resources may be a complementary tool.

Context-dependent coloration of prey and predator decision making in contrasting light environments.

A big question in behavioral ecology is what drives diversity of color signals. One possible explanation is that environmental conditions, such as light environment, may alter visual signaling of prey, which could affect predator decision-making. Here, we tested the context-dependent predator selection on prey coloration. In the first experiment, we tested detectability of artificial visual stimuli to blue tits (Cyanistes caeruleus) by manipulating stimulus luminance and chromatic context of the background. We expected the presence of the chromatic context to facilitate faster target detection. As expected, blue tits found targets on chromatic yellow background faster than on achromatic grey background whereas in the latter, targets were found with smaller contrast differences to the background. In the second experiment, we tested the effect of two light environments on the survival of aposematic, color polymorphic wood tiger moth (Arctia plantaginis). As luminance contrast should be more detectable than chromatic contrast in low light intensities, we expected birds, if they find the moths aversive, to avoid the white morph which is more conspicuous than the yellow morph in low light (and vice versa in bright light). Alternatively, birds may attack first moths that are more detectable. We found birds to attack yellow moths first in low light conditions, whereas white moths were attacked first more frequently in bright light conditions. Our results show that light environments affect predator foraging decisions, which may facilitate context-dependent selection on visual signals and diversity of prey phenotypes in the wild.

Sexually dimorphic dorsal coloration in a jumping spider: testing a potential case of sex-specific mimicry.

To avoid predation, many animals mimic behaviours and/or coloration of dangerous prey. Here we examine potential sex-specific mimicry in the jumping spider Habronattus pyrrithrix. Previous work proposed that males' conspicuous dorsal coloration paired with characteristic leg-waving (i.e. false antennation) imperfectly mimics hymenopteran insects (e.g. wasps and bees), affording protection to males during mate-searching and courtship. By contrast, less active females are cryptic and display less leg-waving. Here we test the hypothesis that sexually dimorphic dorsal colour patterns in H. pyrrithrix are most effective when paired with sex-specific behaviours. We manipulated spider dorsal coloration with makeup to model the opposite sex and exposed them to a larger salticid predator (Phidippus californicus). We predicted that males painted like females should suffer higher predation rates than sham-control males. Likewise, females painted like males should suffer higher predation rates than sham-control females. Contrary to expectations, spiders with male-like coloration were attacked more than those with female-like coloration, regardless of their actual sex. Moreover, males were more likely to be captured, and were captured sooner, than females (regardless of colour pattern). With these unexpected negative results, we discuss alternative functional hypotheses for H. pyrrithrix colours, as well as the evolution of defensive coloration generally.

Variable crab camouflage patterns defeat search image formation

Understanding what maintains the broad spectrum of variation in animal phenotypes and how this influences survival is a key question in biology. Frequency dependent selection – where predators temporarily focus on one morph at the expense of others by forming a “search image” – can help explain this phenomenon. However, past work has never tested real prey colour patterns, and rarely considered the role of different types of camouflage. Using a novel citizen science computer experiment that presented crab “prey” to humans against natural backgrounds in specific sequences, we were able to test a range of key hypotheses concerning the interactions between predator learning, camouflage and morph. As predicted, switching between morphs did hinder detection, and this effect was most pronounced when crabs had “disruptive” markings that were more effective at destroying the body outline. To our knowledge, this is the first evidence for variability in natural colour patterns hindering search image formation in predators, and as such presents a mechanism that facilitates phenotypic diversity in nature.

The effect of pelage, background, and distance on predator detection and the evolution of primate color vision.

Primates' predators, such as carnivore mammals, usually rely on camouflage to increase proximity to prey and start a predatory attempt. Camouflage depends not only on the color pattern presented by a predator's pelage but also on the background scene in which the hunting takes place. Another factor that influences camouflage effectiveness is prey's color vision since a given camouflage strategy might not work for all visual phenotypes. Still, little research has been made on the effect of primate visual phenotype on predator detection. Here, we investigate the effects of natural pelages, background scenarios, visual phenotypes, and detection distances on predator detection. We used photographs of taxidermized carnivores (ocelots, cougars, and lesser grisons) as detection stimuli, taken in three different natural scenarios (forest, savanna, and grassland), and at two viewing distances (near and far). On a touchscreen monitor, sets of four images (only one containing a hidden animal) were randomly presented to 39 human males (19 dichromats and 20 trichromats). We found that trichromats, when compared to dichromats, present a lower latency and a higher accuracy of carnivore detection for some conditions tested. We also found that pelage color, background scenario, and detection distance interact to influence the effectiveness of camouflage. Our results suggest that trichromacy might be even more advantageous for carnivore detection than thought before, since it facilitates detection of mammals with diverse pelage colorations, in environments with different phytophysiognomies, and at longer distances. We also propose that the higher rates of dichromacy found in modern human societies could have resulted from a relaxation in predation.

Prey colour biases of araneophagic mud-daubing wasps

While foraging, it is critical for a predator to detect and recognize its prey quickly in order to optimize its energy investment. In response, prey can use low-cost energy strategies such as crypsis and immobility that operate early in the detection–attack sequence. Mesopredators, such as spiders, are themselves attacked by visually oriented predators such as mud-dauber wasps. However, it is not known which colour cues are used by wasps to detect and capture their spider prey or whether there are biases towards such cues. In this study, we evaluated the prey colour biases of two mud-dauber wasps ( Trypoxylon tridentatum and Trypoxylon bridwelli ) using full-spectrum digital photography and visual modelling. We compared the colour contrast of spiders that were preyed upon with that of the spiders in the surrounding habitat. We show that the spiders captured by the wasps had higher chromatic contrast with their typical backgrounds compared with other co-occurring spider species not found in Trypoxylon nests. Our results suggest that Trypoxylon wasps may exhibit colour biases and/or preferences when hunting their spider prey. Our study highlights the importance of considering the perceptual abilities and biases of predators when studying predator–prey interactions. • We evaluated mud-dauber wasps' colour biases for spider prey. • Araneophagic wasp species showed distinct preferences when foraging for spiders. • Spiders with higher colour contrast with the background were captured more often. • Wasps may use chromatic cues at different stages during detection and attack.

Effects of prey colour on bird predation: an experiment in Mediterranean woodlands

Prey detection and selection by birds can be influenced by prey coloration. Whereas certain colours can indicate to predators the unpalatability of prey (i.e. aposematism), other colours can render prey cryptic against the background. However, there are discrepancies in the response of birds to prey coloration reported in different studies. Such discrepancies can be the result of geographical or temporal (e.g. seasonal) differences between studies if birds in different regions respond differently to coloration or if responses vary seasonally due to changes in bird composition. Experimental studies aiming to understand bird responses to prey colour should consider the effect of geographical variation while accounting for seasonal as well as interannual variability. We investigated the effects of colour on attack rates by exposing plasticine caterpillars of different colours to bird communities in 13 Mediterranean forests in central Spain for a period from 17 weeks to 7 months. Overall, yellow and green dummy caterpillars suffered the lowest attack rates. We also observed a bimodal pattern of bird attack rates through time, with highest predation occurring in late winter and summer (June to September). Low attack rates on yellow dummies are probably a consequence of aposematism, while low attack rates on green dummies probably resulted from crypsis. Rapid decreases in attack rates over time are probably a result of avoidance learning, whereas the increase in attacks in summer could be explained by the increase in fledglings and migrant birds.

Size and unpredictable movement together affect the effectiveness of dynamic flash coloration

Many animals have colour patterns that appear to change dynamically when the animal moves. Experiments have suggested that such colour patterns, termed ‘dynamic flash’ coloration, can reduce predatory attacks by misrepresenting the prey's location. However, the conditions that make this coloration effective are not known. We here tested the influence of two factors, target size and unpredictable movement, on the efficacy of dynamic flash coloration. Both these factors have independently been shown to affect the predator's ability to attack a moving prey accurately, but whether they interact with prey coloration remains unclear. Using a virtual predation experiment with human participants, we found that the effectiveness of dynamic flash coloration, when compared to background-matching coloration, declined as the size of the target increased, but only when the target movement was linear (i.e. predictable). However, when the movement was unpredictable (i.e. when the target adopted a ‘protean’ motion), we found dynamic flash coloration to be effective in reducing the number and accuracy of attacks irrespective of target size. Under most conditions, the effectiveness of dynamic flash coloration did not differ from that of a uniform luminance-matched grey target. Our results suggest that the efficacy of dynamic flash coloration is limited by prey size, but animals can overcome this constraint by employing an unpredictable movement trajectory. The study also provides direct empirical evidence that protean antipredator behaviour influences the effectiveness of prey coloration that works in motion.

Spatial and temporal variation in prey color patterns for background matching across a continuous heterogeneous environment.

In heterogeneous habitats, camouflage via background matching can be challenging because visual characteristics can vary dramatically across small spatial scales. Additionally, temporal variation in signaling functions of coloration can affect crypsis, especially when animals use coloration seasonally for intraspecific signaling (e.g., mate selection). We currently have a poor understanding of how wild prey optimize background matching within continuously heterogeneous habitats, and whether this is affected by requirements of intraspecific signaling across biological seasons. Here, we quantified color patterns of a wild population of shore skink (Oligosoma smithi), a variably colored lizard endemic to New Zealand, to (a) investigate whether background matching varies across a vegetation gradient; (b) assess potential signaling functions of color; and (c) to determine whether there is a trade‐off between requirements for crypsis and intraspecific signaling in coloration across seasons. Although all pattern types occurred throughout the vegetation gradient, we found evidence for background matching in skinks across the vegetation gradient, where dorsal brightness and pattern complexity corresponded with the proportion of vegetation cover. There was also a significant disparity between ventral color (saturation) of juveniles and adults, and also between sexes, suggestive of sex recognition. However, there was little indication that color was condition‐dependent in adults. Despite some evidence for a potential role in signaling, crypsis did not greatly differ across seasons. Our study suggests that selection favors a mix of generalist and specialist background matching strategies across continuously heterogeneous habitats.

How do predators generalize warning signals in simple and complex prey communities? Insights from a videogame.

The persistence of distinct warning signals within and between sympatric mimetic communities is a puzzling evolutionary question because selection favours convergence of colour patterns among toxic species. Such convergence is partly shaped by predators' reaction to similar but not identical stimulus (i.e. generalization behaviour), and generalization by predators is likely to be shaped by the diversity of local prey. However, studying generalization behaviour is generally limited to simple variations of prey colour patterns. Here, we used a computer game played by humans as surrogate predators to investigate generalization behaviours in simple (4 morphs) and complex (10 morphs) communities of unprofitable (associated with a penalty) and profitable butterflies. Colour patterns used in the game are observed in the natural populations of unprofitable butterfly species such as Heliconius numata. Analyses of 449 game participants' behaviours show that players avoided unprofitable prey more readily in simple than in complex communities. However, generalization was observed only in players that faced complex communities, enhancing the protection of profitable prey that looked similar to at least one unprofitable morph. Additionally, similarity among unprofitable prey also reduced attack rates only in complex communities. These results are consistent with previous studies using avian predators but artificial colour patterns and suggest that mimicry is more likely to evolve in complex communities where increases in similarity are more likely to be advantageous.

High contrast yellow mosaic patterns are prey attractants for orb‐weaving spiders

Abstract Many animals improve their foraging success by producing signals that exploit the sensory biases of potential prey, but the specific properties that make these sensory traps effective remain unclear. We combine field experiments with phylogenetic comparative analyses to investigate the visual luring properties of different signal designs in web‐building spiders. Our field experiments used cardboard spider models to examine the effects of area of colour patches, colour and pattern on the foraging success of the colourful giant wood spider, Nephila pilipes. These experiments revealed that both the colour (yellow) and pattern (yellow and black mosaic) are essential for luring prey in a high ambient light environment. We subsequently used phylogenetic comparative analyses to demonstrate an evolutionary association between prey viewing environment and spider ventral signal among 63 species of orb‐weavers from 53 genera. Combined, our data show that (a) the colour of the bright body parts of orb‐weavers is essential for both diurnal and nocturnal prey attraction, whereas the pattern and area of colour patches are important for diurnal foraging and (b) the evolution of these visual lures is associated with the viewing environment, specifically ambient light intensity. We conclude that the effectiveness of colour luring might be a major driver of the convergent evolution of yellow mosaic patterns in phylogenetically divergent orb‐weavers. Our discoveries indicate that prey colour preferences and signal efficacy play a significant role in the evolution of visually mediated prey‐luring systems. A free Plain Language Summary can be found within the Supporting Information of this article.

Aposematic coloration of prey enhances memory retention in an agamid lizard

Toxic or noxious prey often signal their unpalatability through aposematic coloration, and the evolution of aposematism has become a model system in evolutionary behaviour. Aposematic colours are not only easily recognized by predators, but, for many predators, aposematism enhances learning and memory retention. In this study, we used a visually oriented, insectivorous agamid lizard, Diploderma swinhonis, to test whether aposematic coloration enhances lizards’ ability to detect and remember distasteful prey. We exposed lizards to quinine-flavoured crickets, Gryllus bimaculatus, that were dyed with colours generally regarded as aposematic (red) and nonaposematic (green). After a single exposure, lizards readily learned to reject both red and green crickets, but in subsequent trials they were more hesitant to attack red than green ones. However, the lizards remembered both types of prey for up to 60 days and showed a similarly high rate of generalizing that aversion from coloured to noncoloured crickets. Our results demonstrate that visually hunting lizards exhibit nuanced patterns of learning and memory in foraging tasks and make ideal subjects for experimental work on aposematism.

Opposite latitudinal patterns for bird and arthropod predation revealed in experiments with differently colored artificial prey.

The strength of biotic interactions is generally thought to increase toward the equator, but support for this hypothesis is contradictory. We explored whether predator attacks on artificial prey of eight different colors vary among climates and whether this variation affects the detection of latitudinal patterns in predation. Bird attack rates negatively correlated with model luminance in cold and temperate environments, but not in tropical environments. Bird predation on black and on white (extremes in luminance) models demonstrated different latitudinal patterns, presumably due to differences in prey conspicuousness between habitats with different light regimes. When attacks on models of all colors were combined, arthropod predation decreased, whereas bird predation increased with increasing latitude. We conclude that selection for prey coloration may vary geographically and according to predator identity, and that the importance of different predators may show contrasting patterns, thus weakening the overall latitudinal trend in top‐down control of herbivorous insects.

The role of male coloration and ornamentation in potential alternative mating strategies of the dimorphic jumping spider, Maevia inclemens

Polymorphism can arise across taxa due to various selection pressures and potentially lead to alternative mating or antipredator strategies. For male jumping spiders, sexual selection and predation risk are often intertwined when courting cannibalistic females and may be a driving factor in the polymorphism of the jumping spider, Maevia inclemens. The dimorphic males of M. inclemens differ dramatically in their complex courtship behavior and display traits that may function as alternative mating strategies to reduce female aggression and maximize mating success. We hypothesized that males of the “tufted” morph honestly communicate condition or body size to females with three conspicuous tufts of setae on their head and males of the “striped” morph reduce female aggression with coloration commonly found in aposematic animals (here, yellow-orange pedipalps and striped legs). We examined correlations between tuft length and symmetry and metrics of body size and condition in field-collected spiders and conducted prey color choice tests (with live color-manipulated prey) to determine if yellow-orange and striped prey are avoided. Tuft length was variable and correlated with male size (but not condition). All prey color types were attacked at equal rates, but spiders oriented to striped prey more often, suggesting that male stripes may attract female attention without increasing predation. This study provides insight into the potential functions of the different courtship and visual displays of M. inclemens males. Using jumping spiders to study polymorphism can provide new insight into how multiple morphs can evolve, as males use mating strategies not only to impress females but also avoid getting eaten by their potential mates.Significance statementUnderstanding the selection pressures that shape and maintain polymorphisms in natural populations is an active area of inquiry, yet most of what we know comes from a small handful of well-studied vertebrate taxa. The unique biology of jumping spiders and the fact that males have to avoid cannibalism during courtship, makes them well-suited to provide novel insights into the functions and maintenance of dimorphic male traits. The unusual male dimorphism of M. inclemens captured the attention of naturalists as early as the 1800s, yet we still do not understand why the two male morphs differ so dramatically in morphology and courtship behavior. Here, we propose and test a novel hypothesis that provides insight into the long-studied but still largely unexplained phenomenon of male dimorphism in this species.

Prey colour biases in jumping spiders (Habronattus brunneus) differ across populations

AbstractPredators often avoid aposematic prey as a result of aversions to particular prey signals (e.g., bright colours and noxious odours). These aversions may be flexible, that is, they can be reinforced or extinguished with experience. As such, we might expect populations to differ in their biases against certain prey characteristics (e.g., colour or pattern) depending on the prey available in the community. Here, we tested whether the jumping spider, Habronattus brunneus(Salticidae), exhibits colour biases against red prey using choice tests with novel (artificially coloured) prey, and then went on to examine how these biases differ across four geographically distinct focal populations. We then conducted preliminary field surveys at each of these four sites to explore differences in habitat type and prey availability. Overall, we found that field‐caught H. brunneusexhibited a bias against the colour red (compared with black) when tested with artificially coloured prey in the laboratory. However, the degree of colour bias varied among our four focal populations (with two populations exhibiting strong biases against red and two showing no colour biases). Preliminary habitat and prey surveys suggest that these populations also differed in both habitat structure (percentage of grass, leaf litter and bare ground) and prey availability across many taxa, suggesting that the spiders from each population may have been exposed to, and had experiences with, different potential prey. We discuss how prey availability may influence colour biases in predators, as well as how predator experience may shape the evolution of prey colour signals.