Predator perception and the interrelation between different forms of protective coloration

Animals possess a range of defensive markings to reduce the risk of predation, including warning colours, camouflage, eyespots and mimicry. These different strategies are frequently considered independently, and with little regard towards predator vision, even though they may be linked in various ways and can be fully understood only in terms of predator perception. For example, camouflage and warning coloration need not be mutually exclusive, and may frequently exploit similar features of visual perception. This paper outlines how different forms of protective markings can be understood from predator perception and illustrates how this is fundamental in determining the mechanisms underlying, and the interrelation between, different strategies. Suggestions are made for future work, and potential mechanisms discussed in relation to various forms of defensive coloration, including disruptive coloration, eyespots, dazzle markings, motion camouflage, aposematism and mimicry.     

Phenotypic variation in male guppies from natural inland populations: an additional test of Haskins' sexual selection/predation hypothesis

Synopsis In Venezuela, guppies,Poecilia reticulata, are found in a diversity of aquatic ecosystems fringing the western slope of the eastern Andes. These inland drainages are associated with large between-site variation in both physical and biotic environments. Numbers of potential guppy predators vary greatly between low diversity piedmont streams and high diversity llanos swamps. We analyze geographic variation in several phenotypic traits associated with conspicuousness of male guppies as an independent test of Haskins' (Haskins et al. 1961) hypothesis of natural balance between sexual selection (driving male conspicuousness) and predation (driving crypsis). Four sites were compared: a diverse llanos swamp (high predation), two Andean piedmont streams (intermediate and low predation), and a spring pool located south of Venezuela's Paría Peninsula (no aquatic predators). Because tropical wet and dry seasons are associated with varying degrees of environmental change at these sites, within-site seasonal samples provided an additional test of the role of selective predation on Male phenotypes. Phenotypic traits associated with both size and coloration supported the sexual selection/predation hypothesis. male guppies from the spring were generally more colorful than male guppies from inland drainages. Males from the diverse swamp site were smaller and less colorful than guppies from other sites. Males from the swamp population were smallest and least colorful during the early dry season, when diurnal aquatic piscivores were more diverse and abundant. Dominant spot pigments at each site were generally those that provided greatest contrast with the predominant environmental background color, lending further evidence that coloration patterns in male guppies enhance conspicuousness.     

Color variation in signal crayfish Pacifastacus leniusculus

External coloration in animals depends on the interaction of several different factors including the genetics and epigenetics processes that underlie the color expression,the mechanisms of color perception,and the general mechanisms controlling color evolution and function.Among all,camouflages from predators and conspicuousness are of particular interest because pose animal to choose between opposite adjustment in coloration.The external coloration of crustaceans is mainly due to the accumulation of carotenoids in the exoskeleton and the epidermal layer,and the trade-off between camouflage and communication had led to a variety of responses,involving signal partitioning,spectral sensibility,changing coloration,or signaling behavior.Here,we used digital images to explore intrapopulation variability of the external coloration of Pacifastacus leniusculus among body regions within an individual and between sexes.We found that 1)ventral coloration of claws are more saturated and brilliant than upper parts,2)males express a more saturated and brightness coloration than females,especially on the lower portion of claws,3)color intensity and brightness increases with size differently in different body regions,and 4)brightness is more variable in males than in females.All the above patterns support the hypothesis that color in this species could be the result of a compromise between camouflage from predators and conspicuousness for communication.The results of this study suggest that carotenoid might have something to do with intraspecific communication and perform more complex functions than that of a simple pigment.     

Evidence of selection for egg crypsis in conspicuous nests

ABSTRACT The value of egg coloration as crypsis, once accepted as a general principle, has recently been questioned because most experiments have failed to show that egg coloration deters predation. The nest‐crypsis hypothesis postulates that, among species that build conspicuous nests, selection for egg crypsis is relaxed or absent because visually searching predators detect nests prior to eggs. I tested the nest‐crypsis hypothesis using the large, relatively conspicuous nests of American Robins (Turdus migratorius), and eggs that differed markedly in color that were collected from the nests of Red‐winged Blackbirds (Agelaius phoeniceus), Brewer's Blackbirds (Euphagus cyanocephalus), and Yellow‐headed Blackbirds (Xanthocephalus xanthocephalus). Each nest (N= 22) received a clutch of each species during three sequential predation trials that were 16 d in duration. The order of clutch presentation was randomized for each nest. Survival trends for Brewer's and Yellow‐headed Blackbirds were similar, and higher than those for clutches of Red‐winged Blackbirds. By the end of trials, overall survival of the three clutch types was roughly equivalent. However, clutches of Red‐winged Blackbird eggs, the most conspicuous egg type to the human eye, were discovered sooner by predators. Because the experimental design controlled for effects of nest crypsis, nest location, and nest size, this difference in egg survival can be attributed to differences in egg pigmentation. Thus, my results support a role for egg coloration as camouflage in conspicuous nests.     

Evaluation of disruptive camouflage of avian cup‐nests

Parent birds employ various strategies to protect their offspring against nest predators. Two well‐researched anti‐nest‐predation strategies involve visual concealment of the nest by way of parental camouflage and egg camouflage. By contrast, camouflage of nest structures is relatively under‐researched, particularly in the case of cup‐nests in trees and bushes. We explored how birds camouflage cup‐nests in nature. Specifically, we tested Hansell’s hypothesis that birds use externally applied pale and white objects such as spider cocoons and lichens to achieve cup‐nest camouflage. To test Hansell’s hypothesis, three complementary experiments were performed: (1) an in situ nest predation experiment; (2) a photo‐based visual search experiment; and (3) contrast analyses using PAT‐GEOM software in IMAGEJ. White paper and chalk spots were used to mimic white objects used by birds in nature. Whereas predation rates in Experiment 1 were not affected by white spots, location rates in Experiment 2 were lower for natural nests with white spots than without white spots. Experiment 3 demonstrated that white spots significantly increased the contrast between different visual elements of nests. It was concluded that white objects can potentially camouflage nests against some nest predators, and that any improved camouflage was probably achieved via disruptive camouflage.     

Investigating Müllerian mimicry: predator learning and variation in prey defences

Inexperienced predators are assumed to select for similarity of warning signals in aposematic species (Müllerian mimicry) when learning to avoid them. Recent theoretical work predicts that if co-mimic species have unequal defences, predators attack them according to their average unpalatability and mimicry may not be beneficial for the better defended co-mimic. In this study, we tested in a laboratory environment whether a uniform warning signal is superior to a variable one in promoting predator learning, and simultaneously whether co-mimics are preyed upon according to their average unpalatability. There was an interaction of signal variation and unpalatability but inexperienced birds did not select for signal similarity in artificial prey; when the prey was moderately defended a variable signal was even learnt faster than a uniform one. Due to slow avoidance learning, moderately defended prey had higher mortality than highly defended prey (although this was not straightforward), but mixing high and moderate unpalatability did not increase predation compared with high unpalatability. This does not support the view that predators are sensitive to varying unpalatability. The results suggest that inexperienced predators may neither strongly select for accurate Müllerian mimicry nor affect the benefits of mimicry when the co-mimics are unequally defended.     

Pupal warning color development in above-ground pupating species but cryptic color in ground-surface pupating species of the nine-spotted diurnal moths (Erebidae: Arctiinae: Syntomini)

Insects usually have cryptic colors to avoid detection by visually hunting predators. However, if the insects acquire toxic or repellent substances against predators, some of them develop conspicuous coloration to exhibit their unpalatability. Such warning colors allow insects to survive. In the nine-spotted diurnal moths (Erebidae: Arctiinae: Syntomini), we found the above-ground pupating species to have conspicuous colored pupae, but the ground-surface pupating species to have cryptic colored pupae. In this study, the relationships between unpalatability and coloration of these pupae are examined among three species of Amata and one species of Syntomoides. Pupae of the two species (A. germana and A. flava) are conspicuous in their color pattern with seven black dotted lines longitudinally on their pale-yellow bodies. These pupae are exposed to the aerial predators in a coarse silk mesh hanging from leaves and/or branches. The other two species (A. fortunei and S. imaon) pupate in spaces under stones, fallen twigs and leaves on the ground surface, and the pupae in a coarse silk cocoon is cryptic dark brown. Their pupation site selections are reproduced in the rearing glass vessels. Palatability assessment using lizards as a potential predator suggests that pupae of A. germana, A. flava and A. fortunei are unpalatable and the lizard's feeding response decreases with experience. However, pupae of S. imaon are all eaten (palatable). Finally, the possible evolutionary scenario of pupal colors of these four species is discussed in relation to pupation site selection and palatability.     

Alternative camouflage strategies mediate predation risk among closely related co-occurring kelp crabs

Although camouflage is a common predator defense strategy across a wide variety of organisms, direct tests of the adaptive and ecological consequences of camouflage are rare. In this study, we demonstrated that closely related crabs in the family Epialtidae coexist in the same algal environment but use alternative forms of camouflage––decoration and color change––to protect themselves from predation. Decoration and color change are both plastic camouflage strategies in that they can be changed to match different habitats: decoration occurs on a short timescale (hours to days), while color change accompanies molting and occurs on longer timescales (months). We found that the species that decorated the most had the lowest magnitude of color change (Pugettia richii); the species that decorated the least showed the highest magnitude of color change (Pugettia producta), and a third species (Mimulus foliatus) was intermediate in both decoration and color change, suggesting a negative correlation in utilization of these strategies. This negative correlation between color change and decoration camouflage utilization mirrored the effectiveness of these camouflage strategies in reducing predation in different species. Color camouflage primarily reduced predation on P. producta, while decoration camouflage (but not color camouflage) reduced predation on P. richii. These results indicate there might be among-species trade-offs in utilization and/or effectiveness of these two forms of plastic camouflage, with important consequences for distribution of these species among habitats and the evolution of different camouflage strategies in this group.     

Wing coloration and reflectance in Morpho butterflies as related to reproductive behavior and escape from avian predators

Summary Different species of large tropical butterflies belonging to the genus Morpho vary dramatically in both the amount of blue color on their wings and the associated irridescence (reflectance). This paper discusses how such a morphological properties may be related to both courtship behavior and effective means of reducing predation (especially by birds) in the low density adult populations. Essentially, the hypothesis is advanced that territorial species of Morpho can afford to possess very conspicuous wing coloration that may facilitate courtship interactions, in addition to spacing the territorial male population over the suitable habitat. While territoriality may be favored by natural selection, such behavior can only evolve if the species involved possess effective means of reducing predation, because territoriality in morphos is an extremely predictable form of behavior, toward which predators can easily orient. Two alternate hypotheses are advanced to account for low predation in a territorial morpho, Morpho amathonte, a species in which males are very bright and showy. The first hypothesis, which is more consistent with traditional ideas on the function of bright colors in morpho wings, maintains that predators learn quickly to avoid these butterflies as prey, since they are very difficult to catch. The second hypothesis, suggests that conspicuous territorial male morphos actually employ pursuit-stimuli to invite birds to attack and be subsequently unsuccessful.     

Predation of eggs ofSitona hispidulus [Col.: Curculionidae] in alfalfa

The predation on egg populations ofSitona hispidus (Fabricius) [Col.: Curculionidae] in a stand of alfalfa was evaluated in 1982 and 1983. By using pitfall traps, catches of reproductive adults ofS. hispidulus were correlated with catches of carabid species, and potential egg predators were identified for further evaluation. Results indicated that predators removed 28 % of eggs under field conditions.Amara aenea DeGeer was found to be particularly efficient on eggs ofS. hispidulus under caged-field conditions.      

Significance of butterfly eyespots as an anti-predator device in ground-based and aerial attacks

Many butterfly genera are characterised by the presence of marginal eyespots on their wings. One hypothesis to account for an occurrence of eyespots is that these wing pattern elements are partly the outcome of visual selection by predators. Bicyclus anynana (Satyrinae) has underside spotting on its wings but there is also a seasonal form in which the eyespots are reduced in size or totally absent. This natural variation gives us a useful tool to test the hypothesis that marginal eyespot patterns can decoy the attacking predator by, at least sometimes, diverting attack from vital body parts to the edges of the wings. We used lizards, Anolis carolinensis , and pied flycatchers, Ficedula hypoleuca , as predators for living spotted and spotless B. anynana . The presence of eyespots did not increase the escape probability of resting butterflies once captured (even a form with enlarged eyespots did not add to effective deflection of attacks). There was also no evidence that eyespots influenced the location of strikes by the predators. This study thus provides no support that marginal eyespot patterns can act as an effective deflection mechanism to avoid lizard or avian predation.     

Coral snake mimicry: live snakes not avoided by a mammalian predator

The occurrence of coral snake coloration among unrelated venomous and non-venomous New World snake species has often been explained in terms of warning coloration and mimicry. The idea that snake predators would avoid coral snakes in nature seems widely established and is postulated in many discussions on coral snake mimicry. However, the few workers that have tested a potential aposematic function of the conspicuous colour pattern focused exclusively on behaviour of snake predators towards coloured abstract models. Here we report on behaviour of temporarily caged, wild coatis (Nasua narica) when confronted with co-occurring live snakes, among which were two species of venomous coral snakes. Five different types of responses have been observed, ranging from avoidance to predation, yet none of the coatis avoided either of the two coral snake species or other species resembling these. As in earlier studies coatis appeared to avoid coral snake models, our findings show that results from studies with abstract snake models cannot unconditionally serve as evidence for an aposematic function of coral snake coloration.     

Predation,thermoregulation, and wing color in pierid butterflies

Summary This paper explores two hypotheses about the relationships among predation, thermoregulation, and wing color in butterflies: First, that butterflies are susceptible to predation during thermally marginal periods (e.g., cool weather) when effective thermoregulation and flight are not possible; second, that Pieris butterflies are relatively unpalatable to visual predators, supporting the idea that the white wing pigment of Pieris represents aposematic coloration. Field experiments with Pieris and Colias in 1984 and 1985 demonstrate that substantial predation may occur during the morning period before butterflies are able to actively fly. Circumstantial evidence is presented to suggest that at least some of the predation is by small, cursorial mammals. Feeding experiments in the field using Grey Jays as predators indicate that Pieris napi and P. occidentalis are less palatable than other sympatric butterflies, including confamial Colias alexandra. These and previous results suggest that Pieris are edible but less preferred as prey by birds, and that the degree of palatibility may vary among Pieris species. The relatively low palatability of these Pieris is consistent with the hypothesis that their white pigmentation represents aposematic coloration; however, the cues by which potential bird predators might discriminate against Pieris have not been established.     

Batesian mimics influence the evolution of conspicuousness in an aposematic salamander

Conspicuousness, or having high contrast relative to the surrounding background, is a common feature of unpalatable species. Several hypotheses have been proposed to explain the occurrence of conspicuousness, and while most involve the role of conspicuousness as a direct signal of unpalatability to potential predators, one hypothesis suggests that exaggerated conspicuousness may evolve in unpalatable species to reduce predator confusion with palatable species (potential Batesian mimics). This hypothesis of antagonistic coevolution between palatable and unpalatable species hinges on the ‘cost of conspicuousness’, in which conspicuousness increases the likelihood of predation more in palatable species than in unpalatable species. Under this mimicry scenario, four patterns are expected: (i) mimics will more closely resemble local models than models from other localities, (ii) there will be a positive relationship between mimic and model conspicuousness, (iii) models will be more conspicuous in the presence of mimics, and (iv) when models and mimics differ in conspicuousness, mimics will be less conspicuous than models. We tested these predictions in the salamander mimicry system involving Notophthalmus viridescens (model) and one colour morph of Plethodon cinereus (mimic). All predictions were supported, indicating that selection for Batesian mimicry not only influences the evolution of mimics, but also the evolution of the models they resemble. These findings indicate that mimicry plays a large role in the evolution of model warning signals, particularly influencing the evolution of conspicuousness.     

Conspicuous male coloration impairs survival against avian predators in Aegean wall lizards,Podarcis erhardii

Animal coloration is strikingly diverse in nature. Within‐species color variation can arise through local adaptation for camouflage, sexual dimorphism and conspicuous sexual signals, which often have conflicting effects on survival. Here, we tested whether color variation between two island populations of Aegean wall lizards (Podarcis erhardii) is due to sexual dimorphism and differential survival of individuals varying in appearance. On both islands, we measured attack rates by wild avian predators on clay models matching the coloration of real male and female P. erhardii from each island population, modeled to avian predator vision. Avian predator attack rates differed among model treatments, although only on one island. Male‐colored models, which were more conspicuous against their experimental backgrounds to avian predators, were accordingly detected and attacked more frequently by birds than less conspicuous female‐colored models. This suggests that female coloration has evolved primarily under selection for camouflage, whereas sexually competing males exhibit costly conspicuous coloration. Unexpectedly, there was no difference in avian attack frequency between local and non‐local model types. This may have arisen if the models did not resemble lizard coloration with sufficient precision, or if real lizards behaviorally choose backgrounds that improve camouflage. Overall, these results show that sexually dimorphic coloration can affect the risk of predator attacks, indicating that color variation within a species can be caused by interactions between natural and sexual selection. However, more work is needed to determine how these findings depend on the island environment that each population inhabits.     

Are European White Butterflies Aposematic?

It has been suggested that the white coloration of Pieridae butterflies is a warning signal and therefore all white Pieridae could profit from a mimetic resemblance. We tested whether green-veined white (Pieris napi) and orange-tip (Anthocharis cardamines) butterflies benefit from white coloration. We compared their relative acceptability to wild, adult pied flycatchers (Ficedula hypoleuca) by offering live A. cardamines and P. napi together with two non-aposematic butterflies on the tray attached to birds' nesting boxes. Experienced predators equally attacked white and non-white butterflies, and the order of attack among the Pieridae was random. If anything, there was a slight indication that the female A. cardamines was the least favoured prey. Since birds did not avoid white coloration, we compared the palatability of these two species against known palatable and unpalatable butterflies by presenting them to great tits (Parus major). Pieris brassicae, which has been earlier described as unpalatable, was also included in the palatability test. However, there were no significant differences in the palatability of the butterflies to birds, and even P. brassicae was apparently palatable to the great tits. Our results do not unambiguously support the hypothesis that the white coloration of Pieridae would signal unpalatability. Nevertheless, in our last experiment, pied flycatchers often rejected or left untouched free flying P. napi and A. cardamines. This suggests that other features in a more natural situation, such as the agile flight pattern or odours might still make them unprofitable to birds. This revised version was published online in July 2006 with corrections to the Cover Date.     

Reduced predation risk for melanistic pygmy grasshoppers in post‐fire environments

The existence of melanistic (black) color forms in many species represents interesting model systems that have played important roles for our understanding of selective processes, evolution of adaptations, and the maintenance of variation. A recent study reported on rapid evolutionary shifts in frequencies of the melanistic forms in replicated populations of Tetrix subulata pygmy grasshoppers; the incidence of the melanistic form was higher in recently burned areas with backgrounds blackened by fire than in nonburned areas, and it declined over time in postfire environments. Here, we tested the hypothesis that the frequency shifts of the black color variant were driven, at least in part, by changes in the selective regime imposed by visual predators. To study detectability of the melanistic form, we presented human “predators” with images of black grasshoppers and samples of the natural habitat on computer screens. We demonstrate that the protective value of black coloration differs between burnt and nonburnt environments and gradually increases in habitats that have been more blackened by fire. These findings support the notion that a black color pattern provides improved protection from visually oriented predators against blackened backgrounds and implicate camouflage and predation as important drivers of fire melanism in pygmy grasshoppers.     

Predatory behaviour ofScatophaga stercoraria under laboratory conditions

Laboratory experiments tested the effectiveness ofScatophaga stercoraria (L.) as a predator of various insect species. Photophases, ages and gender of predators and effects of dung presence on predation rates were compared for either sex using counts of prey cadavers, behavioral observations and oviposition rates. Males consistently killed more prey than females, but longer photophases did not significantly increase daily predation rates. Nine to 10-day-old flies approaching sexual maturity achieved highest predation rates. Dung was found to affect predatory behaviour but not cumulative predation. Predatory behaviour of sexually mature males was more affected than female behaviour by the presence of dung, whereas sexually immatures flies showed no response to dung presence. Preconditioning ofS. stercoraria adults using 3 prey species of different sizes did not affect the prey chosen in subsequent random choice experiments. Larger prey species such asMusca domestica (L.) orDelia antiqua (Meigen) were preferred toDrosophila sp. by both sexes ofS. stercoraria. This species may be a useful predator for future integrated pest management techniques in vegetable crops or control of house flies in barns.      

Not all colors are equal: predation and color polytypism in the aposematic poison frog Oophaga pumilio

Aposematic organisms are not predicted to show high levels of warning signal diversity because they are expected to be under stabilizing selection to decrease costs of ‘educating’ predators about their unpalatability. However, systematic changes in warning signals (polytypism) can be expected if they represent adaptations to local predators. The aposematic strawberry poison frog (Oophaga pumilio) is red throughout its mainland distribution in Costa Rica and Panamá, but displays high levels of warning signal diversity in the Bocas del Toro Archipelago of Panamá. Both coloration and spot pattern vary in a polytypic sense. Sexual selection contributes to maintaining the polytypism, but little work has investigated the potential influence of predation. We used unspotted models of O. pumilio to determine if predation might help explain the color polytypism on Isla Colón in the Bocas del Toro Archipelago of Panamá. We tested whether attack rates differed among the red mainland morph, green/yellow Isla Colón morph, and the brown control. We found that frog color significantly predicted being attacked. The local green Isla Colón models were attacked more than foreign red or brown models. No difference in attack rate existed between red and brown control models. Our results suggest that the red mainland morph possesses a more effective warning signal, even when it is not the local morph. Honest signaling of unpalatability, neophobia, and the use of search images by local predators are potential explanations. Similarity of the brown model to other local poison frogs might explain the lower attack rate compared to previous work. The attack rate was lower on Isla Colón compared to mainland Costa Rica, which supports the hypothesis that less overall predation in the Bocas del Toro Archipelago may contribute to the overall warning signal diversity in O. pumilio there by relaxing selection for aposematic traits.     

Spots and stripes: ecology and colour pattern evolution in butterflyfishes

The incredible diversity of colour patterns in coral reef fishes has intrigued biologists for centuries. Yet, despite the many proposed explanations for this diversity in coloration, definitive tests of the role of ecological factors in shaping the evolution of particular colour pattern traits are absent. Patterns such as spots and eyespots (spots surrounded by concentric rings of contrasting colour) have often been assumed to function for predator defence by mimicking predators'' enemies'' eyes, deflecting attacks or intimidating predators, but the evolutionary processes underlying these functions have never been addressed. Striped body patterns have been suggested to serve for both social communication and predator defence, but the impact of ecological constraints remains unclear. We conducted the first comparative analysis of colour pattern diversity in butterflyfishes (Family: Chaetodontidae), fishes with conspicuous spots, eyespots and wide variation in coloration. Using a dated molecular phylogeny of 95 species (approx. 75% of the family), we tested whether spots and eyespots have evolved characteristics that are consistent with their proposed defensive function and whether the presence of spots and body stripes is linked with species'' body length, dietary complexity, habitat diversity or social behaviour. Contrary to our expectations, spots and eyespots appeared relatively recently in butterflyfish evolution and are highly evolutionarily labile, suggesting that they are unlikely to have played an important part in the evolutionary history of the group. Striped body patterns showed correlated evolution with a number of ecological factors including habitat type, sociality and dietary complexity. Our findings question the prevailing view that eyespots are an evolutionary response to predation pressure, providing a valuable counter example to the role of these markings as revealed in other taxa.