Being a bright snake: Testing aposematism and mimicry in a neotropical forest

Based on color patterns and behavioral similarities, venomous coral snake Micrurus corallinus (Elapidae) may act as a model for two polymorphic species, Erythrolamprus aesculapii (Dipsadidae) and Micrurus decoratus (Elapidae). Plasticine replicas were used to investigate the aposematism of these coloration patterns and whether these species may be part of mimetic complexes in two Atlantic Forest localities in Southeast Brazil. Coral replicas were more avoided when set upon a white background, evincing that the pattern may act aposematically in contrast with light substrates. Birds attacked all four patterns equally during the mimicry experiments. Birds of prey, known to be effective in predating snakes, are quite abundant in the study areas, which may have led to this lack of avoidance. Accordingly, they predated more adult-sized replicas, which could be more dangerous. Interestingly, opossum avoided the Micrurus corallinus and Erythrolamprus aesculapii replicas that resembled the model. This suggests that opportunistic predators, as the opossum may be important selective agents in mimicry complexes.     

Predation on snakes of Argentina: Effects of coloration and ring pattern on coral and false coral snakes

The occurrence of coral snake coloration among unrelated venomous and non‐venomous snake species has often been explained in terms of warning coloration and mimicry. In Argentina, no field tests have been conducted to confirm this mimetic association between one venomous coral species (Micrurus phyrrocryptus, Elapidae) and two non‐venomous snake species with a similar color pattern (Lystrophis pulcher and Oxyrhopus rhombifer, Colubridae). The aims of this work were to test for the possible aposematic or cryptic function of the ring pattern and coloration of coral snakes and false coral snakes from central Argentina, and to analyse whether the pattern is effective throughout the year. Predation on snakes was estimated by using non‐toxic plasticine replicas of ringed venomous and non‐venomous snakes and unbanded green snakes placed along transects in their natural habitat during the dry and rainy season. Ringed color pattern was attacked by predators despite the background color. One of the replica types was attacked more than expected during the dry season, suggesting that both shape and width of rings may influence the choice by predators. The reaction of predators towards replicas that mimic snake species with ringed patterns is independent of the geographical region, and we can conclude that mimicry characteristics are quite general when the true models are present in the area.     

Rapid evolution of mimicry following local model extinction

Batesian mimicry evolves when individuals of a palatable species gain the selective advantage of reduced predation because they resemble a toxic species that predators avoid. Here, we evaluated whether—and in which direction—Batesian mimicry has evolved in a natural population of mimics following extirpation of their model. We specifically asked whether the precision of coral snake mimicry has evolved among kingsnakes from a region where coral snakes recently (1960) went locally extinct. We found that these kingsnakes have evolved more precise mimicry; by contrast, no such change occurred in a sympatric non-mimetic species or in conspecifics from a region where coral snakes remain abundant. Presumably, more precise mimicry has continued to evolve after model extirpation, because relatively few predator generations have passed, and the fitness costs incurred by predators that mistook a deadly coral snake for a kingsnake were historically much greater than those incurred by predators that mistook a kingsnake for a coral snake. Indeed, these results are consistent with prior theoretical and empirical studies, which revealed that only the most precise mimics are favoured as their model becomes increasingly rare. Thus, highly noxious models can generate an ‘evolutionary momentum’ that drives the further evolution of more precise mimicry—even after models go extinct.     

Diverse Evidence for the Decline of an Adaptation in a Coral Snake Mimic

Losses of adaptations in response to changed selective pressures are evolutionarily important phenomena but relatively few empirical examples have been investigated in detail. To help fill this gap, we took advantage of a natural experiment in which coral snake mimics occur on two nearby tropical islands, one that has coral snake models (Trinidad) and one that lacks them (Tobago). On Tobago, an endemic coral snake mimic (Erythrolamprus ocellatus) exists but has a relatively poor resemblance to coral snakes. Quantitative image analysis of museum specimens confirmed that E. ocellatus is a poor mimic of coral snakes. To address questions related to the functional importance of this phenotype, we conducted a field experiment on both islands with snake replicas made of clay. These results clearly indicated a strong inter-island difference in predator attack rates where snake replicas that resembled coral snakes received protection in Trinidad but not in Tobago. Further, a molecular phylogenetic analysis of the ancestry of E. ocellatus revealed that this poor coral snake mimic is deeply nested in a clade of good coral snake mimics. These data suggest that the lack of coral snakes on Tobago altered the selective environment such that the coral snake mimicry adaptation was no longer advantageous. The failure to maintain this ancestral feature in allopatry provides a compelling example of how losses of complex adaptations can occur.     

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.     

The colouration of the venomous coral snakes (family Elapidae) and their mimics (families Aniliidae and Golubridae)

The bright coloured, highly venomous coral snakes, Leptomicrurus, Micrurus and Micruroides (family Elapidae) and a series of harmless or mildly toxic mimics form an important component of the snake fauna of the Americas. Coral snake patterns are defined as any dorsal pattern found in any species of venomous coral snake and/or any dorsal pattern containing a substantial amount of red, pink or orange distributed so as to resemble that of some species of venomous coral snake. The components of coral snake colouration are described and four principal dorsal patterns are recognized: unicolour, bicolour, tricolour and quadricolour. The tricolour patterns may be further clustered based on the number of black bands or rings separating the red ones as: monads, dyads, triads, tetrads or pentads. A detailed classification of all coral snake colour patterns is presented and each pattern is illustrated. The taxonomic distribution of these patterns is surveyed for mimics and the 56 species of highly venomous coral snakes. Among the latter, the most frequent encountered patterns are tricolour monads, tricolour triads and bicolour rings, in that order. No venomous coral snakes have a tricolour dyad, tricolour tetrad or quadricolour pattern. As many as 115 species of harmless or mildly toxic species, c. 18% of all American snakes, are regarded as coral snake mimics. The colouration and behavioural traits of venomous coral snakes combine to form a significant antipredator defence of an aposematic type. The mimics in turn receive protection from predators that innately or through learning avoid coral snake colour patterns. The precise resemblances in colouration between sympatric non-coral snakes and venomous coral snakes and the concordant geographic variation between the two strongly support this view. Batesian mimicry with the highly venomous coral snakes as the models and the other forms as the mimics is the favoured explanation for this situation. It is further concluded that a number of species in the genera Elaphe, Farancia, Nerodia and Thamnophis, although having red in their colouration, should not be included in the coral snake mimic guild.     

Predator cognition permits imperfect coral snake mimicry

Batesian mimicry is often imprecise. An underexplored explanation for imperfect mimicry is that predators might not be able to use all dimensions of prey phenotype to distinguish mimics from models and thus permit imperfect mimicry to persist. We conducted a field experiment to test whether or not predators can distinguish deadly coral snakes (Micrurus fulvius) from nonvenomous scarlet kingsnakes (Lampropeltis elapsoides). Although the two species closely resemble one another, the order of colored rings that encircle their bodies differs. Despite this imprecise mimicry, we found that L. elapsoides that match coral snakes in other respects are not under selection to match the ring order of their model. We suggest that L. elapsoides have evolved only those signals necessary to deceive predators. Generally, imperfect mimicry might suffice if it exploits limitations in predator cognitive abilities.     

High-model abundance may permit the gradual evolution of Batesian mimicry: an experimental test

In Batesian mimicry, a harmless species (the ‘mimic’) resembles a dangerous species (the ‘model’) and is thus protected from predators. It is often assumed that the mimetic phenotype evolves from a cryptic phenotype, but it is unclear how a population can transition through intermediate phenotypes; such intermediates may receive neither the benefits of crypsis nor mimicry. Here, we ask if selection against intermediates weakens with increasing model abundance. We also ask if mimicry has evolved from cryptic phenotypes in a mimetic clade. We first present an ancestral character-state reconstruction showing that mimicry of a coral snake (Micrurus fulvius) by the scarlet kingsnake (Lampropeltis elapsoides) evolved from a cryptic phenotype. We then evaluate predation rates on intermediate phenotypes relative to cryptic and mimetic phenotypes under conditions of both high- and low-model abundances. Our results indicate that where coral snakes are rare, intermediate phenotypes are attacked more often than cryptic and mimetic phenotypes, indicating the presence of an adaptive valley. However, where coral snakes are abundant, intermediate phenotypes are not attacked more frequently, resulting in an adaptive landscape without a valley. Thus, high-model abundance may facilitate the evolution of Batesian mimicry.     

Do aposematism and Batesian mimicry require bright colours? A test,using European viper markings.

Predator avoidance of noxious prey, aposematism and defensive mimicry are normally associated with bright, contrasting patterns and colours. However, noxious prey may be unable to evolve conspicuous coloration because of other selective constraints, such as the need to be inconspicuous to their own prey or to specialist predators. Many venomous snakes, particularly most vipers, display patterns that are apparently cryptic, but nevertheless highly characteristic, and appear to be mimicked by other, non-venomous snakes. However, predator avoidance of viper patterns has never been demonstrated experimentally. Here, the analysis of 813 avian attacks on 12,636 Plasticine snake models in the field shows that models bearing the characteristic zigzag band of the adder (Vipera berus) are attacked significantly less frequently than plain models. This suggests that predator avoidance of inconspicuously but characteristically patterned noxious prey is possible. Our findings emphasize the importance of mimicry in the ecological and morphological diversification of advanced snakes.     

Unlinked Mendelian inheritance of red and black pigmentation in snakes: Implications for Batesian mimicry

Identifying the genetic basis of mimetic signals is critical to understanding both the origin and dynamics of mimicry over time. For species not amenable to large laboratory breeding studies, widespread color polymorphism across natural populations offers a powerful way to assess the relative likelihood of different genetic systems given observed phenotypic frequencies. We classified color phenotype for 2175 ground snakes (Sonora semiannulata) across the continental United States to analyze morph ratios and test among competing hypotheses about the genetic architecture underlying red and black coloration in coral snake mimics. We found strong support for a two‐locus model under simple Mendelian inheritance, with red and black pigmentation being controlled by separate loci. We found no evidence of either linkage disequilibrium between loci or sex linkage. In contrast to Batesian mimicry systems such as butterflies in which all color signal components are linked into a single “supergene,” our results suggest that the mimetic signal in colubrid snakes can be disrupted through simple recombination and that color evolution is likely to involve discrete gains and losses of each signal component. Both outcomes are likely to contribute to the exponential increase in rates of color evolution seen in snake mimicry systems over insect systems.     

Mimicry on the edge: why do mimics vary in resemblance to their model in different parts of their geographical range?

Batesian mimics-benign species that predators avoid because they resemble a dangerous species-often vary geographically in resemblance to their model. Such geographical variation in mimic-model resemblance may reflect geographical variation in model abundance. Natural selection should favour even poor mimics where their model is common, but only good mimics where their model is rare. We tested these predictions in a snake-mimicry complex where the geographical range of the mimic extends beyond that of its model. Mimics on the edge of their model's range (where the model was rare) resembled the model more closely than did mimics in the centre of their model's range (where the model was common). When free-ranging natural predators on the edge of the model's range were given a choice of attacking replicas of good or poor mimics, they avoided only good mimics. By contrast, those in the centre of the model's range attacked good and poor mimics equally frequently. Generally, although poor mimics may persist in areas where their model is common, only the best mimics should occur in areas where their model is rare. Thus, counter-intuitively, the best mimics may occur on the edge of their model's range.     

The status of Pliocercus and Urotheca (Serpentes: Golubridae), with a review of included species of coral snake mimics

The generic name Urotheca Bibron, 1843 is revived for a group of Neotropical colubrid snakes diagnosed by a long, thickened but fragile tail and the presence of a specialized naked pocket on the asulcate surface of the hemipenial capitulum. Urotheca includes those species previously placed in the lateristriga group of the genus Rhadinaea and the coral snake mimics usually referred to the genus Pliocercus. The many names based upon the coral snake mimics are shown to represent two species at most: Urotheca elapoides, a bicolour (red and black) or tricolour (red, yellow and black) banded or ringed form found in Mexico and northern Central America and U. euryzona, which is usually bicolour (red, yellow or white and black) and ranges from Nicaragua to western Ecuador. Coloration in U. elapoides resembles closely that of sympatric species of venomous coral snakes. Local variation in coloration and a geographic trend in the colour of the light rings (usually red in the north, white to the south) in U. euryzona parallels similar colour variation in the sympatric venomous coral snake Micrurus mipartitus. These patterns of variation add strong support to the idea that the two species are mimics of the highly venomous coral snakes. Urotheca, including the non-mimetic species U. decipiens, U. fulmceps, U. guentheri, U. lateristriga, U. multilineata and U. pachyura, shares the characteristic of a very long and disproportionately thickened and fragile tail with the coral snake mimics of the distantly related genus Scapkiodontophis. Members of both genera have a very high proportion (about 50%) of the tails broken indicating a probable predator escape device. Breakage is intercentral, with a calcified cap developing over the tip of the distal surface of the new terminal vertebra unlike the situation in many lizards where there is an intracentral fracture septum and the tail is regenerated.     

Why don't small snakes bask? Juvenile broad‐headed snakes trade thermal benefits for safety

Previous studies have suggested that most small Australian elapid snakes are nocturnal and rarely bask in the open because of the risk of predation by diurnal predatory birds. Because the physiology and behaviour of reptiles is temperature dependent, staying in refuges by day can entail high thermoregulatory costs, particularly for juveniles that must grow rapidly to maximise their chances of survival. We investigated whether the risk of predation deters juveniles of the endangered broad-headed snake ( Hoplocephalus bungaroides ) from basking, and if so, whether there are thermal costs associated with refuge use. To estimate avian attack rates on snakes, we placed 900 plasticine snake replicas in sunny locations and underneath small stones on three sandstone plateaus for 72 h. At the same time we quantified the thermal benefits of basking vs refuge use. On sunny days, juveniles could maintain preferred body temperatures for 4.7 h by basking but only for 2.0 h if they remained inside refuges. Our predation experiment showed that basking has high costs for juvenile snakes. Predators attacked a significantly higher proportion of exposed models (13.3%) than models under rocks (1.6%). Birds were the major predators of exposed models (75% of attacks), and avian predation did not vary across the landscape. By trading heat for safety, juvenile H. bungaroides decreased the potential time period that they could maintain preferred body temperatures by 57%. Thermal costs of refuge use may therefore contribute to the slow growth and late maturation of this endangered species. Our results support the hypothesis that nocturnal activity in elapid snakes has evolved to minimise the risk of avian predation.     

Disruption or aposematism? Significance of dorsal zigzag pattern of European vipers

European vipers (genus Vipera) are venomous and often have a distinctive dorsal zigzag pattern. The zigzag pattern of vipers has been suggested to be an example of disruptive colouration which reduces the detectability of a snake. However, recent studies suggest that the patterns have an aposematic function, although those experiments did not exclude the possibility of disruptive colouration. We used plasticine replicas of snakes to examine whether the zigzag pattern of European vipers provides protection from avian predator attacks via disruptive or aposematic function, or if the zigzag pattern might simultaneously serve both antipredatory functions. Experiments were conducted in the Coto Doñana National Park southern Spain. In the experiment, predation pressure caused by birds was compared between zigzag pattern (patterns were painted with and without disruptive effect i.e. breaking body outline or not), classical disruptive colouration (non-randomly placed patterns that breaks body outline) and control markings (replicas with length wise stripes and models without painted pattern) on natural and controlled backgrounds. We found that zigzag patterned snake replicas suffered less predation than striped ones regardless of the background, providing further evidence that the zigzag pattern of European vipers functions as a warning signal against predators. However, we did not find evidence that the zigzag pattern involves a disruptive effect.     

Diversity of warning signal and social interaction influences the evolution of imperfect mimicry

Mimicry, the resemblance of one species by another, is a complex phenomenon where the mimic (Batesian mimicry) or the model and the mimic (Mullerian mimicry) gain an advantage from this phenotypic convergence. Despite the expectation that mimics should closely resemble their models, many mimetic species appear to be poor mimics. This is particularly apparent in some systems in which there are multiple available models. However, the influence of model pattern diversity on the evolution of mimetic systems remains poorly understood. We tested whether the number of model patterns a predator learns to associate with a negative consequence affects their willingness to try imperfect, novel patterns. We exposed week‐old chickens to coral snake (Micrurus) color patterns representative of three South American areas that differ in model pattern richness, and then tested their response to the putative imperfect mimetic pattern of a widespread species of harmless colubrid snake (Oxyrhopus rhombifer) in different social contexts. Our results indicate that chicks have a great hesitation to attack when individually exposed to high model pattern diversity and a greater hesitation to attack when exposed as a group to low model pattern diversity. Individuals with a fast growth trajectory (measured by morphological traits) were also less reluctant to attack. We suggest that the evolution of new patterns could be favored by social learning in areas of low pattern diversity, while individual learning can reduce predation pressure on recently evolved mimics in areas of high model diversity. Our results could aid the development of ecological predictions about the evolution of imperfect mimicry and mimicry in general.     

Perceived predation risk as a function of predator dietary cues in terrestrial salamanders

Prey often avoid predator chemical cues, and in aquatic systems, prey may even appraise predation risk via cues associated with the predator's diet. However, this relationship has not been shown for terrestrial predator-prey systems, where the proximity of predators and prey, and the intensity of predator chemical cues in the environment, may be less than in aquatic systems. In the laboratory, we tested behavioural responses (avoidance, habituation and activity) of terrestrial red-backed salamanders, Plethodon cinereus, to chemical cues from garter snakes, Thamnophis sirtalis, fed either red-backed salamanders or earthworms (Lumbricus spp.). We placed salamanders in arenas lined with paper towels pretreated with snake chemicals, and monitored salamander movements during 120 min. Salamanders avoided substrates preconditioned by earthworm-fed (avoidanceX+/-SE=91.1+/-2.5%, N=25) and salamander-fed (95.2+/-2.5%, N=25) snakes, when tested against untreated substrate (control). Salamanders avoided cues from salamander-fed snakes more strongly (75.2+/-5.5%, N=25) than earthworm-fed snakes when subjected to both treatments simultaneously, implying that salamanders were sensitive to predator diet. Salamanders tended to avoid snake substrate more strongly during the last 60 min of a trial, but activity patterns were similar between salamanders exposed exclusively to control substrate versus those subject to snake cues. In another experiment, salamanders failed to avoid cues from dead conspecifics, suggesting that the stronger avoidance of salamander-fed snakes in the previous experiment was not directly due to chemical cues emitted by predator-killed salamanders. Salamanders also did not discriminate between cues from a salamander-fed snake versus a salamander-fed snake that was recently switched (i.e. <14 days) to an earthworm diet. Our results imply that terrestrial salamanders are sensitive to perceived predation risk via by-products of predator diet, and that snake predators rather than dead salamanders may be largely responsible for the release of such chemicals. Copyright 1999 The Association for the Study of Animal Behaviour.     

The importance of pattern similarity between Müllerian mimics in predator avoidance learning

Müllerian mimicry, where unpalatable prey share common warning patterns, has long fascinated evolutionary biologists. It is commonly assumed that Müllerian mimics benefit by sharing the costs of predator education, thus reducing per capita mortality, although there has been no direct test of this assumption. Here, we specifically measure the selection pressure exerted by avian predators on unpalatable prey with different degrees of visual similarity in their warning patterns. Using wild-caught birds foraging on novel patterned prey in the laboratory, we unexpectedly found that pattern similarity did not increase the speed of avoidance learning, and even dissimilar mimics shared the education of naive predators. This was a consistent finding across two different densities of unpalatable prey, although mortalities were lower at the higher density as expected. Interestingly, the mortalities of Müllerian mimics were affected by pattern similarity in the predicted way by the end of our experiment, although the result was not quite significant. This suggests that the benefits to Müllerian mimics may emerge only later in the learning process, and that predator experience of the patterns may affect the degree to which pattern similarity is important. This highlights the need to measure the behaviour of real predators if we are to understand fully the evolution of mimicry systems.     

Similar yet different: differential response of a praying mantis to ant‐mimicking spiders

Batesian mimics typically dupe visual predators by resembling noxious or deadly model species. Ants are unpalatable and dangerous to many arthropod taxa, and are popular invertebrate models in mimicry studies. Ant mimicry by spiders, especially jumping spiders, has been studied and researchers have examined whether visual predators can distinguish between the ant model, spider mimic and spider non‐mimics. Tropical habitats harbour a diverse community of ants, their mimics and predators. In one such tripartite mimicry system, we investigated the response of an invertebrate visual predator, the ant‐mimicking praying mantis (Euantissa pulchra), to two related ant‐mimicking spider prey of the genus Myrmarachne, each closely mimicking its model ant species. We found that weaver ants (Oecophylla smaragdina) were much more aggressive than carpenter ants (Camponotus sericeus) towards the mantis. Additionally, mantids exhibited the same aversive response towards ants and their mimics. More importantly, mantids approached carpenter ant‐mimicking spiders significantly more than often that they approached weaver ant‐mimicking spiders. Thus, in this study, we show that an invertebrate predator, the praying mantis, can indeed discriminate between two closely related mimetic prey. The exact mechanism of the discrimination remains to be tested, but it is likely to depend on the level of mimetic accuracy by the spiders and on the aggressiveness of the ant model organism.     

Generalization of Mimics Imperfect in Colour Patterns: The Point of View of Wild Avian Predators

Current research of imperfect mimicry brings ambiguous results. Experiments simulating more natural conditions rather than laboratory experiments show lower willingness of avian predators to attack less perfect mimics. We decided to simulate a natural situation by testing responses of wild‐caught adult avian predators (Great tit – Parus major) to variously perfect mimics of the red firebug (Pyrrhocoris apterus), which were in previous studies shown to elicit avoidance in Great tits. Presented mimics were perfect in all traits (firebug with its own colour pattern), imperfect in colour pattern (firebug with modified colour pattern), perfect in colour pattern, but imperfect in other visual traits (cockroach with firebug colour pattern), and imperfect in colour pattern as well as in other visual traits (cockroach with modified colour patterns). Modification of the pattern focused on the rounded spots on firebug's hemielytra, which is a conspicuous trait within the pattern. The pattern modification had no influence on the number of birds attacking the prey; nevertheless, birds spent more time observing the cockroaches that displayed the perfect firebug colour pattern than in the case of any other prey. Moreover, firebugs that displayed the perfect firebug colour pattern were observed for the shortest time (equal to that of the model – unmodified firebug). Cockroaches were attacked more often than firebugs, which suggest that birds were able to use additional visual cues (shape of legs and antennae) in prey recognition. Given these result, we conclude that differences in morphological traits characteristic for used prey taxa (true bugs, cockroaches) seem to be more important in the prey's protection than its colour pattern.     

Prey from the eyes of predators: Color discriminability of aposematic and mimetic butterflies from an avian visual perspective

Predation exerts strong selection on mimetic butterfly wing color patterns, which also serve other functions such as sexual selection. Therefore, specific selection pressures may affect the sexes and signal components differentially. We tested three predictions about the evolution of mimetic resemblance by comparing wing coloration of aposematic butterflies and their Batesian mimics: (a) females gain greater mimetic advantage than males and therefore are better mimics, (b) due to intersexual genetic correlations, sexually monomorphic mimics are better mimics than female‐limited mimics, and (c) mimetic resemblance is better on the dorsal wing surface that is visible to predators in flight. Using a physiological model of avian color vision, we quantified mimetic resemblance from predators’ perspective, which showed that female butterflies were better mimics than males. Mimetic resemblance in female‐limited mimics was comparable to that in sexually monomorphic mimics, suggesting that intersexual genetic correlations did not constrain adaptive response to selection for female‐limited mimicry. Mimetic resemblance on the ventral wing surface was better than that on the dorsal wing surface, implying stronger natural and sexual selection on ventral and dorsal surfaces, respectively. These results suggest that mimetic resemblance in butterfly mimicry rings has evolved under various selective pressures acting in a sex‐ and wing surface‐specific manner.