Resembling a Viper: Implications of Mimicry for Conservation of the Endangered Smooth Snake

The phenomenon of Batesian mimicry, where a palatable animal gains protection against predation by resembling an unpalatable model, has been a core interest of evolutionary biologists for 150 years. An extensive range of studies has focused on revealing mechanistic aspects of mimicry (shared education and generalization of predators) and the evolutionary dynamics of mimicry systems (co‐operation vs. conflict) and revealed that protective mimicry is widespread and is important for individual fitness. However, according to our knowledge, there are no case studies where mimicry theories have been applied to conservation of mimetic species. Theoretically, mimicry affects, for example, frequency dependency of predator avoidance learning and human induced mortality. We examined the case of the protected, endangered, nonvenomous smooth snake (Coronella austriaca) that mimics the nonprotected venomous adder (Vipera berus), both of which occur in the Åland archipelago, Finland. To quantify the added predation risk on smooth snakes caused by the rarity of vipers, we calculated risk estimates from experimental data. Resemblance of vipers enhances survival of smooth snakes against bird predation because many predators avoid touching venomous vipers. Mimetic resemblance is however disadvantageous against human predators, who kill venomous vipers and accidentally kill endangered, protected smooth snakes. We found that the effective population size of the adders in Åland is very low relative to its smooth snake mimic (28.93 and 41.35, respectively).Because Batesian mimicry is advantageous for the mimic only if model species exist in sufficiently high numbers, it is likely that the conservation program for smooth snakes will fail if adders continue to be destroyed. Understanding the population consequences of mimetic species may be crucial to the success of endangered species conservation. We suggest that when a Batesian mimic requires protection, conservation planners should not ignore the model species (or co‐mimic in Mullerian mimicry rings) even if it is not itself endangered. Implications of mimicry for Conservation of the endangered smooth snake     

Female sex pheromone in immature insect males—a case of pre-emergence chemical mimicry?

Sexual selection by competition for mates is a formidable force that has led to extraordinary adaptations in males. Here we present results suggesting a novel case of pheromone mimicry in males of Lariophagus distinguendus, a parasitic wasp of beetle larvae that develop in stored grain. Females of L. distinguendus produce a pheromone even before they emerge from a grain. Males are attracted to the parasitised grain and wait for females to emerge. Males emerging later than others are under enormous selection pressure since females mate only once. We show evidence that developing males fool their earlier emerging competitors by mimicking the female pheromone. Males exposed to pupae of either sex exhibit typical courtship behaviour. Searching males are not only arrested by grains containing developing females but spend as much time on grains containing developing males. Hence, by distracting their competitors away from receptive females late males may increase their own chance to mate with these females. After emergence, males decompose the active compounds within 32 h probably to decrease molestation during their own search for mates. Chemical analyses of active pheromone extracts and bioassays using fractions demonstrate that the active compounds are among the cuticular hydrocarbons.     

The evolution of Müllerian mimicry

It is now 130 years since Fritz Müller proposed an evolutionary explanation for the close similarity of co-existing unpalatable prey species, a phenomenon now known as Müllerian mimicry. Müller's hypothesis was that unpalatable species evolve a similar appearance to reduce the mortality involved in training predators to avoid them, and he backed up his arguments with a mathematical model in which predators attack a fixed number (n) of each distinct unpalatable type in a given season before avoiding them. Here, I review what has since been discovered about Müllerian mimicry and consider in particular its relationship to other forms of mimicry. Müller's specific model of associative learning involving a "fixed n" in a given season has not been supported, and several experiments now suggest that two distinct unpalatable prey types may be just as easy to learn to avoid as one. Nevertheless, Müller's general insight that novel unpalatable forms have higher mortality than common unpalatable forms as a result of predation has been well supported by field experiments. From its inception, there has been a heated debate over the nature of the relationship between Müllerian co-mimics that differ in their level of defence. There is now a growing awareness that this relationship can be mediated by many factors, including synergistic effects between co-mimics that differ in their mode of defence, rates of generalisation among warning signals and concomitant changes in prey density as mimicry evolves. I highlight areas for future enquiry, including the possibility of Müllerian mimicry systems based on profitability rather than unprofitability and the co-evolution of defence.     

Why do Horsfield’s bronze-cuckoo <Emphasis Type="Italic">Chalcites basalis</Emphasis> eggs mimic those of their hosts?

The Horsfield’s bronze-cuckoo (Chalcites basalis) egg closely matches the appearance of its host fairy-wren (Malurus spp.) eggs. Mimicry of host eggs by cuckoos is usually attributed to coevolution between cuckoos and hosts, with host discrimination against odd-looking eggs selecting for ever better mimicry by cuckoos. However, this process cannot explain Horsfield’s bronze-cuckoo egg mimicry because fairy-wren hosts rarely reject odd-looking eggs from their nest. An alternative hypothesis is that cuckoos have evolved egg mimicry to disguise their eggs from other cuckoos. Female cuckoos remove one egg from the nest during parasitism and would potentially benefit by selectively removing any cuckoo egg that has already been laid in the nest because otherwise, their egg will be evicted by the first nestling cuckoo along with the host clutch. We used painted, non-mimetic eggs to test whether cuckoos selectively remove odd-looking eggs during parasitism. We found that they were no more likely to remove a non-mimetic egg from a superb fairy-wren Malurus cyaneus clutch than would be expected by chance. Thus, our study does not support the cuckoo egg replacement hypothesis to explain mimicry of host eggs by cuckoos.     

Evolutionary aspects of perfume collection in male euglossine bees (Hymenoptera) and of nest deception in bee-pollinated flowers

Summary A fascinating pollination system has been evolved between perfume producing flowers and perfume collecting male euglossine bees in the neotropics. Detailed investigations have contributed to an understanding of the interactions between euglossine males and flowers as a pollination system. The role which the collected perfume plays in the reproductive behaviour of euglossine bees is not fully understood. A favoured hypothesis suggests that the collected fragrances are used as precursors for male sex pheromones and thus serve to attract conspecific males or females. It is not known how perfume collection behaviour evolved. Here, an evolutionary approach presents a new hypothesis which suggests that the evolution of perfume collection in euglossine males is based upon pre-existing signals which were attractive to females and males. It is further suggested that, at the evolutionary outset, flowers mimicked nest sites to deceive nest-seeking euglossine bees. In addition, a comparative study was undertaken on the phenomena of nest-mimicking flowers in related bee families.     

Chemical defence in ladybird beetles (Coccinellidae). II. Amount of reflex fluid,the alkaloid adaline and individual variation in defence in 2-spot ladybirds (Adalia bipunctata)

Summary 2-spot ladybirds secrete alkaloid (adaline)-rich defence fluid (reflex blood) in response to predator attack. Reflex fluid was collected from individual ladybirds and weighed and the alkaloid content measured by GC. The amount of fluid produced built up rapidly following winter hibernation in animals feeding on aphids. The concentration of adaline in the fluid was highest in the first bleeding after winter hibernation. A large sample of beetles was reflex bled several times. Significant among beetle variation was found in the amount of fluid produced and the concentration of the reflex blood. The results are discussed in relation to the possibility that 2-spot ladybirds are Batesian mimics of 7-spot ladybirds and to the possible functions of adaline.     

Toxicity assays of ladybirds using natural predators

Nestling blue titsParus caeruleus L. were given diets containing homogenized ladybirds, to assess the effects of their chemical defences. The 2spot, 10spot and water ladybirds produced no apparent toxic effects when small numbers were given at regular intervals.The pine and kidney-spot ladybirds slightly inhibit growth and may be toxic to very young nestlings. The Water ladybird is extremely distasteful to this predator, despite its lack of toxicity. The results are discussed with reference to the proposed Müllerian and Batesian mimetic relationships between the ladybird species.     

Delayed plumage maturation in Lazuli buntings: tests of the female mimicry and status signalling hypotheses

The evolutionary importance of delayed plumage maturation (DPM) in passerines, the condition when more than 1 year is required to achieve adult-like coloration, remains highly contentious. Adaptive hypotheses propose that aggression from after 2nd-year (ASY) males or predation favors DPM in 2nd-year (SY) males, thereby increasing SY male survivorship or reproductive success. However, each hypothesis suggests a distinct selective mechanism explaining “how” this is accomplished. Alternatively, DPM may be a consequence of a nonadaptive molt constraint. We tested the female mimicry and status signalling hypotheses in territorial ASY male lazuli buntings (Passerinaamoena) using three sets of model presentation experiments. The female mimicry hypothesis proposes that dull SY male plumage deceptively mimics female plumage, and predicts that ASY males can not distinguish SY male from female plumage. The status signalling hypothesis proposes that dull SY male plumage honestly signals low competitive threat, and predicts that ASY males respond less aggressively to dull versus bright, ASY-like plumage. Contrary to the female mimicry hypothesis, ASY males distinguished between SY male and female plumage, as they were aggressive to SY male models exclusively and attempted to copulate with female models. Supporting the status signalling hypothesis, ASY males were significantly less aggressive to SY versus ASY male plumage. While DPM may result from a physiological constraint on bright SY male plumage, our results support the idea that dull plumage in an SY male's first breeding season may be maintained by selection to reduce aggression from ASY males, serving as a signal of competitive status. Received: 21 February 1997 / Accepted after revision: 16 June 1997     

Defensive chemistry of lycid beetles and of mimetic cerambycid beetles that feed on them

Summary.  Beetles of the family Lycidae have long been known to be chemically protected. We present evidence that North American species of the lycid genera Calopteron and Lycus are rejected by thrushes, wolf spiders, and orb-weaving spiders, and that they contain a systemic compound that could account, at least in part, for this unacceptability. This compound, a novel acetylenic acid that we named lycidic acid, proved actively deterrent in feeding tests with wolf spiders and coccinellid beetles. Species of Lycuscommonly figure as models of mimetic associations. Among their mimics are species of the cerambycid beetle genus Elytroleptus, remarkable because they prey upon the model lycids. We postulated that by doing so Elytroleptus might incorporate the lycidic acid from their prey for their own defense. However, judging from analytical data, the beetles practice no such sequestration, explaining why they remain relatively palatable (in tests with wolf spiders) even after having fed on lycids. Chemical analyses also showed the lycids to contain pyrazines, such as were already known from other Lycidae, potent odorants that could serve in an aposematic capacity to forestall predatory attacks. David Utterback: Deceased     

Population differences in predation on Batesian mimics in allopatry with their model: selection against mimics is strongest when they are common

Batesian mimicry evolves when a palatable species, the “mimic,” resembles a dangerous species, the “model,” because both receive protection from predation. Yet, this protection should break down where the model is absent, because predators in such areas would not be under selection to avoid the model. Here, we test this prediction in a coral snake mimicry complex. We exposed plasticine replicas of milk snakes that closely mimic coral snakes to natural predators to determine if good mimetic milk snakes are preferentially attacked in allopatry with their model. Moreover, we evaluated whether attack rates on these replicas varied among three different allopatric regions that differed in the type of mimic found locally (i.e., good mimic, poor mimic, or no mimic). When all three regions were considered together, mimics were not preferentially attacked. When regions were analyzed separately, however, attacks on mimics were significantly greater than randomness only where good mimics were found. These variable levels of predation on good mimics might reflect frequency-dependent (i.e., apostatic) predation. In allopatric regions where good mimics are present, predators might have learned or evolved preferences for conspicuous, palatable prey that they encounter frequently. By contrast, in allopatric regions where good mimics are absent, predators might not have learned or evolved preferences for novel phenotypes. Thus, when predation is frequency-dependent, as long as good mimics are rare, they might not experience elevated levels of predation in allopatry with their model as predicted by the Batesian mimicry hypothesis.