Biogeography,ecology and conservation of Erebia oeme (Hübner) in the Carpathians (Lepidoptera: Nymphalidae: Satyrinae)

The European endemic Erebia oeme (Hübner [1804]) (Lepidoptera: Nymphalidae: Satyrinae) is discovered in the Carpathian Chain, from where it was considered to be absent. The single population found is situated in the southern part of the Romanian Carpathians (Retezat Mountains), where it flies sympatrically and synchronically with Erebia medusa ([Denis & Schiffermüller] 1775). The similar external morphology of these two species probably caused E. oeme to be overlooked in the Carpathians, leading to an unexpected information gap in the otherwise thoroughly studied European continent. The morphology of the Romanian specimens is compared to populations from the rest of the species’ range and to E. medusa. In addition, we tested DNA barcoding as a method to discriminate between these species and confirmed that it represents an effective identification tool for the taxa involved. The habitat of E. oeme, adults of both sexes and their genitalia are illustrated in comparison with E. medusa. Based on the study of several collections, we show that E. oeme is likely to be extremely local in the Carpathians and provide arguments to consider the species as vulnerable in Romania.     

Bird attacks on a butterfly with marginal eyespots and the role of prey concealment against the background

Small eyespots on butterflies have long been thought to deflect attacks, and birds are the presumptive drivers selecting for these patterns; however, evidence of this function is still ambiguous. Marginal eyespots typically consist of a UV‐reflective white pupil, surrounded by one black and one yellowish ring. We have recently shown that Cyanistes caeruleus (blue tits) attack such eyespots, but only under low light intensities with accentuated UV levels: the increased salience of the eyespots relative to the rest of the butterfly probably explains this result. Possibly the background against which the butterfly is concealed may deceive birds to make similar errors. We therefore presented speckled wood butterflies decorated with eyespots (or controls without eyespots) to C. caeruleus against two backgrounds: oak and birch bark. Our results show that: (1) eyespots, independent of background, were effective in deflecting attacks; (2) the time elapsed between a bird landing and the attack was interactively dependent on the background and whether the butterfly bore an eyespot; and (3) the speed at which a butterfly was attacked predicted the outcome, with faster birds being more prone to errors than slower birds. This underscores a speed–accuracy trade‐off in the predators, and that background plays a role in the defensive qualities of marginal eyespots. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 290–297.     

STEPWISE EVOLUTION OF RESISTANCE TO TOXIC CARDENOLIDES VIA GENETIC SUBSTITUTIONS IN THE NA+/K+‐ATPASE OF MILKWEED BUTTERFLIES (LEPIDOPTERA: DANAINI)

Despite the monarch butterfly (Danaus plexippus) being famous for its adaptations to the defensive traits of its milkweed host plants, little is known about the macroevolution of these traits. Unlike most other animal species, monarchs are largely insensitive to cardenolides, because their target site, the sodium pump (Na⁺/K⁺‐ATPase), has evolved amino acid substitutions that reduce cardenolide binding (so‐called target site insensitivity, TSI). Because many, but not all, species of milkweed butterflies (Danaini) are associated with cardenolide‐containing host plants, we analyzed 16 species, representing all phylogenetic lineages of milkweed butterflies, for the occurrence of TSI by sequence analyses of the Na⁺/K⁺‐ATPase gene and by enzymatic assays with extracted Na⁺/K⁺‐ATPase. Here we report that sensitivity to cardenolides was reduced in a stepwise manner during the macroevolution of milkweed butterflies. Strikingly, not all Danaini typically consuming cardenolides showed TSI, but rather TSI was more strongly associated with sequestration of toxic cardenolides. Thus, the interplay between bottom‐up selection by plant compounds and top‐down selection by natural enemies can explain the evolutionary sequence of adaptations to these toxins.     

Testing of divergent patterns of butterfly niche breadth in a peninsula

The butterfly fauna on the Korean peninsula are comprised of both the Palearctic and Oriental species. We hypothesized that the Oriental species (immigrated across the sea) tend to have a wider niche breadth compared with the Palearctic species (immigrated from the continent) since the former migrates long distances across the sea and has to adapt to new environments. We tested this hypothesis using Korean butterfly data on distribution, habitat, food and life history traits. The distribution and ecological traits such as habitat breadth, overwintering stage, and voltinism of the Oriental species were found to be significantly different from the Palearctic species. However, the diet breadth and food plant type were not different. These results partly confirm the peninsula niche breadth hypothesis, which predicted that Oriental species have a broader niche breadth than Palearctic species.     

Simulating effects of climate change under direct and diapause development in a butterfly

Temperature is one of the most important ecological factors affecting species survival and distributions. Therefore, global climate change, involving increases in mean surface temperature and the occurrence of extreme weather events, may pose a substantial challenge to biodiversity. Whereas tropical ectotherms are believed to be very sensitive to climate change, temperate‐zone species may actually benefit from higher temperatures. However, as in temperate zones large parts of the year are unsuitable for growth and reproduction, seasonal time constraints may complicate matters. Against this background we here investigate the impact of simulated climate change, involving increased mean temperatures and heat waves, across developmental pathways of the butterfly Lycaena tityrus (Poda) (Lepidoptera: Lycaenidae). Increased temperatures speeded up development but decreased pupal mass as expected. However, we found no evidence for detrimental effects of increased temperatures or even simulated heat waves. Furthermore, patterns did not differ between indirectly and directly developing individuals, which are assumed to be more time constrained. Our findings support the notion that not all species will be detrimentally affected by climate change, and suggest that species attributes may be more important than potential time constraints imposed by different developmental pathways.     

Floral specialization for different pollinators and divergent use of the same pollinator among co‐occurring Impatiens species (Balsaminaceae) from Southeast Asia

Floral variation among closely related species is thought to often reflect differences in pollination systems. Flowers of the large genus Impatiens are characterized by extensive variation in colour, shape and size and in anther and stigma positioning, but studies of their pollination ecology are scarce and most lack a comparative context. Consequently, the function of floral diversity in Impatiens remains enigmatic. This study documents floral variation and pollination of seven co‐occurring Impatiens spp. in the Southeast Asian diversity hotspot. To assess whether floral trait variation reflects specialization for different pollination systems, we tested whether species depend on pollinators for reproduction, identified animals that visit flowers, determined whether these visitors play a role in pollination and quantified and compared key floral traits, including floral dimensions and nectar characteristics. Experimental exclusion of insects decreased fruit and seed set significantly for all species except I. muscicola, which also received almost no visits from animals. Most species received visits from several animals, including bees, birds, butterflies and hawkmoths, only a subset of which were effective pollinators. Impatiens psittacina, I. kerriae, I. racemosa and I. daraneenae were pollinated by bees, primarily Bombus haemorrhoidalis. Impatiens chiangdaoensis and I. santisukii had bimodal pollination systems which combined bee and lepidopteran pollination. Floral traits differed significantly among species with different pollination systems. Autogamous flowers were small and spurless, and did not produce nectar; bee‐pollinated flowers had short spurs and large floral chambers with a wide entrance; and bimodally bee‐ and lepidopteran‐pollinated species had long spurs and a small floral chamber with a narrow entrance. Nectar‐producing species with different pollination systems did not differ in nectar volume and sugar concentration. Despite the high frequency of bee pollination in co‐occurring species, individuals with a morphology suggestive of hybrid origin were rare. Variation in floral architecture, including various forms of corolla asymmetry, facilitates distinct, species‐specific pollen‐placement on visiting bees. Our results show that floral morphological diversity among Impatiens spp. is associated with both differences in functional pollinator groups and divergent use of the same pollinator. Non‐homologous mechanisms of floral asymmetry are consistent with repeated independent evolution, suggesting that competitive interactions among species with the same pollination system have been an important driver of floral variation among Impatiens spp.     

Tolerance to deer herbivory and resistance to insect herbivores in the common evening primrose (Oenothera biennis)

The evolution of plant defence in response to herbivory will depend on the fitness effects of damage, availability of genetic variation and potential ecological and genetic constraints on defence. Here, we examine the potential for evolution of tolerance to deer herbivory in Oenothera biennis while simultaneously considering resistance to natural insect herbivores. We examined (i) the effects of deer damage on fitness, (ii) the presence of genetic variation in tolerance and resistance, (iii) selection on tolerance, (iv) genetic correlations with resistance that could constrain evolution of tolerance and (v) plant traits that might predict defence. In a field experiment, we simulated deer damage occurring early and late in the season, recorded arthropod abundances, flowering phenology and measured growth rate and lifetime reproduction. Our study showed that deer herbivory has a negative effect on fitness, with effects being more pronounced for late‐season damage. Selection acted to increase tolerance to deer damage, yet there was low and nonsignificant genetic variation in this trait. In contrast, there was substantial genetic variation in resistance to insect herbivores. Resistance was genetically uncorrelated with tolerance, whereas positive genetic correlations in resistance to insect herbivores suggest there exists diffuse selection on resistance traits. In addition, growth rate and flowering time did not predict variation in tolerance, but flowering phenology was genetically correlated with resistance. Our results suggest that deer damage has the potential to exert selection because browsing reduces plant fitness, but limited standing genetic variation in tolerance is expected to constrain adaptive evolution in O. biennis.     

Giant clams discriminate threats along a risk gradient and display varying habituation rates to different stimuli

It is often beneficial for animals to discriminate between different threats and to habituate to repeated exposures of benign stimuli. While much is known about risk perception in vertebrates and some invertebrates, risk perception in marine invertebrates is less extensively studied. One method to study risk perception is to habituate animals to a series of exposures to one stimulus, and then present a novel stimulus to test if it transfers habituation. Transfer of habituation is seen as a continued decrease in response while lack of transfer is seen either by having a similar or greater magnitude response. We asked whether giant clams (Tridacna maxima) discriminate between biologically relevant types of threats along a risk gradient. Giant clams retract their mantle and close their shell upon detecting a threat. While closed, they neither feed nor photosynthesize, and prior work has shown that the cost of being closed increases as the duration of their response increases. We recorded a clam's latency to emerge after simulated threats chosen to represent a risk gradient: exposure to a small shading event, a medium shading event, a large shading event (chosen to simulate fish swimming above them), tapping on their shell and touching their mantle (chosen to simulate different degrees of direct attack). Although these stimuli are initially perceived as threatening, we expected clams to habituate to them because they are ultimately non‐damaging and it would be costly for clams to remain closed for extended periods of time when there is no threat present. Clams had different initial latencies to emerge and different habituation rates to these treatments, and they did not transfer habituation to higher risk stimuli and to some lower risk stimuli. These results suggest that clams discriminated between these stimuli along a risk gradient and the lack of habituation transfer shows that the new stimulus was perceived as a potential threat. This study demonstrates that sessile bivalves can discern between levels of predatory threat. These photosynthetic clams may benefit from being able to categorize predator cues for efficient energy allocation.