Shape of Evasive Prey Can Be an Important Cue That Triggers Learning in Avian Predators

Advertising escape ability could reduce predatory attacks. However, the effectiveness of certain phenotypic cues (e.g., color, shape, and size) in signaling evasiveness is still unknown. Understanding the role of such signals in driving predator learning is important to infer the evolutionary mechanisms leading to convergent evasiveness signals among prey species (i.e., evasive mimicry). We aim to understand the role of the color pattern (white patches on dark background) and morphology (extended butterfly hindwings) in driving learning and avoidance of escaping prey by surrogate avian predators, the European blue tit. These cues are common in butterflies and have been suspected to advertise escape ability in nature. We use dummy butterflies harboring shape and color patterns commonly found in skippers (family Hesperiidae). The prey models displayed the studied phenotypical cues (hindwing tails and white bands) in factorial combinations, and we tested whether those cues were learned as evasive signals and were generalised to different phenotypes. Our results suggest that hindwing tails and white bands can be associated with prey evasiveness. In addition, wild blue tits might learn and avoid attacking prey models bearing the studied phenotypic cues. Although blue tits seem to have an initial preference for the phenotype consisting of white patches and hindwing tails, the probability of attacking it was substantially reduced once the cues were associated with escaping ability. This suggests that the same morphological cues might be interchangeable as preference/avoidance signals. Further investigation of the salience of hindwing tails vs. white bands as cues for escaping ability, revealed that predators can associate both color pattern and shape to the difficulty of capture, and possibly generalize their aversion to other prey harboring those cues. More studies with larger sample sizes are needed to confirm this trend. Altogether, our results highlight the hitherto overlooked role of shape (butterfly hindwing tails) for signaling prey unprofitability.Peer reviewe

Thermoregulatory ability and mechanism do not differ consistently between neotropical and temperate butterflies

Climate change is a major threat to species worldwide, yet it remains uncertain whether tropical or temperate species are more vulnerable to changing temperatures. To further our understanding of this, we used a standardised field protocol to (1) study the buffering ability (ability to regulate body temperature relative to surrounding air temperature) of neotropical (Panama) and temperate (the United Kingdom, Czech Republic and Austria) butterflies at the assemblage and family level, (2) determine if any differences in buffering ability were driven by morphological characteristics and (3) used ecologically relevant temperature measurements to investigate how butterflies use microclimates and behaviour to thermoregulate. We hypothesised that temperate butterflies would be better at buffering than neotropical butterflies as temperate species naturally experience a wider range of temperatures than their tropical counterparts. Contrary to our hypothesis, at the assemblage level, neotropical species (especially Nymphalidae) were better at buffering than temperate species, driven primarily by neotropical individuals cooling themselves more at higher air temperatures. Morphology was the main driver of differences in buffering ability between neotropical and temperate species as opposed to the thermal environment butterflies experienced. Temperate butterflies used postural thermoregulation to raise their body temperature more than neotropical butterflies, probably as an adaptation to temperate climates, but the selection of microclimates did not differ between regions. Our findings demonstrate that butterfly species have unique thermoregulatory strategies driven by behaviour and morphology, and that neotropical species are not likely to be more inherently vulnerable to warming than temperate species

Conserved ancestral tropical niche but different continental histories explain the latitudinal diversity gradient in brush-footed butterflies.

The global increase in species richness toward the tropics across continents and taxonomic groups, referred to as the latitudinal diversity gradient, stimulated the formulation of many hypotheses to explain the underlying mechanisms of this pattern. We evaluate several of these hypotheses to explain spatial diversity patterns in a butterfly family, the Nymphalidae, by assessing the contributions of speciation, extinction, and dispersal, and also the extent to which these processes differ among regions at the same latitude. We generate a time-calibrated phylogeny containing 2,866 nymphalid species (~45% of extant diversity). Neither speciation nor extinction rate variations consistently explain the latitudinal diversity gradient among regions because temporal diversification dynamics differ greatly across longitude. The Neotropical diversity results from low extinction rates, not high speciation rates, and biotic interchanges with other regions are rare. Southeast Asia is also characterized by a low speciation rate but, unlike the Neotropics, is the main source of dispersal events through time. Our results suggest that global climate change throughout the Cenozoic, combined with tropical niche conservatism, played a major role in generating the modern latitudinal diversity gradient of nymphalid butterflies

Facing the Heat: Thermoregulation and Behaviour of Lowland Species of a Cold-Dwelling Butterfly Genus, Erebia.

Understanding the potential of animals to immediately respond to changing temperatures is imperative for predicting the effects of climate change on biodiversity. Ectothermic animals, such as insects, use behavioural thermoregulation to keep their body temperature within suitable limits. It may be particularly important at warm margins of species occurrence, where populations are sensitive to increasing air temperatures. In the field, we studied thermal requirements and behavioural thermoregulation in low-altitude populations of the Satyrinae butterflies Erebia aethiops, E. euryale and E. medusa. We compared the relationship of individual body temperature with air and microhabitat temperatures for the low-altitude Erebia species to our data on seven mountain species, including a high-altitude population of E. euryale, studied in the Alps. We found that the grassland butterfly E. medusa was well adapted to the warm lowland climate and it was active under the highest air temperatures and kept the highest body temperature of all species. Contrarily, the woodland species, E. aethiops and a low-altitude population of E. euryale, kept lower body temperatures and did not search for warm microclimates as much as other species. Furthermore, temperature-dependence of daily activities also differed between the three low-altitude and the mountain species. Lastly, the different responses to ambient temperature between the low- and high-altitude populations of E. euryale suggest possible local adaptations to different climates. We highlight the importance of habitat heterogeneity for long-term species survival, because it is expected to buffer climate change consequences by providing a variety of microclimates, which can be actively explored by adults. Alpine species can take advantage of warm microclimates, while low-altitude grassland species may retreat to colder microhabitats to escape heat, if needed. However, we conclude that lowland populations of woodland species may be more severely threatened by climate warming because of the unavailability of relatively colder microclimates

Overview of temperature data.

<p>Summary of measured values for the two lowland butterfly species <i>Erebia aethiops</i> and <i>E. medusa</i> and for low- and high-altitude populations of <i>E. euryale</i> are shown; data for the remaining alpine congeners are available in [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0150393#pone.0150393.ref014" target="_blank">14</a>]. <i>N</i>(<i>F</i>, <i>M</i>) = the number of individuals measured (females, males); <i>T</i>_<i>a</i> = air temperature; <i>T</i>_<i>m</i> = microhabitat temperature; <i>T</i>_<i>b</i> = body temperature.</p

Comparison of body temperatures of lowland and alpine species and populations.

<p>The dependence of body temperature <i>T</i>_<i>b</i> on air temperature <i>T</i>_<i>a</i> (A) and on microhabitat temperature <i>T</i>_<i>m</i> (B) of low-altitude (orange lines) and high-altitude (blue lines) species of <i>Erebia</i> butterflies fitted by generalized additive models. Two populations of <i>E. euryale</i> are shown in red (low-altitude) and dark blue (high-altitude). Only the fitted lines are shown to facilitate comparison. See <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0150393#pone.0150393.t002" target="_blank">Table 2</a> for detailed results of statistical tests.</p

Facing the Heat: Thermoregulation and Behaviour of Lowland Species of a Cold-Dwelling Butterfly Genus, <i>Erebia</i>

<div><p>Understanding the potential of animals to immediately respond to changing temperatures is imperative for predicting the effects of climate change on biodiversity. Ectothermic animals, such as insects, use behavioural thermoregulation to keep their body temperature within suitable limits. It may be particularly important at warm margins of species occurrence, where populations are sensitive to increasing air temperatures. In the field, we studied thermal requirements and behavioural thermoregulation in low-altitude populations of the Satyrinae butterflies <i>Erebia aethiops</i>, <i>E. euryale</i> and <i>E. medusa</i>. We compared the relationship of individual body temperature with air and microhabitat temperatures for the low-altitude <i>Erebia</i> species to our data on seven mountain species, including a high-altitude population of <i>E. euryale</i>, studied in the Alps. We found that the grassland butterfly <i>E. medusa</i> was well adapted to the warm lowland climate and it was active under the highest air temperatures and kept the highest body temperature of all species. Contrarily, the woodland species, <i>E. aethiops</i> and a low-altitude population of <i>E. euryale</i>, kept lower body temperatures and did not search for warm microclimates as much as other species. Furthermore, temperature-dependence of daily activities also differed between the three low-altitude and the mountain species. Lastly, the different responses to ambient temperature between the low- and high-altitude populations of <i>E. euryale</i> suggest possible local adaptations to different climates. We highlight the importance of habitat heterogeneity for long-term species survival, because it is expected to buffer climate change consequences by providing a variety of microclimates, which can be actively explored by adults. Alpine species can take advantage of warm microclimates, while low-altitude grassland species may retreat to colder microhabitats to escape heat, if needed. However, we conclude that lowland populations of woodland species may be more severely threatened by climate warming because of the unavailability of relatively colder microclimates.</p></div

Proportion of settling, nectaring, and flying <i>Erebia</i> butterflies depends on air temperature.

<p>Results of generalized additive models (GAM) testing the dependence of the proportion of settling, nectaring and flying individuals of <i>Erebia</i> species on the air temperature <i>T</i>_<i>a</i>. The fitted relationships are visualised in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0150393#pone.0150393.g004" target="_blank">Fig 4</a>. Estimated d.f. describes the complexity of the fitted relationship; <i>e</i>.<i>d</i>.<i>f</i>. = 1 for a linear relationship, <i>e</i>.<i>d</i>.<i>f</i>.>1 for a non-linear relationship.</p

Main types of behaviour are affected by the air temperature.

<p>The dependence of the proportion of settling, nectaring and flying individuals on air temperature <i>T</i>_<i>a</i> in individual species of <i>Erebia</i> butterflies as estimated by generalized additive models (GAM). Only species with at least some significant trends are displayed; full results of the GAMs are shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0150393#pone.0150393.t003" target="_blank">Table 3</a>.</p

Body temperature depends on air and microhabitat temperatures.

<p>The relationship between body temperature <i>T</i>_<i>b</i> and air temperature <i>T</i>_<i>a</i> (A-D) and body temperature and microhabitat temperature <i>T</i>_<i>m</i> (E-H) in two lowland species of <i>Erebia</i> butterflies and in low- (<i>E. euryale</i>-CZ) and high-altitude (<i>E. euryale</i>-Alps) populations of a mountain species, <i>E. euryale</i>. See <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0150393#pone.0150393.t002" target="_blank">Table 2</a> for detailed results of statistical tests.</p