Tropical butterflies use thermal buffering and thermal tolerance as alternative strategies to cope with temperature increase.

Climate change poses a severe threat to many taxa, with increased mean temperatures and frequency of extreme weather events predicted. Insects can respond to high temperatures using behaviour, such as angling their wings away from the sun or seeking cool local microclimates to thermoregulate or through physiological tolerance. In a butterfly community in Panama, we compared the ability of adult butterflies from 54 species to control their body temperature across a range of air temperatures (thermal buffering ability), as well as assessing the critical thermal maxima for a subset of 24 species. Thermal buffering ability and tolerance were influenced by family, wing length, and wing colour, with Pieridae, and butterflies that are large or darker in colour having the strongest thermal buffering ability, but Hesperiidae, small, and darker butterflies tolerating the highest temperatures. We identified an interaction between thermal buffering ability and physiological tolerance, where species with stronger thermal buffering abilities had lower thermal tolerance, and vice versa. This interaction implies that species with more stable body temperatures in the field may be more vulnerable to increases in ambient temperatures, for example heat waves associated with ongoing climate change. Our study demonstrates that tropical species employ diverse thermoregulatory strategies, which is also reflected in their sensitivity to temperature extremes.

El cambio climático representa una grave amenaza para muchos taxones, con un aumento de las temperaturas medias y la frecuencia de eventos climáticos extremos pronosticados. Los insectos pueden responder a las altas temperaturas mediante comportamientos, como inclinar sus alas fuera del alcance del sol o buscar microclimas frescos locales para termorregular, o a través de la tolerancia fisiológica. En una comunidad de mariposas en Panamá, comparamos la capacidad de las mariposas adultas de 54 especies para controlar su temperatura corporal en un rango de temperaturas del aire (capacidad de amortiguación térmica), así como evaluar el máximo térmico crítico para un subconjunto de 24 especies. La capacidad de amortiguación térmica y la tolerancia se influenciaron por la familia, la longitud del ala y el colour del ala; con Pieridae y mariposas grandes o de colour más oscuro teniendo la capacidad de amortiguación térmica más fuerte, pero Hesperiidae, mariposas pequeñas y de colour más oscuro tolerando las temperaturas más altas. Identificamos una relación entre la capacidad de amortiguación térmica y la tolerancia fisiológica, en la que las especies con mayores capacidades de amortiguación térmica tenían una menor tolerancia térmica, y viceversa. Esta interacción implica que las especies con temperaturas corporales más estables en el campo pueden ser más vulnerables a los aumentos en las temperaturas ambientales, por ejemplo, las olas de calor asociadas con el cambio climático actual. Nuestra investigación demuestra que las especies tropicales emplean diversas estrategias de termorregulación, las cuales también se reflejan en su sensibilidad a las temperaturas extremas.

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.

El calentamiento global es una gran amenaza para las especies alrededor del mundo, sin embargo, no se tiene bien definido sí en los insectos, las especies distribuídas en las zonas tropicales son más vulnerables a los cambios de temperature que las especies de zonas templadas o viceversa. Para responder a este interrogante, utilizamos un protocolo de campo estandarizado aplicado a especies de mariposas distribuídas en zonas tropicales (Panamá) versus zonas templadas (Reino Unido, República Checa y Austria), con el cual buscamos: (1) Evaluar la capacidad de amortiguación (capacidad de regular la temperatura corporal en relación con la temperatura del aire circundante) en el a nivel de ensamblaje y familia, (2) Determinar sí las diferencias en la capacidad de amortiguación es facilitada por sus características morfológicas, y (3) Investigar cómo las mariposas usan los microclimas y el comportamiento para termorregularse a tráves de mediciones de temperatura ecológicamente relevantes. Nuestra hipotesis incial soportaba que las mariposas templadas estaban adaptadas para amortiguar los cambios de temperatura en comparación con las mariposas neotropicales, ya que las especies templadas experimentan un rango más amplio de temperaturas que sus contrapartes tropicales. Contrariamente a nuestra hipótesis, a nivel de ensamble, las especies neotropicales (especialmente familia Nymphalidae) fueron mejores en la capaicidad de amortiguacion que las especies templadas, explicado por el hecho de que individuos se enfrían más a altas temperaturas del aire. Así, la morfología fué el principal impulsor de las diferencias en la capacidad de amortiguación entre las especies neotropicales y templadas en comparación con el ambiente térmico experimentado por las mismas. Encontramos que las mariposas templadas utilizaron la termorregulación de postura para elevar su temperatura corporal más que las mariposas neotropicales, probablemente como una adaptación a los climas templados, aunque la selección de microclimas no difirió entre regiones. Nuestros hallazgos demuestran que las especies de mariposas tienen estrategias de termorregulación únicas, impulsadas principalmente por el comportamiento y morfología, además nuestros resultados demuestran que a diferencia de lo que se ha pensado, las especies neotropicales son igual de vulnerables al calentamiento de su hábitat que las especies templadas.

Indirect maternal effects via nest microbiome composition drive gut colonization in altricial chicks.

Gut microbial communities are complex and heterogeneous and play critical roles for animal hosts. Early-life disruptions to microbiome establishment can negatively impact host fitness and development. However, the consequences of such early-life disruptions remain unknown in wild birds. To help fill this gap, we investigated the effect of continuous early-life gut microbiome disruptions on the establishment and development of gut communities in wild Great tit (Parus major) and Blue tit (Cyanistes caeruleus) nestlings by applying antibiotics and probiotics. Treatment neither affected nestling growth nor their gut microbiome composition. Independent of treatment, nestling gut microbiomes of both species grouped by brood, which shared the highest numbers of bacterial taxa with both nest environment and their mother. Although fathers showed different gut communities than their nestlings and nests, they still contributed to structuring chick microbiomes. Lastly, we observed that the distance between nests increased inter-brood microbiome dissimilarity, but only in Great tits, indicating that species-specific foraging behaviour and/or microhabitat influence gut microbiomes. Overall, the strong maternal effect, driven by continuous recolonization from the nest environment and vertical transfer of microbes during feeding, appears to provide resilience towards early-life disruptions in nestling gut microbiomes.

Body size, not species identity, drives body heating in alpine Erebia butterflies.

Efficient thermoregulation is crucial for animals living under fluctuating climatic and weather conditions. We studied the body heating of six butterfly species of the genus Erebia (Lepidoptera: Nymphalidae) that co-occur in the European Alps. We tested whether butterfly physical characteristics (body size, wing loading) are responsible for the inter-specific differences in body temperatures recorded previously under natural conditions. We used a thermal camera to measure body heating of wild butterfly individuals in a laboratory experiment with artificial light and heating sources. We revealed that physical characteristics had a small effect on explaining inter-specific differences in mean body temperatures recorded in the field. Our results show that larger butterflies, with higher weight and wing loading, heated up more slowly but reached the same asymptotic body temperature as smaller butterflies. Altogether, our results suggest that differences in body temperatures among Erebia species observed in the field might be caused mainly by species-specific microhabitat use and point towards an important role of active behavioural thermoregulation in adult butterflies. We speculate that microclimate heterogeneity in mountain habitats facilitates behavioural thermoregulation of adults. Similarly, microclimate structuring might also increase survival of less mobile butterfly life stages, i.e., eggs, larvae and pupae. Thus, landscape heterogeneity in management practices may facilitate long term survival of montane invertebrates under increased anthropogenic pressures.

Specific gut bacterial responses to natural diets of tropical birds.

The composition of gut bacterial communities is strongly influenced by the host diet in many animal taxa. For birds, the effect of diet on the microbiomes has been documented through diet manipulation studies. However, for wild birds, most studies have drawn on literature-based information to decipher the dietary effects, thereby, overlooking individual variation in dietary intake. Here we examine how naturally consumed diets influence the composition of the crop and cloacal microbiomes of twenty-one tropical bird species, using visual and metabarcoding-based identification of consumed diets and bacterial 16S rRNA microbiome sequencing. We show that diet intakes vary markedly between individuals of the same species and that literature-based dietary guilds grossly underestimate intraspecific diet variability. Furthermore, despite an effect of literature-based dietary guild assignment of host taxa, the composition of natural diets does not align with crop and cloacal microbiome similarity. However, host-taxon specific gut bacterial lineages are positively correlated with specific diet items, indicating that certain microbes associate with different diet components in specific avian hosts. Consequently, microbiome composition is not congruent with the overall consumed diet composition of species, but specific components of a consumed diet lead to host-specific effects on gut bacterial taxa.

Low winter precipitation, but not warm autumns and springs, threatens mountain butterflies in middle-high mountains.

Low-elevation mountains represent unique model systems to study species endangered by climate warming, such as subalpine and alpine species of butterflies. We aimed to test the effect of climate variables experienced by Erebia butterflies during their development on adult abundances and phenology, targeting the key climate factors determining the population dynamics of mountain insects. We analysed data from a long-term monitoring of adults of two subalpine and alpine butterfly species, Erebia epiphron and E. sudetica (Nymphalidae: Satyrinae) in the Jeseník Mts and Krkonose Mts (Czech Republic). Our data revealed consistent patterns in their responses to climatic conditions. Lower precipitation (i.e., less snow cover) experienced by overwintering larvae decreases subsequent adult abundances. Conversely, warmer autumns and warmer and drier springs during the active larval phase increase adult abundances and lead to earlier onset and extended duration of the flight season. The population trends of these mountain butterflies are stable or even increasing. On the background of generally increasing temperatures within the mountain ranges, population stability indicates dynamic equilibrium of positive and detrimental consequences of climate warming among different life history stages. These contradictory effects warn against simplistic predictions of climate change consequences on mountain species based only on predicted increases in average temperature. Microclimate variability may facilitate the survival of mountain insect populations, however the availability of suitable habitats will strongly depend on the management of mountain grasslands.

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.

Climatic niche evolution is faster in sympatric than allopatric lineages of the butterfly genus Pyrgus.

Understanding how speciation relates to ecological divergence has long fascinated biologists. It is assumed that ecological divergence is essential to sympatric speciation, as a mechanism to avoid competition and eventually lead to reproductive isolation, while divergence in allopatry is not necessarily associated with niche differentiation. The impact of the spatial context of divergence on the evolutionary rates of abiotic dimensions of the ecological niche has rarely been explored for an entire clade. Here, we compare the magnitude of climatic niche shifts between sympatric versus allopatric divergence of lineages in butterflies. By combining next-generation sequencing, parametric biogeography and ecological niche analyses applied to a genus-wide phylogeny of Palaearctic Pyrgus butterflies, we compare evolutionary rates along eight climatic dimensions across sister lineages that diverged in large-scale sympatry versus allopatry. In order to examine the possible effects of the spatial scale at which sympatry is defined, we considered three sets of biogeographic assignments, ranging from narrow to broad definition. Our findings suggest higher rates of niche evolution along all climatic dimensions for sister lineages that diverge in sympatry, when using a narrow delineation of biogeographic areas. This result contrasts with significantly lower rates of climatic niche evolution found in cases of allopatric speciation, despite the biogeographic regions defined here being characterized by significantly different climates. Higher rates in allopatry are retrieved when biogeographic areas are too widely defined-in such a case allopatric events may be recorded as sympatric. Our results reveal the macro-evolutionary significance of abiotic niche differentiation involved in speciation processes within biogeographic regions, and illustrate the importance of the spatial scale chosen to define areas when applying parametric biogeographic analyses.

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.

Thermoregulation and microhabitat use in mountain butterflies of the genus Erebia: importance of fine-scale habitat heterogeneity.

Mountain butterflies have evolved efficient thermoregulation strategies enabling their survival in marginal conditions with short flight season and unstable weather. Understanding the importance of their behavioural thermoregulation by habitat use can provide novel information for predicting the fate of alpine Lepidoptera and other insects under ongoing climate change. We studied the link between microhabitat use and thermoregulation in adults of seven species of a butterfly genus Erebia co-occurring in the Austrian Alps. We captured individuals in the field and measured their body temperature in relation to microhabitat and air temperature. We asked whether closely related species regulate their body temperature differently, and if so, what is the effect of behaviour, species traits and individual traits on body to air and body to microhabitat temperature differences. Co-occurring species differed in mean body temperature. These differences were driven by active microhabitat selection by individuals and also by species-specific habitat preferences. Species inhabiting grasslands and rocks utilised warmer microclimates to maintain higher body temperature than woodland species. Under low air temperatures, species of rocky habitats heated up more effectively than species of grasslands and woodlands which allowed them to stay active in colder weather. Species morphology and individual traits play rather minor roles in the thermoregulatory differences; although large species and young individuals maintained higher body temperature. We conclude that diverse microhabitat conditions at small spatial scales probably contribute to sympatric occurrence of closely related species with different thermal demands and that preserving heterogeneous conditions in alpine landscapes might mitigate detrimental consequences of predicted climate change.