Microhabitats in the tropics buffer temperature in a globally coherent manner

Vegetated habitats contain a variety of fine-scale features that can ameliorate temperate extremes. These buffered microhabitats may be used by species to evade extreme weather and novel climates in the future. Yet, the magnitude and extent of this buffering on a global scale remains unknown. Across all tropical continents and using 36 published studies, we assessed temperature buffering from within microhabitats across various habitat strata and structures (e.g. soil, logs, epiphytes and tree holes) and compared them to non-buffered macro-scale ambient temperatures (the thermal control). Microhabitats buffered temperature by 3.9°C and reduced maximum temperatures by 3.5°C. Buffering was most pronounced in tropical lowlands where temperatures were most variable. With the expected increase in extreme weather events, microhabitats should provide species with a local layer of protection that is not captured by traditional climate assessments, which are typically derived from macro-scale temperatures (e.g. satellites). Our data illustrate the need for a next generation of predictive models that account for species'' ability to move within microhabitats to exploit favourable buffered microclimates.     

Tree-hugging koalas demonstrate a novel thermoregulatory mechanism for arboreal mammals

How climate impacts organisms depends not only on their physiology, but also whether they can buffer themselves against climate variability via their behaviour. One of the way species can withstand hot temperatures is by seeking out cool microclimates, but only if their habitat provides such refugia. Here, we describe a novel thermoregulatory strategy in an arboreal mammal, the koala Phascolarctos cinereus. During hot weather, koalas enhanced conductive heat loss by seeking out and resting against tree trunks that were substantially cooler than ambient air temperature. Using a biophysical model of heat exchange, we show that this behaviour greatly reduces the amount of heat that must be lost via evaporative cooling, potentially increasing koala survival during extreme heat events. While it has long been known that internal temperatures of trees differ from ambient air temperatures, the relevance of this for arboreal and semi-arboreal mammals has not previously been explored. Our results highlight the important role of tree trunks as aboveground ‘heat sinks’, providing cool local microenvironments not only for koalas, but also for all tree-dwelling species.     

Modeling plant species distributions under future climates: how fine scale do climate projections need to be?

Recent studies suggest that species distribution models (SDMs) based on fine‐scale climate data may provide markedly different estimates of climate‐change impacts than coarse‐scale models. However, these studies disagree in their conclusions of how scale influences projected species distributions. In rugged terrain, coarse‐scale climate grids may not capture topographically controlled climate variation at the scale that constitutes microhabitat or refugia for some species. Although finer scale data are therefore considered to better reflect climatic conditions experienced by species, there have been few formal analyses of how modeled distributions differ with scale. We modeled distributions for 52 plant species endemic to the California Floristic Province of different life forms and range sizes under recent and future climate across a 2000‐fold range of spatial scales (0.008–16 km²). We produced unique current and future climate datasets by separately downscaling 4 km climate models to three finer resolutions based on 800, 270, and 90 m digital elevation models and deriving bioclimatic predictors from them. As climate‐data resolution became coarser, SDMs predicted larger habitat area with diminishing spatial congruence between fine‐ and coarse‐scale predictions. These trends were most pronounced at the coarsest resolutions and depended on climate scenario and species' range size. On average, SDMs projected onto 4 km climate data predicted 42% more stable habitat (the amount of spatial overlap between predicted current and future climatically suitable habitat) compared with 800 m data. We found only modest agreement between areas predicted to be stable by 90 m models generalized to 4 km grids compared with areas classified as stable based on 4 km models, suggesting that some climate refugia captured at finer scales may be missed using coarser scale data. These differences in projected locations of habitat change may have more serious implications than net habitat area when predictive maps form the basis of conservation decision making.     

Topographic microclimates drive microhabitat associations at the range margin of a butterfly

The habitat associations of individuals underpin the dynamics of species distributions. Broad‐scale gradients in climate can alter habitat associations across species’ geographic ranges, but topographic heterogeneity creates local microclimates which could generate variation in habitat use at finer spatial scales. We examined the selection of microhabitats for egg‐laying by populations of a thermally‐constrained butterfly, the skipper Hesperia comma, across 16 sites with different regional temperatures and topographic microclimates. Using models of thermal microclimate, we examined how the association between eggs and warm bare ground microhabitats varied with ambient temperature, and predicted bare ground associations in 287 existing H. comma populations, to investigate the relative impacts of regional temperatures and topographic microclimates on microhabitat use. Eggs were most strongly associated with bare ground in relatively cool sites, indicating climate‐driven changes in microhabitat use. The majority of temperature variation between study sites was attributable to topographic microclimates rather than regional temperature differences, such that changes in microhabitat associations occurred principally between north‐ and south‐facing slopes within the same region. Predicted microhabitat associations across the UK distribution of H. comma showed that, due to the large temperature differences generated by topography, most of the between‐population variation in microhabitat use occurs locally within 5 km grid squares, with a smaller proportion occurring at a regional level between 5 km squares. Our findings show how microclimatic variation generated by topography alters the habitat associations of populations at fine spatial scales, suggesting that microclimate‐driven changes in habitat suitability could shape species’ distribution dynamics and their responses to environmental change.     

Thermal Buffering of Microhabitats is a Critical Factor Mediating Warming Vulnerability of Frogs in the Philippine Biodiversity Hotspot

Species may circumvent the impacts of climate warming if the habitats they use reduce ambient temperature. In this study, we identified which frog species from a tropical montane rain forest in the Philippines may be vulnerable to climate warming. To do so, we selected five anuran species that utilize four breeding habitats and identified the sensitivity and exposure of tadpoles and direct‐developer eggs to heat by measuring their critical thermal maximums (CT_max) and the habitat‐specific temperatures they experience. Our study species included two direct‐developer frogs—one species that lays its eggs on exposed leaves, and another that lays its eggs in ferns—and three species that produce aquatic free‐swimming tadpoles—two stream breeders, and one phytotelm (tree hole) breeder. We compared thermal tolerances derived from microclimates of breeding habitats with tolerances derived from macroclimate (i.e., non‐buffered air temperature taken from the rain forest canopy). We also examined whether differences in CT_max existed across life‐history stages (egg, metamorph/young‐of‐year, and adult) for the two direct‐developer frog species. Habitats buffered ambient temperature and expanded thermal tolerances of all frog species. We found that direct‐developers, however, are more vulnerable to increased temperatures than aquatic breeders—indicated by their high sensitivity to temperature, and exposure to high temperatures. Direct‐developer eggs were more sensitive to warming than both metamorph and adult life‐history stages. Thermally buffered microhabitats may represent the only protection against current and impending climate warming. Our data highlight the importance of considering sensitivity and exposure in unison when deciphering warming vulnerability of frogs.     

Identifying refugia from climate change

This article highlights how the loose definition of the term ‘refugia’ has led to discrepancies in methods used to assess the vulnerability of species to the current trend of rising global temperatures. The term ‘refugia’ is commonly used without distinguishing between macrorefugia and microrefugia, ex situ refugia and in situ refugia, glacial and interglacial refugia or refugia based on habitat stability and refugia based on climatic stability. It is not always clear which definition is being used, and this makes it difficult to assess the appropriateness of the methods employed. For example, it is crucial to develop accurate fine‐scale climate grids when identifying microrefugia, but coarse‐scale macroclimate might be adequate for determining macrorefugia. Similarly, identifying in situ refugia might be more appropriate for species with poor dispersal ability but this may overestimate the extinction risk for good dispersers. More care needs to be taken to properly define the context when referring to refugia from climate change so that the validity of methods and the conservation significance of refugia can be assessed.     

Temperature‐related shifts in butterfly phenology depend on the habitat

Many species are becoming active earlier in the season as the climate becomes warmer. In parallel to phenological responses to climate change, many species have also been affected by habitat changes due to anthropogenic land use. As habitat type can directly affect microclimatic conditions, concurrent changes in climate and habitat could have interacting effects on the phenology of species. Temperature‐related shifts in phenology, however, have mostly been studied independent of habitat types. Here, I used long‐term data from a highly standardized monitoring program with 519 transects to study how phenology of butterflies is affected by ambient temperature and habitat type. I compared forests, agricultural areas and settlements, reflecting three major land use forms, and considered butterfly species that were observed in all three of these habitats. Seasonal appearance of the butterflies was affected both by the ambient temperature and the habitat type. As expected, warmer temperatures led to an overall advancement of the appearance and flight period of most species. Surprisingly, however, phenology of species was delayed in settlement habitats, even though this habitat type is generally associated with higher temperatures. A possible explanation is dispersal among habitat types, such that source–sink effects affect local phenology. When there is little productivity in settlement areas, observed butterflies may have immigrated from forest or agricultural habitats and thus appear later in settlements. My findings suggest that a spillover of individuals among habitats may affect phenology trends and indicate that phenological studies need to be interpreted in the context of habitat types. This becomes especially important when defining strategies to prevent or mitigate effects of climate and land‐use changes on phenology and abundance of species.     

Habitat microclimates drive fine‐scale variation in extreme temperatures

Most multicellular terrestrial organisms experience climate at scales of millimetres to metres, yet most species‐climate associations are analysed at resolutions of kilometres or more. Because individuals experience heterogeneous microclimates in the landscape, species sometimes survive where the average background climate appears unsuitable, and equally may be eliminated from sites within apparently suitable grid cells where microclimatic extremes are intolerable. Local vegetation structure and topography can be important determinants of fine‐resolution microclimate, but a literature search revealed that the vast majority of bioclimate studies do not include fine‐scale habitat information, let alone a representation of how habitat affects microclimate. In this paper, we show that habitat type (grassland, heathland, deciduous woodland) is a major modifier of the temperature extremes experienced by organisms. We recorded differences among these habitats of more than 5°C in monthly temperature maxima and minima, and of 10°C in thermal range, on a par with the level of warming expected for extreme future climate change scenarios. Comparable differences were found in relation to variation in local topography (slope and aspect). Hence, we argue that the microclimatic effects of habitat and topography must be included in studies if we are to obtain sufficiently detailed projections of the ecological impacts of climate change to develop detailed adaptation strategies for the conservation of biodiversity.     

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.     

Climate change may drive cave spiders to extinction

Subterranean ecosystems present ideal opportunities to study mechanisms underlying responses to changes in climate because species within them are often adapted to a largely constant temperature. We have characterized the thermal conditions of caves in the western Alps, and related these hypogean climate data to the occurrence of Troglohyphantes spiders (Araneae, Linyphiidae). Our data indicated that present distributions reflect Pleistocene glaciation events and also pointed to specific responses as a consequence of changes in temperature. Constant temperatures recorded inside caves provide an approximation of the mean annual temperature outside, thus we extended the results to a regional scale. We used ecological niche modeling to predict habitat suitability both in the Pleistocene and under future global warming scenarios. These analyses pointed toward a future decline in habitat suitability for subterranean spiders and the potential extinction of the most restricted endemic species. When compared with other species that live in confined habitats such as islands and mountains, we expect cave species to be as much, if not more, vulnerable to climate change.     

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.     

Holocene climate changes and warm man-made refugia may explain why a sixth of British butterflies possess unnatural early-successional habitats

Analyses of their habitats indicate that 18% of British butterfly species are restricted to the earliest seral stages of ecosystems, whereas the same species occupy later seral stages in central Europe, where spring and summer temperatures are warmer. The microclimates of their British habitats are exceptionally warm, compensating for the cooler climate. Most of these British habitats are also ephemeral, and have long depended on man for their creation and regeneration This poses the question of where these species lived before man created their habitats, roughly 6000 BP, I suggest that they are relics from a period when British summers were warmer than today, and that they avoided extinction when the climate cooled by moving into warm refugia created by prehistoric man within three types of ecosystem If summer temperatures become warmer, these species should return to later seral stages that are commoner and less dependent on man.     

Physical effects of habitat‐forming species override latitudinal trends in temperature

Latitudinal and elevational temperature gradients (LTG and ETG) play central roles in biogeographical theory, underpinning predictions of large‐scale patterns in organismal thermal stress, species' ranges and distributional responses to climate change. Yet an enormous fraction of Earth's taxa live exclusively in habitats where foundation species modify temperatures. We examine little‐explored implications of this widespread trend using a classic model system for understanding heat stresses – rocky intertidal shores. Through integrated field measurements and laboratory trials, we demonstrate that thermal buffering by centimetre‐thick mussel and seaweed beds eliminates differences in stress‐inducing high temperatures and associated mortality risk that would otherwise arise over 14° of latitude and ~ 1 m of shore elevation. These results reveal the extent to which physical effects of habitat‐formers can overwhelm broad‐scale thermal trends, suggesting a need to re‐evaluate climate change predictions for many species. Notably, inhabitant populations may exhibit deceptive resilience to warming until refuge‐forming taxa become imperiled.     

Tropical forests are thermally buffered despite intensive selective logging

Tropical rainforests are subject to extensive degradation by commercial selective logging. Despite pervasive changes to forest structure, selectively logged forests represent vital refugia for global biodiversity. The ability of these forests to buffer temperature‐sensitive species from climate warming will be an important determinant of their future conservation value, although this topic remains largely unexplored. Thermal buffering potential is broadly determined by: (i) the difference between the “macroclimate” (climate at a local scale, m to ha) and the “microclimate” (climate at a fine‐scale, mm to m, that is distinct from the macroclimate); (ii) thermal stability of microclimates (e.g. variation in daily temperatures); and (iii) the availability of microclimates to organisms. We compared these metrics in undisturbed primary forest and intensively logged forest on Borneo, using thermal images to capture cool microclimates on the surface of the forest floor, and information from dataloggers placed inside deadwood, tree holes and leaf litter. Although major differences in forest structure remained 9–12 years after repeated selective logging, we found that logging activity had very little effect on thermal buffering, in terms of macroclimate and microclimate temperatures, and the overall availability of microclimates. For 1°C warming in the macroclimate, temperature inside deadwood, tree holes and leaf litter warmed slightly more in primary forest than in logged forest, but the effect amounted to <0.1°C difference between forest types. We therefore conclude that selectively logged forests are similar to primary forests in their potential for thermal buffering, and subsequent ability to retain temperature‐sensitive species under climate change. Selectively logged forests can play a crucial role in the long‐term maintenance of global biodiversity.     

Implications of Climate Change for Bird Conservation in the Southwestern U.S. under Three Alternative Futures

Future expected changes in climate and human activity threaten many riparian habitats, particularly in the southwestern U.S. Using Maximum Entropy (MaxEnt3.3.3) modeling, we characterized habitat relationships and generated spatial predictions of habitat suitability for the Lucy’s warbler (Oreothlypis luciae), the Southwestern willow flycatcher (Empidonax traillii extimus) and the Western yellow-billed cuckoo (Coccyzus americanus). Our goal was to provide site- and species-specific information that can be used by managers to identify areas for habitat conservation and/or restoration along the Rio Grande in New Mexico. We created models of suitable habitat for each species based on collection and survey samples and climate, biophysical, and vegetation data. We projected habitat suitability under future climates by applying these models to conditions generated from three climate models for 2030, 2060 and 2090. By comparing current and future distributions, we identified how habitats are likely to change as a result of changing climate and the consequences of those changes for these bird species. We also examined whether land ownership of high value sites shifts under changing climate conditions. Habitat suitability models performed well. Biophysical characteristics were more important that climate conditions for predicting habitat suitability with distance to water being the single most important predictor. Climate, though less important, was still influential and led to declines of suitable habitat of more than 60% by 2090. For all species, suitable habitat tended to shrink over time within the study area leaving a few core areas of high importance. Overall, climate changes will increase habitat fragmentation and reduce breeding habitat patch size. The best strategy for conserving bird species within the Rio Grande will include measures to maintain and restore critical habitat refugia. This study provides an example of a presence-only habitat model that can be used to inform the management of species at intermediate scales.     

Range expansion through fragmented landscapes under a variable climate

Ecological responses to climate change may depend on complex patterns of variability in weather and local microclimate that overlay global increases in mean temperature. Here, we show that high‐resolution temporal and spatial variability in temperature drives the dynamics of range expansion for an exemplar species, the butterfly Hesperia comma. Using fine‐resolution (5 m) models of vegetation surface microclimate, we estimate the thermal suitability of 906 habitat patches at the species' range margin for 27 years. Population and metapopulation models that incorporate this dynamic microclimate surface improve predictions of observed annual changes to population density and patch occupancy dynamics during the species' range expansion from 1982 to 2009. Our findings reveal how fine‐scale, short‐term environmental variability drives rates and patterns of range expansion through spatially localised, intermittent episodes of expansion and contraction. Incorporating dynamic microclimates can thus improve models of species range shifts at spatial and temporal scales relevant to conservation interventions.     

Physiological correlates of habitat association in East African sunbirds (Nectariniidae)

East African sunbirds (Nectariniidae) vary in the degree to which they use open habitats and forest habitats. Species that use open habitats may experience more extreme temperatures and greater exposure to solar radiation than those in forest habitats. Basal rates of metabolism, body temperature and thermal conductance were compared for open habitat- and forest-associated sunbirds from Kibale National Park, Uganda. Variation in basal rate of metabolism was associated with body mass, but there was no difference between forest and open habitat species. Variation in body temperature was not associated with body mass or habitat. Variation in thermal conductance was associated with body mass and habitat; open habitat species were characterized by significantly lower thermal conductances than forest species. Because reduced thermal conductance may decrease energy expenditure at low ambient temperatures and reduce exogenous heat gain at high ambient temperatures, this difference may optimize energy expenditure when temperatures are highly variable. This suggests a mechanism by which physiological characteristics may influence energetic consequences of habitat selection.     

Resource selection by an ectothermic predator in a dynamic thermal landscape

Predicting the effects of global climate change on species interactions has remained difficult because there is a spatiotemporal mismatch between regional climate models and microclimates experienced by organisms. We evaluated resource selection in a predominant ectothermic predator using a modeling approach that permitted us to assess the importance of habitat structure and local real‐time air temperatures within the same modeling framework. We radio‐tracked 53 western ratsnakes (Pantherophis obsoletus) from 2010 to 2013 in central Missouri, USA, at study sites where this species has previously been linked to prey population demographics. We used Bayesian discrete choice models within an information theoretic framework to evaluate the seasonal effects of fine‐scale vegetation structure and thermal conditions on ratsnake resource selection. Ratsnake resource selection was influenced most by canopy cover, canopy cover heterogeneity, understory cover, and air temperature heterogeneity. Ratsnakes generally preferred habitats with greater canopy heterogeneity early in the active season, and greater temperature heterogeneity later in the season. This seasonal shift potentially reflects differences in resource requirements and thermoregulation behavior. Predicted patterns of space use indicate that ratsnakes preferentially selected open habitats in spring and early summer and forest–field edges throughout the active season. Our results show that downscaled temperature models can be used to enhance our understanding of animal resource selection at scales that can be addressed by managers. We suggest that conservation of snakes or their prey in a changing climate will require consideration of fine‐scale interactions between local air temperatures and habitat structure.     

Incorporating microclimate into species distribution models

Species distribution models (SDMs) have rapidly evolved into one of the most widely used tools to answer a broad range of ecological questions, from the effects of climate change to challenges for species management. Current SDMs and their predictions under anthropogenic climate change are, however, often based on free‐air or synoptic temperature conditions with a coarse resolution, and thus fail to capture apparent temperature (cf. microclimate) experienced by living organisms within their habitats. Yet microclimate operates as soon as a habitat can be characterized by a vertical component (e.g. forests, mountains, or cities) or by horizontal variation in surface cover. The mismatch between how we usually express climate (cf. coarse‐grained free‐air conditions) and the apparent microclimatic conditions that living organisms experience has only recently been acknowledged in SDMs, yet several studies have already made considerable progress in tackling this problem from different angles. In this review, we summarize the currently available methods to obtain meaningful microclimatic data for use in distribution modelling. We discuss the issue of extent and resolution, and propose an integrated framework using a selection of appropriately‐placed sensors in combination with both the detailed measurements of the habitat 3D structure, for example derived from digital elevation models or airborne laser scanning, and the long‐term records of free‐air conditions from weather stations. As such, we can obtain microclimatic data with a relevant spatiotemporal resolution and extent to dynamically model current and future species distributions.     

Stream channel restoration increases climate resiliency in a thermally vulnerable Appalachian river

We quantified stream temperature response to in‐stream habitat restoration designed to improve thermal suitability and resiliency of a high‐elevation Appalachian stream known to support a temperature‐limited brook trout population. Our specific objectives were to determine if: (1) construction of deep pools created channel unit‐scale thermal refugia and (2) reach scale stream channel reconfiguration reduced peak water temperatures along a longitudinal continuum known to be highly susceptible to summer‐time warming. Contrary to expectations, constructed pools did not significantly decrease channel unit‐scale summer water temperatures relative to paired control sites. This suggests that constructed pools did not successfully intercept a cool groundwater source. However, we did find a significant effect of stream channel restoration on reach‐scale thermal regimes. Both mean and maximum daily stream temperatures experienced significantly reduced warming trends in restored sections relative to control sections. Furthermore, we found that restoration efforts had the greatest effect on stream temperatures downstream of large tributaries. Restoration appears to have significantly altered thermal regimes within upper Shavers Fork, largely in response to changes in channel morphology that facilitated water movement below major cold‐water inputs. Decreased longitudinal warming will likely increase the thermal resiliency of the Shavers Fork main‐stem, sustaining the ability of these key large river habitats to continue supporting critical metapopulation processes (e.g. supplemental foraging and dispersal among tributary populations) in the face of climate change.