The impact of climate change measured at relevant spatial scales: new hope for tropical lizards

Much attention has been given to recent predictions that widespread extinctions of tropical ectotherms, and tropical forest lizards in particular, will result from anthropogenic climate change. Most of these predictions, however, are based on environmental temperature data measured at a maximum resolution of 1 km², whereas individuals of most species experience thermal variation on a much finer scale. To address this disconnect, we combined thermal performance curves for five populations of Anolis lizard from the Bay Islands of Honduras with high‐resolution temperature distributions generated from physical models. Previous research has suggested that open‐habitat species are likely to invade forest habitat and drive forest species to extinction. We test this hypothesis, and compare the vulnerabilities of closely related, but allopatric, forest species. Our data suggest that the open‐habitat populations we studied will not invade forest habitat and may actually benefit from predicted warming for many decades. Conversely, one of the forest species we studied should experience reduced activity time as a result of warming, while two others are unlikely to experience a significant decline in performance. Our results suggest that global‐scale predictions generated using low‐resolution temperature data may overestimate the vulnerability of many tropical ectotherms to climate change.     

Ontogenetic thermal tolerance and performance of ectotherms at variable temperatures

Early experience and environmental conditions during ontogeny may affect organismal structure, physiology and fitness. Here, we assessed the effect of developmental acclimation to environmental thermal variability on walking speed in Drosophila melanogaster adults. Our results showed a shift in the performance curve to the right. Thus, upper and lower thermal limits exhibited developmental plasticity. Additionally, in constant and variable climatic scenarios, flies shifted to the right the optimum temperature but the maximum performance decreased only in flies reared on high temperatures and high thermal variability. Overall, we showed that environmental cues during ontogeny might help to construct phenotypic variation, which supports the hypothesis of ontogenetic dependence of thermal tolerances.     

A conceptual framework for understanding thermal constraints on ectotherm activity with implications for predicting responses to global change

Activity budgets influence the expression of life history traits as well as population dynamics. For ectotherms, a major constraint on activity is environmental temperature. Nonetheless, we currently lack a comprehensive conceptual framework for understanding thermal constraints on activity, which hinders our ability to rigorously apply activity data to answer ecological and evolutionary questions. Here, we integrate multiple aspects of temperature‐dependent activity into a single unified framework that has general applicability. We also provide examples of the implementation of this framework to address fundamental questions in ecology relating to climate change vulnerability and species’ distributions using empirical data from a tropical lizard.     

Too hot to die? The effects of vegetation shading on past,present, and future activity budgets of two diurnal skinks from arid Australia

Behavioral thermoregulation is an important mechanism allowing ectotherms to respond to thermal variations. Its efficiency might become imperative for securing activity budgets under future climate change. For diurnal lizards, thermal microhabitat variability appears to be of high importance, especially in hot deserts where vegetation is highly scattered and sensitive to climatic fluctuations. We investigated the effects of a shading gradient from vegetation on body temperatures and activity timing for two diurnal, terrestrial desert lizards, Ctenotus regius, and Morethia boulengeri, and analyzed their changes under past, present, and future climatic conditions. Both species’ body temperatures and activity timing strongly depended on the shading gradient provided by vegetation heterogeneity. At high temperatures, shaded locations provided cooling temperatures and increased diurnal activity. Conversely, bushes also buffered cold temperature by saving heat. According to future climate change scenarios, cooler microhabitats might become beneficial to warm‐adapted species, such as C. regius, by increasing the duration of daily activity. Contrarily, warmer microhabitats might become unsuitable for less warm‐adapted species such as M. boulengeri for which midsummers might result in a complete restriction of activity irrespective of vegetation. However, total annual activity would still increase provided that individuals would be able to shift their seasonal timing towards spring and autumn. Overall, we highlight the critical importance of thermoregulatory behavior to buffer temperatures and its dependence on vegetation heterogeneity. Whereas studies often neglect ecological processes when anticipating species’ responses to future climate change the strongest impact of a changing climate on terrestrial ectotherms in hot deserts is likely to be the loss of shaded microhabitats rather than the rise in temperature itself. We argue that conservation strategies aiming at addressing future climate changes should focus more on the cascading effects of vegetation rather than on shifts of species distributions predicted solely by climatic envelopes.     

Calling behaviour under climate change: geographical and seasonal variation of calling temperatures in ectotherms

Calling behaviour is strongly temperature‐dependent and critical for sexual selection and reproduction in a variety of ectothermic taxa, including anuran amphibians, which are the most globally threatened vertebrates. However, few studies have explored how species respond to distinct thermal environments at time of displaying calling behaviour, and thus it is still unknown whether ongoing climate change might compromise the performance of calling activity in ectotherms. Here, we used new audio‐trapping techniques (automated sound recording and detection systems) between 2006 and 2009 to examine annual calling temperatures of five temperate anurans and their patterns of geographical and seasonal variation at the thermal extremes of species ranges, providing insights into the thermal breadths of calling activity of species, and the mechanisms that enable ectotherms to adjust to changing thermal environments. All species showed wide thermal breadths during calling behaviour (above 15 °C) and increases in calling temperatures in extremely warm populations and seasons. Thereby, calling temperatures differed both geographically and seasonally, both in terrestrial and aquatic species, and were 8–22 °C below the specific upper critical thermal limits (CT_max) and strongly associated with the potential temperatures of each thermal environment (operative temperatures during the potential period of breeding). This suggests that calling behaviour in ectotherms may take place at population‐specific thermal ranges, diverging when species are subjected to distinct thermal environments, and might imply plasticity of thermal adjustment mechanisms (seasonal and developmental acclimation) that supply species with means of coping with climate change. Furthermore, the thermal thresholds of calling at the onset of the breeding season were dissimilar between conspecific populations, suggesting that other factors besides temperature are needed to trigger the onset of reproduction. Our findings imply that global warming would not directly inhibit calling behaviour in the study species, although might affect other temperature‐dependent features of their acoustic communication system.     

Broad thermal capacity facilitates the primarily pelagic existence of northern fur seals (Callorhinus ursinus)

Thermoregulatory capacity may constrain the distribution of marine mammals despite having anatomical and physiological adaptations to compensate for the thermal challenges of an aquatic lifestyle. We tested whether subadult female northern fur seals (Callorhinus ursinus) experience increased thermoregulatory costs in water temperatures potentially encountered during their annual migration in the Bering Sea and North Pacific Ocean. Metabolic rates were measured seasonally in 6 captive female northern fur seals (2.75–3.5 yr old) in ambient air and controlled water temperatures of 2°C, 10°C, and 18°C. Rates of oxygen consumption in ambient air (1°C–18°C) were not related to environmental temperature except below 2.5°C (winter only). However, metabolism was significantly higher during the fall seasonal trials (September–October) compared to other times of year, perhaps due to the costs of molting. The fur seals appeared thermally neutral in all seasons for all water temperatures tested (2°C–18°C) except during the summer when metabolic rates were higher in the 2°C water. Comparing this broad thermal neutral zone to the average sea surface temperatures potentially encountered during annual migrations indicates wild fur seals can likely exploit a large geographic area without added thermal metabolic costs.     

The final thermal preferendum of fishes: Shuttling behavior and acclimation overshoot

The concept of final preferendum is reexamined in light of data concerning acclimation in a cyclic thermal regime. Because of Shuttling behavior to temperatures above and below the mean preferendum, and because of faster acclimation upward than downward, which result in acclimation to a temperature exceeding the mean of the cycle, a fish may finally gravitate to a preferendum which does not equal acclimation temperature. It is suggested that a distinction be made between the crossover-point preferendum, where preference and acclimation are equal, and the ultimate preferendum to which a fish will ultimately gravitate.     

Using a historic drought and high‐heat event to validate thermal exposure predictions for ground‐dwelling birds

Deviations from typical environmental conditions can provide insight into how organisms may respond to future weather extremes predicted by climate modeling. During an episodic and multimonth heat wave event (i.e., ambient temperature up to 43.4°C), we studied the thermal ecology of a ground‐dwelling bird species in Western Oklahoma, USA. Specifically, we measured black bulb temperature (T_bb) and vegetation parameters at northern bobwhite (Colinus virginianus; hereafter bobwhite) adult and brood locations as well as at stratified random points in the study area. On the hottest days (i.e., ≥39°C), adults and broods obtained thermal refuge using tall woody cover that remained on average up to 16.51°C cooler than random sites on the landscape which reached >57°C. We also found that refuge sites used by bobwhites moderated thermal conditions by more than twofold compared to stratified random sites on the landscape but that T_bb commonly exceeded thermal stress thresholds for bobwhites (39°C) for several hours of the day within thermal refuges. The serendipitous high heat conditions captured in our study represent extreme heat for our study region as well as thermal stress for our study species, and subsequently allowed us to assess ground‐dwelling bird responses to temperatures that are predicted to become more common in the future. Our findings confirm the critical importance of tall woody cover for moderating temperatures and functioning as important islands of thermal refuge for ground‐dwelling birds, especially during extreme heat. However, the potential for extreme heat loads within thermal refuges that we observed (albeit much less extreme than the landscape) indicates that the functionality of tall woody cover to mitigate heat extremes may be increasingly limited in the future, thereby reinforcing predictions that climate change represents a clear and present danger for these species.     

Decadal losses of canopy‐forming algae along the warm temperate coastline of Brazil

The loss of canopy‐forming seaweeds from urbanized coasts has intensified in response to warming seas and non‐climatic pressures such as population growth and declining water quality. Surprisingly, there has been little information on the extent of historical losses in the South‐western Atlantic, which limits our ability to place this large marine ecosystem in a global context. Here, we use meta‐analysis to examine long‐term (1969–2017) changes to the cover and biomass of Sargassum spp. and structurally simple algal turfs along more than 1,000 kilometres of Brazil's warm temperate coastline. Analysis revealed major declines in canopy cover that were independent of season (i.e., displaying similar trends for both summer and winter) but varied with coastal environmental setting, whereby sheltered bays experienced greater losses than coastal locations. On average, covers of Sargassum spp. declined by 2.6% per year, to show overall losses of 52% since records began (ranging from 20% to 89%). This contrasted with increases in the cover of filamentous turfs (24% over the last 27 years) which are known to proliferate along human‐impacted coasts. To test the relative influence of climatic versus non‐climatic factors as drivers of this apparent canopy‐to‐turf shift, we examined how well regional warming trends (decadal changes to sea surface temperature) and local proxies of coastal urbanization (population density, thermal pollution, turbidity and nutrient inputs) were able to predict the changes in seaweed communities. Our results revealed that the most pronounced canopy losses over the past 50 years were at sites exhibiting the greatest degree of coastal warming, the highest population growth and those located in semi‐enclosed sheltered bays. These findings contribute knowledge on the drivers of canopy loss in the South‐western Atlantic and join with global efforts to understand and mitigate declines of marine keystone species.     

Getting to the core: Internal body temperatures help reveal the ecological function and thermal implications of the lions’ mane

It has been proposed that there is a thermal cost of the mane to male lions, potentially leading to increased body surface temperatures (T_s), increased sperm abnormalities, and to lower food intake during hot summer months. To test whether a mane imposes thermal costs on males, we measured core body temperature (T_b) continuously for approximately 1 year in 18 free‐living lions. There was no difference in the 24‐hr maximum T_b of males (n = 12) and females (n = 6), and males had a 24‐hr mean T_b that was 0.2 ± 0.1°C lower than females after correcting for seasonal effects. Although feeding on a particular day increased 24‐hr mean and 24‐hr maximum T_b, this phenomenon was true of both male and female lions, and females had higher 24‐hr mean and 24‐hr maximum T_b than males, on both days when lions did not feed, and on days when lions did feed. Twenty‐four‐hour T_b was not influenced by mane length or color, and 24‐hr mean T_b was negatively correlated with mane length. These data contradict the suggestion that there exists a thermal cost to male lions in possessing a long dark mane, but do not preclude the possibility that males compensate for a mane with increased heat loss. The increased insulation caused by a mane does not necessarily have to impair heat loss by males, which in hot environments is primarily through respiratory evaporative cooling, nor does in necessarily lead to increased heat gain, as lions are nocturnal and seek shade during the day. The mane may even act as a heat shield by increasing insulation. However, dominant male lions frequent water points more than twice as often as females, raising the possibility that male lions are increasing water uptake to facilitate increased evaporative cooling. The question of whether male lions with manes compensate for a thermal cost to the mane remains unresolved, but male lions with access to water do not have higher T_b than females or males with smaller manes.     

Host‐specific thermal profiles affect fitness of a widespread pathogen

Host behavior can interact with environmental context to influence outcomes of pathogen exposure and the impact of disease on species and populations. Determining whether the thermal behaviors of individual species influence susceptibility to disease can help enhance our ability to explain and predict how and when disease outbreaks are likely to occur. The widespread disease chytridiomycosis (caused by the fungal pathogen Batrachochytrium dendrobatidis, Bd) often has species‐specific impacts on amphibian communities; some host species are asymptomatic, whereas others experience mass mortalities and population extirpation. We determined whether the average natural thermal regimes experienced by sympatric frog species in nature, in and of themselves, can account for differences in vulnerability to disease. We did this by growing Bd under temperatures mimicking those experienced by frogs in the wild. At low and high elevations, the rainforest frogs Litoria nannotis, L. rheocola, and L. serrata maintained mean thermal regimes within the optimal range for pathogen growth (15–25°C). Thermal regimes for L. serrata, which has recovered from Bd‐related declines, resulted in slower pathogen growth than the cooler and less variable thermal regimes for the other two species, which have experienced more long‐lasting declines. For L. rheocola and L. serrata, pathogen growth was faster in thermal regimes corresponding to high elevations than in those corresponding to low elevations, where temperatures were warmer. For L. nannotis, which prefers moist and thermally stable microenvironments, pathogen growth was fastest for low‐elevation thermal regimes. All of the thermal regimes we tested resulted in pathogen growth rates equivalent to, or significantly faster than, rates expected from constant‐temperature experiments. The effects of host body temperature on Bd can explain many of the broad ecological patterns of population declines in our focal species, via direct effects on pathogen fitness. Understanding the functional response of pathogens to conditions experienced by the host is important for determining the ecological drivers of disease outbreaks.     

Impact of global warming at the range margins: phenotypic plasticity and behavioral thermoregulation will buffer an endemic amphibian

When dispersal is not an option to evade warming temperatures, compensation through behavior, plasticity, or evolutionary adaptation is essential to prevent extinction. In this work, we evaluated whether there is physiological plasticity in the thermal performance curve (TPC) of maximum jumping speed in individuals acclimated to current and projected temperatures and whether there is an opportunity for behavioral thermoregulation in the desert landscape where inhabits the northernmost population of the endemic frog Pleurodema thaul. Our results indicate that individuals acclimated to 20°C and 25°C increased the breath of their TPCs by shifting their upper limits with respect to when they were acclimated at 10°C. In addition, even when dispersal is not possible for this population, the landscape is heterogeneous enough to offer opportunities for behavioral thermoregulation. In particular, under current climatic conditions, behavioral thermoregulation is not compulsory as available operative temperatures are encompassed within the population TPC limits. However, for severe projected temperatures under climate change, behavioral thermoregulation will be required in the sunny patches. In overall, our results suggest that this population of Pleurodema thaul will be able to endure the worst projected scenario of climate warming as it has not only the physiological capacities but also the environmental opportunities to regulate its body temperature behaviorally.     

Vicariance of Pyrocoelia fireflies (Coleoptera: Lampyridae) in the Ryukyu islands,Japan

We performed molecular phylogenetic analyses based on the mitochondrial COI gene (687 bp) and the nuclear 28S rRNA gene (715 bp) and reconstructed phylogenetic trees of the Pyrocoelia fireflies in the Ryukyu Islands and eastern Asia. Age calibration was done using a robust geological constraint: the Okinawa trough and associated straits began to rift at 1.55 Ma, isolating the Ryukyu Islands from the Chinese continent, Japanese islands, Taiwan island and some of the islands from each other. We suggest that the physical isolation of these islands began to generate the allopatric speciation within these islands, so the timing of this isolation was assigned to an appropriate node. The topology is completely concordant among phylogenetic trees reconstructed using MEGA (maximum‐likelihood), raxmlGUI (maximum‐likelihood) and BEAST (Bayesian inference; including combined analysis of COI and 28S rRNA genes). Two lineages are recognized, related to their emergence time; spring to summer, and autumn. In each lineage, vicariance is inferred to have begun at 1.55 Ma from our phylogenetic and geological analyses. In lineage 1, P. oshimana (Amami), P. matsumurai (Okinawa), P. discicollis (W. Japan), P. fumosa (E. Japan) and P. abdominalis (Yaeyama) were differentiated. In lineage 2, P. rufa (Tsushima and Korea), P. miyako (Miyako‐jima), P. atripennis (Ishigaki‐jima) and P. praetexta (Taiwan and HongKong) were differentiated. Pyrocoelia analis (Taiwan and China) emerges throughout the year except for winter, and constitutes another lineage. We suggest that Pyrocoelia fireflies differentiated at 2 Ma to generate these three lineages. The base substitution rate for the COI gene is estimated as 4.48% Myr^–1 and that for the 28S rRNA gene is 0.394%  Myr^–1, and these rates were used in a combined BEAty analysis in BEAST.     

Highly‐enhanced larval growth during the cold season mediated by the basking behavior of the butterfly Parnassius citrinarius (Lepidoptera: Papilionidae)

Some insect species are thought to grow quickly, even in low temperatures under natural conditions, presumably by conducting basking behaviors to use sunlight. However, whether basking behavior in fact enhances developmental speed and shortens the larval period in the field has not been determined. Moreover, few studies have examined whether basking is behavioral thermoregulation or simply the result of highly‐heterogeneous heat environments in the field. To examine these issues, we conducted field observations and laboratory experiments using larvae of Parnassius citrinarius Motschulsky, which mature within a short period after the thaw in early spring. First, body temperatures of larvae were measured under sunny and cloudy conditions. Second, larval preference for warmer locations was examined. Finally, we compared the developmental speed of larvae when they basked under field conditions and when did not bask in laboratory conditions under different air temperature regimes. Under sunny conditions, larval body temperature was substantially higher than either the temperature of the host plant or the air temperature, and was equivalent to the temperature of dead leaves, which the larvae used as basking sites. In contrast, no such tendency was observed under cloudy conditions. Larvae exhibited an exclusive preference for warmer locations. Moreover, in the field, despite the low ambient temperature, larvae grew much faster than those reared in the laboratory. These results imply that the basking behavior of P. citrinarius larvae is active thermoregulation to maintain high body temperatures in the cold season.     

The heat is on: Genetic adaptation to urbanization mediated by thermal tolerance and body size

Worldwide, urbanization leads to tremendous anthropogenic environmental alterations, causing strong selection pressures on populations of animals and plants. Although a key feature of urban areas is their higher temperature (“urban heat islands”), adaptive thermal evolution in organisms inhabiting urban areas has rarely been studied. We tested for evolution of a higher heat tolerance (CT_MAX) in urban populations of the water flea Daphnia magna, a keystone grazer in freshwater ecosystems, by carrying out a common garden experiment at two temperatures (20°C and 24°C) with genotypes of 13 natural populations ordered along a well‐defined urbanization gradient. We also assessed body size and haemoglobin concentration to identify underlying physiological drivers of responses in CT_MAX. We found a higher CT_MAX in animals isolated from urban compared to rural habitats and in animals reared at higher temperatures. We also observed substantial genetic variation in thermal tolerance within populations. Overall, smaller animals were more heat tolerant. While urban animals mature at smaller size, the effect of urbanization on thermal tolerance is only in part caused by reductions in body size. Although urban Daphnia contained higher concentrations of haemoglobin, this did not contribute to their higher CT_MAX. Our results provide evidence of adaptive thermal evolution to urbanization in the water flea Daphnia. In addition, our results show both evolutionary potential and adaptive plasticity in rural as well as urban Daphnia populations, facilitating responses to warming. Given the important ecological role of Daphnia in ponds and lakes, these adaptive responses likely impact food web dynamics, top‐down control of algae, water quality, and the socio‐economic value of urban ponds.     

The influence of immune activation on thermal tolerance along a latitudinal cline

Global change is shifting both temperature patterns and the geographic distribution of pathogens, and infection has already been shown to substantially reduce host thermal performance, potentially placing populations at greater risk that previously thought. But what about individuals that are able to successfully clear an infection? Whilst the direct damage a pathogen causes will likely lead to reductions in host's thermal tolerance, the response to infection often shares many underlying pathways with the general stress response, potentially acting as a buffer against subsequent thermal stress. Here, by exposing Drosophila melanogaster to heat‐killed bacterial pathogens, we investigate how activation of a host's immune system can modify any response to both heat and cold temperature stress. In a single focal population, we find that immune activation can improve a host's knockdown times during heat shock, potentially offsetting some of the damage that would subsequently arise as an infection progresses. Conversely, immune activation had a detrimental effect on CT_max and did not influence lower thermal tolerance as measured by chill‐coma recovery time. However, we also find that the influence of immune activation on heat knockdown times is not generalizable across an entire cline of locally adapted populations. Instead, immune activation led to signals of local adaptation to temperature being lost, erasing the previous advantage that populations in warmer regions had when challenged with heat stress. Our results suggest that activation of the immune system may help buffer individuals against the detrimental impact of infection on thermal tolerance; however, any response will be population specific and potentially not easily predicted across larger geographic scales, and dependent on the form of thermal stress faced by a host.     

The life cycle of the giant water bug of northwestern Patagonian wetlands: the effect of hydroperiod and temperature regime

We analyzed the effect of hydroperiod and water temperature on the life cycle of the giant water bug Belostoma bifoveolatum in two wetlands of northwestern Patagonia, Argentina. In each wetland, we estimated adult and nymph abundance and monitored water depth and temperature throughout the study period. We determined the age structure of the giant water bug population in each wetland, and estimated the cumulative degree‐days (DD) needed for eggs to hatch and for nymphs to complete their development. Individuals of B. bifoveolatum colonized temporary wetlands at the beginning of spring when daylight lasts 12 h. The breeding period varied with hydroperiod length and showed both univoltine and bivoltine strategies, with a relatively constant breeding season. Egg‐bearing males appeared in October, carrying between 35 and 144 eggs per individual. Hatching success was high (~80% of eggs) and cumulative temperature for the hatching event was between 250 and 300 DD (which represents 3–4 weeks in nature), while complete development occurred between 800 and 1220 DD (~7–8 weeks). Individuals were more abundant in shallow and sunny patches of the wetlands, where the temperature was comparatively high, than in deeper or shaded sites. These results showed that hydroperiod duration and temperature could be good regulators of voltinism and development in B. bifoveolatum, driving the population structure of this giant water bug at the southern end of its distribution range.     

Genetic connectivity across marginal habitats: the elephants of the Namib Desert

Locally isolated populations in marginal habitats may be genetically distinctive and of heightened conservation concern. Elephants inhabiting the Namib Desert have been reported to show distinctive behavioral and phenotypic adaptations in that severely arid environment. The genetic distinctiveness of Namibian desert elephants relative to other African savanna elephant (Loxodonta africana) populations has not been established. To investigate the genetic structure of elephants in Namibia, we determined the mitochondrial (mt) DNA control region sequences and genotyped 17 microsatellite loci in desert elephants (n = 8) from the Hoanib River catchment and the Hoarusib River catchment. We compared these to the genotypes of elephants (n = 77) from other localities in Namibia. The mtDNA haplotype sequences and frequencies among desert elephants were similar to those of elephants in Etosha National Park, the Huab River catchment, the Ugab River catchment, and central Kunene, although the geographically distant Caprivi Strip had different mtDNA haplotypes. Likewise, analysis of the microsatellite genotypes of desert‐dwelling elephants revealed that they were not genetically distinctive from Etosha elephants, and there was no evidence for isolation by distance across the Etosha region. These results, and a review of the historical record, suggest that a high learning capacity and long‐distance migrations allowed Namibian elephants to regularly shift their ranges to survive in the face of high variability in climate and in hunting pressure.