Global variation in thermal tolerances and vulnerability of endotherms to climate change

The relationships among species'' physiological capacities and the geographical variation of ambient climate are of key importance to understanding the distribution of life on the Earth. Furthermore, predictions of how species will respond to climate change will profit from the explicit consideration of their physiological tolerances. The climatic variability hypothesis, which predicts that climatic tolerances are broader in more variable climates, provides an analytical framework for studying these relationships between physiology and biogeography. However, direct empirical support for the hypothesis is mostly lacking for endotherms, and few studies have tried to integrate physiological data into assessments of species'' climatic vulnerability at the global scale. Here, we test the climatic variability hypothesis for endotherms, with a comprehensive dataset on thermal tolerances derived from physiological experiments, and use these data to assess the vulnerability of species to projected climate change. We find the expected relationship between thermal tolerance and ambient climatic variability in birds, but not in mammals—a contrast possibly resulting from different adaptation strategies to ambient climate via behaviour, morphology or physiology. We show that currently most of the species are experiencing ambient temperatures well within their tolerance limits and that in the future many species may be able to tolerate projected temperature increases across significant proportions of their distributions. However, our findings also underline the high vulnerability of tropical regions to changes in temperature and other threats of anthropogenic global changes. Our study demonstrates that a better understanding of the interplay among species'' physiology and the geography of climate change will advance assessments of species'' vulnerability to climate change.     

Adaptation to host plants may prevent rapid insect responses to climate change

We must consider the role of multitrophic interactions when examining species' responses to climate change. Many plant species, particularly trees, are limited in their ability to shift their geographic ranges quickly under climate change. Consequently, for herbivorous insects, geographic mosaics of host plant specialization could prohibit range shifts and adaptation when insects become separated from suitable host plants. In this study, we examined larval growth and survival of an oak specialist butterfly (Erynnis propertius) on different oaks (Quercus spp.) that occur across its range to determine if individuals can switch host plants if they move into new areas under climate change. Individuals from Oregon and northern California, USA that feed on Q. garryana and Q. kelloggii in the field experienced increased mortality on Q. agrifolia, a southern species with low nutrient content. In contrast, populations from southern California that normally feed on Q. agrifolia performed well on Q. agrifolia and Q. garryana and poorly on the northern, high elevation Q. kelloggii. Therefore, colonization of southern E. propertius in higher elevations and some northern locales may be prohibited under climate change but latitudinal shifts to Q. garryana may be possible. Where shifts are precluded due to maladaptation to hosts, populations may not accrue warm‐adapted genotypes. Our study suggests that, when interacting species experience asynchronous range shifts, historical local adaptation may preclude populations from colonizing new locales under climate change.     

Size matters: plasticity in metabolic scaling shows body-size may modulate responses to climate change

Variability in metabolic scaling in animals, the relationship between metabolic rate (R) and body mass (M), has been a source of debate and controversy for decades. R is proportional to M^b, the precise value of b much debated, but historically considered equal in all organisms. Recent metabolic theory, however, predicts b to vary among species with ecology and metabolic level, and may also vary within species under different abiotic conditions. Under climate change, most species will experience increased temperatures, and marine organisms will experience the additional stressor of decreased seawater pH (‘ocean acidification’). Responses to these environmental changes are modulated by myriad species-specific factors. Body-size is a fundamental biological parameter, but its modulating role is relatively unexplored. Here, we show that changes to metabolic scaling reveal asymmetric responses to stressors across body-size ranges; b is systematically decreased under increasing temperature in three grazing molluscs, indicating smaller individuals were more responsive to warming. Larger individuals were, however, more responsive to reduced seawater pH in low temperatures. These alterations to the allometry of metabolism highlight abiotic control of metabolic scaling, and indicate that responses to climate warming and ocean acidification may be modulated by body-size.     

Behavioral thermoregulation in a tropical gastropod: links to climate change scenarios

Tropical species are vulnerable to global warming because they live at, or near to, their upper thermal threshold limits. Therefore, the predicted increase in the frequency of warming events in the tropics is expected to be critical for the survival of local species. This study explored the major environmental variables which were thought to be correlated with body temperatures (BTs) of the tropical snail Littoraria scabra at the niche level. A correlation between BT and substrate temperature (ST) was detected from field observations which suggests a possible causal relationship between both substrate and BTs. In contrast, there was no correlation between BT and air temperature. Field observations suggest that 33.4 °C may be L. scabra upper limit of substrate surface temperature, although further experiments are needed to assess if the upper limit of physiological tolerance is actually different. As L. scabra individuals were free to choose their substrata, the observed distribution pattern at the niche level is related to L. scabra's behavior. Additionally, substrate surface temperatures were very heterogeneous at centimeter scale (i.e. from 22.5 to 53.1 °C) and L. scabra was shown to select specific STs (i.e. between 22.5 and 33.4 °C) rather than microhabitat type. Therefore, L. scabra did not seem to behaviorally thermoregulate through microhabitat selection nor aggregation. In contrast, behavioral experiments showed that L. scabra has the ability to actively select a thermally favorable site over short temporal scale (i.e. individual average speed of 1.26 cm min^?1) following exposure to high temperatures above 33.4 °C. Hence, this study supports the crucial need to integrate intertidal invertebrate behavioral responses to thermal constraints in climate change studies.     

Arrhenius parameters of mitochondrial membrane respiratory enzymes in relation to thermoregulation in endotherms

The relationship between the body temperature (Tb), the Arrhenius critical temperature (T*), and the apparent activation energy above T* (Ea1), of liver and heart mitochondrial respiratory enzymes from eleven homeothermic and eight heterothermic species was determined using a linear regression analysis. An inverse relation was observed between T* and Ea1 during torpor and hibernation. In all thermoregulatory states, T* decreased with Tb and T* was equal to or below Tb. During torpor Ea1 increased in a linear manner as Tb was lowered. It appears that the above Arrhenius parameters are closely linked to the thermoregulatory state of endotherms and thus may represent an adaptation for function at low Tb's.     

Penguin responses to climate change in the Southern Ocean

Penguins are adapted to live in extreme environments, but they can be highly sensitive to climate change, which disrupts penguin life history strategies when it alters the weather, oceanography and critical habitats. For example, in the southwest Atlantic, the distributional range of the ice‐obligate emperor and Adélie penguins has shifted poleward and contracted, while the ice‐intolerant gentoo and chinstrap penguins have expanded their range southward. In the Southern Ocean, the El Niño‐Southern Oscillation and the Southern Annular Mode are the main modes of climate variability that drive changes in the marine ecosystem, ultimately affecting penguins. The interaction between these modes is complex and changes over time, so that penguin responses to climate change are expected to vary accordingly, complicating our understanding of their future population processes. Penguins have long life spans, which slow microevolution, and which is unlikely to increase their tolerance to rapid warming. Therefore, in order that penguins may continue to exploit their transformed ecological niche and maintain their current distributional ranges, they must possess adequate phenotypic plasticity. However, past species‐specific adaptations also constrain potential changes in phenology, and are unlikely to be adaptive for altered climatic conditions. Thus, the paleoecological record suggests that penguins are more likely to respond by dispersal rather than adaptation. Ecosystem changes are potentially most important at the borders of current geographic distributions, where penguins operate at the limits of their tolerance; species with low adaptability, particularly the ice‐obligates, may therefore be more affected by their need to disperse in response to climate and may struggle to colonize new habitats. While future sea‐ice contraction around Antarctica is likely to continue affecting the ice‐obligate penguins, understanding the responses of the ice‐intolerant penguins also depends on changes in climate mode periodicities and interactions, which to date remain difficult to reproduce in general circulation models.     

Community and ecosystem responses to recent climate change

There is ample evidence for ecological responses to recent climate change. Most studies to date have concentrated on the effects of climate change on individuals and species, with particular emphasis on the effects on phenology and physiology of organisms as well as changes in the distribution and range shifts of species. However, responses by individual species to climate change are not isolated; they are connected through interactions with others at the same or adjacent trophic levels. Also from this more complex perspective, recent case studies have emphasized evidence on the effects of climate change on biotic interactions and ecosystem services. This review highlights the ‘knowns’ but also ‘unknowns’ resulting from recent climate impact studies and reveals limitations of (linear) extrapolations from recent climate-induced responses of species to expected trends and magnitudes of future climate change. Hence, there is need not only to continue to focus on the impacts of climate change on the actors in ecological networks but also and more intensively to focus on the linkages between them, and to acknowledge that biotic interactions and feedback processes lead to highly complex, nonlinear and sometimes abrupt responses.     

Disentangling root responses to climate change in a semiarid grassland

Future ecosystem properties of grasslands will be driven largely by belowground biomass responses to climate change, which are challenging to understand due to experimental and technical constraints. We used a multi-faceted approach to explore single and combined impacts of elevated CO₂ and warming on root carbon (C) and nitrogen (N) dynamics in a temperate, semiarid, native grassland at the Prairie Heating and CO₂ Enrichment experiment. To investigate the indirect, moisture mediated effects of elevated CO₂, we included an irrigation treatment. We assessed root standing mass, morphology, residence time and seasonal appearance/disappearance of community-aggregated roots, as well as mass and N losses during decomposition of two dominant grass species (a C₃ and a C₄). In contrast to what is common in mesic grasslands, greater root standing mass under elevated CO₂ resulted from increased production, unmatched by disappearance. Elevated CO₂ plus warming produced roots that were longer, thinner and had greater surface area, which, together with greater standing biomass, could potentially alter root function and dynamics. Decomposition increased under environmental conditions generated by elevated CO₂, but not those generated by warming, likely due to soil desiccation with warming. Elevated CO₂, particularly under warming, slowed N release from C₄—but not C₃—roots, and consequently could indirectly affect N availability through treatment effects on species composition. Elevated CO₂ and warming effects on root morphology and decomposition could offset increased C inputs from greater root biomass, thereby limiting future net C accrual in this semiarid grassland.     

Variable responses to large-scale climate change in European Parus populations

Spring temperatures in temperate regions have increased over the past 20 years and many organisms have responded to this increase by advancing the timing of their growth and reproduction. However, not all populations show an advancement of phenology. Understanding why some populations advance and others do not will give us insight into the possible constraints and selection pressures on the advancement of phenology. By combining two decades of data on 24 populations of tits (Parus sp.) from six European countries, we show that the phenological response to large-scale changes in spring temperature varies across a species' range, even between populations situated close to each other. We show that this variation cannot be fully explained by variation in the temperature change during the pre- and post-laying periods, as recently suggested. Instead, we find evidence for a link between rising temperatures and the frequency of second broods, which results in complex shifts in the laying dates of first clutches. Our results emphasize the need to consider links between different life-history parameters in order to predict the ecological consequences of large-scale climate changes.     

Dispersal and species’ responses to climate change

Dispersal is fundamental in determining biodiversity responses to rapid climate change, but recently acquired ecological and evolutionary knowledge is seldom accounted for in either predictive methods or conservation planning. We emphasise the accumulating evidence for direct and indirect impacts of climate change on dispersal. Additionally, evolutionary theory predicts increases in dispersal at expanding range margins, and this has been observed in a number of species. This multitude of ecological and evolutionary processes is likely to lead to complex responses of dispersal to climate change. As a result, improvement of models of species’ range changes will require greater realism in the representation of dispersal. Placing dispersal at the heart of our thinking will facilitate development of conservation strategies that are resilient to climate change, including landscape management and assisted colonisation. Synthesis This article seeks synthesis across the fields of dispersal ecology and evolution, species distribution modelling and conservation biology. Increasing effort focuses on understanding how dispersal influences species' responses to climate change. Importantly, though perhaps not broadly widely‐recognised, species' dispersal characteristics are themselves likely to alter during rapid climate change. We compile evidence for direct and indirect influences that climate change may have on dispersal, some ecological and others evolutionary. We emphasise the need for predictive modelling to account for this dispersal realism and highlight the need for conservation to make better use of our existing knowledge related to dispersal.     

Phenological responses of plants to climate change in an urban environment

Global climate change is likely to alter the phenological patterns of plants due to the controlling effects of climate on plant ontogeny, especially in an urbanized environment. We studied relationships between various phenophases (i.e., seasonal biological events) and interannual variations of air temperature in three woody plant species (Prunus davidiana, Hibiscus syriacus, and Cercis chinensis) in the Beijing Metropolis, China, based on phenological data for the period 1962–2004 and meteorological data for the period 1951–2004. Analysis of phenology and climate data indicated significant changes in spring and autumn phenophases and temperatures. Changes in phenophases were observed for all the three species, consistent with patterns of rising air temperatures in the Beijing Metropolis. The changing phenology in the three plant species was reflected mainly as advances of the spring phenophases and delays in the autumn phenophases, but with strong variations among species and phenophases in response to different temperature indices. Most phenophases (both spring and autumn phenophases) had significant relationships with temperatures of the preceding months. There existed large inter- and intra-specific variations, however, in the responses of phenology to climate change. It is clear that the urban heat island effect from 1978 onwards is a dominant cause of the observed phenological changes. Differences in phenological responses to climate change may cause uncertain ecological consequences, with implications for ecosystem stability and function in urban environments.     

Why climate change will invariably alter selection pressures on phenology

The seasonal timing of lifecycle events is closely linked to individual fitness and hence, maladaptation in phenological traits may impact population dynamics. However, few studies have analysed whether and why climate change will alter selection pressures and hence possibly induce maladaptation in phenology. To fill this gap, we here use a theoretical modelling approach. In our models, the phenologies of consumer and resource are (potentially) environmentally sensitive and depend on two different but correlated environmental variables. Fitness of the consumer depends on the phenological match with the resource. Because we explicitly model the dependence of the phenologies on environmental variables, we can test how differential (heterogeneous) versus equal (homogeneous) rates of change in the environmental variables affect selection on consumer phenology. As expected, under heterogeneous change, phenotypic plasticity is insufficient and thus selection on consumer phenology arises. However, even homogeneous change leads to directional selection on consumer phenology. This is because the consumer reaction norm has historically evolved to be flatter than the resource reaction norm, owing to time lags and imperfect cue reliability. Climate change will therefore lead to increased selection on consumer phenology across a broad range of situations.     

Plant metabolomics for plant chemical responses to belowground community change by climate change

General circulation models on global climate change predict increase in surface air temperature and changes in precipitation. Increases in air temperature (thus soil temperature) and altered precipitation are known to affect the species composition and function of soil microbial communities. Plant roots interact with diverse soil organisms such as bacteria, protozoa, fungi, nematodes, annelids and insects. Soil organisms show diverse interactions with plants (eg. competition, mutualism and parasitism) that may alter plant metabolism. Besides plant roots, various soil microbes such as bacteria and fungi can produce volatile organic compounds (VOCs), which can serve as infochemicals among soil organisms and plant roots. While the effects of climate change are likely to alter both soil communities and plant metabolism, it is equally probable that these changes will have cascading consequnces for grazers and subsequent food web components aboveground. Advances in plant metabolomics have made it possibile to track changes in plant metabolomes as they respond to biotic and abiotic environmental changes. Recent developments in analytical instrumentation and bioinformatics software have established metabolomics as an important research tool for studying ecological interactions between plants and other organisms. In this review, we will first summarize recent progress in plant metabolomics methodology and subsequently review recent studies of interactions between plants and soil organisms in relation to climate change issues.     

Adaptive responses to cool climate promotes persistence of a non-native lizard

Successful establishment and range expansion of non-native species often require rapid accommodation of novel environments. Here, we use common-garden experiments to demonstrate parallel adaptive evolutionary response to a cool climate in populations of wall lizards (Podarcis muralis) introduced from southern Europe into England. Low soil temperatures in the introduced range delay hatching, which generates directional selection for a shorter incubation period. Non-native lizards from two separate lineages have responded to this selection by retaining their embryos for longer before oviposition—hence reducing the time needed to complete embryogenesis in the nest—and by an increased developmental rate at low temperatures. This divergence mirrors local adaptation across latitudes and altitudes within widely distributed species and suggests that evolutionary responses to climate can be very rapid. When extrapolated to soil temperatures encountered in nests within the introduced range, embryo retention and faster developmental rate result in one to several weeks earlier emergence compared with the ancestral state. We show that this difference translates into substantial survival benefits for offspring. This should promote short- and long-term persistence of non-native populations, and ultimately enable expansion into areas that would be unattainable with incubation duration representative of the native range.     

Intra- and interspecific facilitation in mangroves may increase resilience to climate change threats

Mangroves are intertidal ecosystems that are particularly vulnerable to climate change. At the low tidal limits of their range, they face swamping by rising sea levels; at the high tidal limits, they face increasing stress from desiccation and high salinity. Facilitation theory may help guide mangrove management and restoration in the face of these threats by suggesting how and when positive intra- and interspecific effects may occur: such effects are predicted in stressed environments such as the intertidal, but have yet to be shown among mangroves. Here, we report the results of a series of experiments at low and high tidal sites examining the effects of mangrove density and species mix on seedling survival and recruitment, and on the ability of mangroves to trap sediment and cause surface elevation change. Increasing density significantly increased the survival of seedlings of two different species at both high and low tidal sites, and enhanced sediment accretion and elevation at the low tidal site. Including Avicennia marina in species mixes enhanced total biomass at a degraded high tidal site. Increasing biomass led to changed microenvironments that allowed the recruitment and survival of different mangrove species, particularly Ceriops tagal.     

Contrasting responses of migration strategies in two European thrushes to climate change

Migration is a widespread strategy that enables animals to escape harsh winter conditions. It has been well documented that migration phenology in birds is changing in response to recent climate warming in the northern hemisphere. Despite the existence of large temporal and geographical scale ringing data on birds in Europe, changes in migration strategies in relation to climate warming have not been well studied, mainly because of a lack of appropriate statistical methods. In this paper, we develop a method that enables us to investigate temporal changes in migration strategies from recoveries of dead ringed birds. We estimated migration probability as the ratio between recovery probabilities of conspecific birds originating from different countries but potentially wintering in the same country. We applied this method to two European thrushes: the entirely migrant redwing Turdus iliacus , and the partially migrant blackbird T. merula . We tested for an immediate and a 1-year lagged relationship between our migration probability and climatic covariates (i.e. mean winter temperature in France and the North Atlantic Oscillation). Using ringing-recovery data collected in Finland, Germany, Switzerland and France from 1970 to 1999, we detected contrasting responses in these two species, likely related to their different migratory behaviours. Both species showed a decline in the probability for northern and eastern birds to winter in France. The entirely migratory redwing exhibited a year-to-year plastic response to climate, whereas the decline in the partially migrant blackbird was smooth, suggesting underlying genetic processes. The proposed method, thus, allows us to identify useful indicators of climatic impacts on migration strategies, as well as highlighting differences between closely related species.     

Genetic and plastic responses of a northern mammal to climate change

Climate change is predicted to be most severe in northern regions and there has been much interest in to what extent organisms can cope with these changes through phenotypic plasticity or microevolutionary processes. A red squirrel population in the southwest Yukon, Canada, faced with increasing spring temperatures and food supply has advanced the timing of breeding by 18 days over the last 10 years (6 days per generation). Longitudinal analysis of females breeding in multiple years suggests that much of this change in parturition date can be explained by a plastic response to increased food abundance (3.7 days per generation). Significant changes in breeding values (0.8 days per generation), were in concordance with predictions from the breeder's equation (0.6 days per generation), and indicated that an evolutionary response to strong selection favouring earlier breeders also contributed to the observed advancement of this heritable trait. The timing of breeding in this population of squirrels, therefore, has advanced as a result of both phenotypic changes within generations, and genetic changes among generations in response to a rapidly changing environment.     

Complex life cycles and the responses of insects to climate change

Many organisms have complex life cycles with distinct life stages that experience different environmental conditions. How does the complexity of life cycles affect the ecological and evolutionary responses of organisms to climate change? We address this question by exploring several recent case studies and synthetic analyses of insects. First, different life stages may inhabit different microhabitats, and may differ in their thermal sensitivities and other traits that are important for responses to climate. For example, the life stages of Manduca experience different patterns of thermal and hydric variability, and differ in tolerance to high temperatures. Second, life stages may differ in their mechanisms for adaptation to local climatic conditions. For example, in Colias, larvae in different geographic populations and species adapt to local climate via differences in optimal and maximal temperatures for feeding and growth, whereas adults adapt via differences in melanin of the wings and in other morphological traits. Third, we extend a recent analysis of the temperature-dependence of insect population growth to demonstrate how changes in temperature can differently impact juvenile survival and adult reproduction. In both temperate and tropical regions, high rates of adult reproduction in a given environment may not be realized if occasional, high temperatures prevent survival to maturity. This suggests that considering the differing responses of multiple life stages is essential to understand the ecological and evolutionary consequences of climate change.     

Idiosyncratic species effects confound size-based predictions of responses to climate change

Understanding and predicting the consequences of warming for complex ecosystems and indeed individual species remains a major ecological challenge. Here, we investigated the effect of increased seawater temperatures on the metabolic and consumption rates of five distinct marine species. The experimental species reflected different trophic positions within a typical benthic East Atlantic food web, and included a herbivorous gastropod, a scavenging decapod, a predatory echinoderm, a decapod and a benthic-feeding fish. We examined the metabolism–body mass and consumption–body mass scaling for each species, and assessed changes in their consumption efficiencies. Our results indicate that body mass and temperature effects on metabolism were inconsistent across species and that some species were unable to meet metabolic demand at higher temperatures, thus highlighting the vulnerability of individual species to warming. While body size explains a large proportion of the variation in species'' physiological responses to warming, it is clear that idiosyncratic species responses, irrespective of body size, complicate predictions of population and ecosystem level response to future scenarios of climate change.