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Responses of large mammals to climate change

Responses of large mammals to climate change Review Temperature 1:2, 115–127; July/August/September 2014; © 2014 Landes Bioscience Responses of large mammals to climate change 1, 1 1,2 1,2 Robyn S Hetem *, Andrea Fuller , Shane K Maloney , and Duncan Mitchell Brain Function Research Group; School of Physiology; University of the w itwatersrand; Faculty of Health Science; Parktown, South Africa; School of Anatomy, Physiology, and Human Biology; University of w estern Australia; Crawley, Australia Keywords: climate change physiology, phenotypic plasticity, physiological acclimation, behavioral f lexibility, range shift, microevolution, temperature Most large terrestrial mammals, including the charismatic species so important for ecotourism, do not have the luxury of rapid micro-evolution or sufficient range shifts as strategies for adjusting to climate change. The rate of climate change is too fast for genetic adaptation to occur in mammals with longevities of decades, typical of large mammals, and land- scape fragmentation and population by humans too widespread to allow spontaneous range shifts of large mammals, leaving only the expression of latent phenotypic plasticity to counter effects of climate change. The expression of pheno- typic plasticity includes anatomical variation within the same species, changes in phenology, and employment of intrin- sic physiological and behavioral capacity that can buffer an animal against the effects of climate change. w hether that buffer will be realized is unknown, because little is known about the efficacy of the expression of plasticity, particularly for large mammals. Future research in climate change biology requires measurement of physiological characteristics of many identified free-living individual animals for long periods, probably decades, to allow us to detect whether expres- sion of phenotypic plasticity will be sufficient to cope with climate change. Introduction sensitivity to environmental change, its resilience to perturbations and its potential to adapt to change’. Vulnerable species or ani- The 2013 Intergovernmental Panel on Climate Change mal populations have only three options when faced with climate synthesis report predicts an increase in global temperatures of change. First, they may shift their distribution range, to habitats between 1.5 °C and 4.5 °C during the 21st Century, which will where the climate is within the species’ tolerance limits. Second, take us to the warmest global climate in more than two million they may remain in a location but adjust to new climatic regimes years. Although the rate of the current warming episode probably either through a change in the genetic composition of a popu- does not exceed the normal background rate of climate change, lation or by phenotypic plasticity, which results in a different continued warming over the next few decades will exceed the phenotype from an existing genotype via changes in epigenetic 2 9 background rate of change by more than an order of magnitude. control of gene expression. Either of these outcomes may bring The rate of future climate change will be unprecedented in the about changes in the timing of events (phenology), anatomical Earth’s history. It probably will be that rate of climate change, variation (e.g., color patterns, body shape and size), or changes rather than the eventual magnitude or duration of the episode, in the behavior or physiology of a species, which could reduce 4 10 that will prove to be critical for biota. Indeed, the typical rate of the impact of climate change. Finally, if neither range shifts nor niche evolution that has been observed in more than 500 species adjustment is possible, global or local extinction (extirpation) is about 10 000 times slower than the rate that will be required may result. Whatever options are realized, climate change will 5 11-14 to keep track with climate change projections for 2100. Though have a significant impact on biodiversity, and current conser- worse is to come, it is delusional to envisage climate change only vation strategies, which attempt to conserve communities and 15-18 as a future challenge. Its biological consequences already are evi- ecosystems as they exist, will be unsustainable. dent. Of the nearly 30 000 documented trends in physical sys- For many large mammals, especially those living in human- tems and biological characteristics of plants and animals between dominated landscapes, range shifts are unlikely options for 1970 and 2004, 90% have been in the direction consistent with coping with climate change. Because the research has not been environmental temperature increases. done, we do not know whether large mammals can express suf- According to Huey et al. ‘the vulnerability of a species to ficient genetic shifts or phenotypic plasticity to adjust to the cur- environmental change depends on the species’ exposure and rent climate change event. We do know that large mammals are *Correspondence to: Robyn S Hetem; Email: robyn.hetem@wits.ac.za Submitted: 06/16/2014; Revised: 7/15/2014; Accepted: 07/19/2014; Published Online: 07/21/2014 http://dx.doi.org/10.4161/temp.29651 www.landesbioscience.com Temperature 115 more likely to be adversely effected by climate change than their smaller counterparts. Here we review what we do know, and need to know, about the possible responses of large terrestrial mammals. We contextualize our discussion of large mammals within established principles of climate change biology. Extinction Global warming has been a common occurrence on Earth for the last 3.5 billion years. Modeling of the current episode predicts a temperature rise of the same order of magnitude as that evident at the end of the Permian, when mass volcanism increased global temperatures by 6 °C and resulted in the extinc- tion of nearly 95% of species. We cannot be sure that it was the warming that was responsible for all of those extinctions, but the fossil record is unequivocal that extinction and extirpation have been common outcomes for species facing past climate change events of comparable magnitude. A pivotal study by Thomas et Figure  1. Small map: Observed current distribution of the scimitar- al. predicted that, under mid-range climate change scenarios, a horned oryx (Oryx dammah). Large map: Predicted habitat distribution quarter of terrestrial plants and animals may be extinct by 2050. for the scimitar-horned oryx in 2050. Light gray indicates habitats that are presently climatically suitable but are predicted to be unsuitable in By extrapolating such predictions to a global scale, the authors 2050. Moderate gray indicates habitats that are presently climatically predicted that well over one million species, among which will suitable that are predicted to remain suitable in 2050. Dark gray indicates be many large terrestrial mammal species, could be threatened habitats that are presently climatically unsuitable that are predicted to with extinction as a result of climate change. Their models pre- 22 be suitable by 2050 (adapted from Thuiller et al. ). dict that 45% of terrestrial species are likely to be committed to extinction by 2050 if their dispersal is limited. Among the large terrestrial mammals seemingly destined to examined have shifted their range into adjacent habitats between become extinct are the charismatic species so important for eco- 1970 and 2000, presumably in response to climate change. tourism. Africa is rich in such species, and serves as an example Observed range shifts averaged 11 m per decade upwards and of the future likely under climate change; 25–40% of a repre- nearly 17 km per decade polewards, with range shifts correlat- sentative sample of 277 of its mammalian species is likely to be ing positively with the rate of warming. Global meta-analyses critically endangered or extinct by 2080. The charismatic spe- have revealed that 80% of range shifts have been consistent with 24,28,29 cies of South Africa are likely to be particularly vulnerable to climate change predictions. However, the recorded shifts climate change, as will be large mammals in human-dominated include few, if any, large mammals. landscapes elsewhere, because the consequences of high human Shifting range in response to climate change requires suitable population density will prevent their dispersal. The extinction new habitats to be accessible, and for the required traveling dis- risk of South African mammals is estimated to be as high as 69% tances to be within the capacity of the species that is shifting by 2050. Indeed, long-term population monitoring in the coun- range. The rapid rate of climate change will mean that nearly try’s f lagship Kruger National Park already has revealed declines 10% of mammals in the western hemisphere will be unable to 23 30 in seven out of 11 ungulate species between 1977 and 1996. move fast enough to keep pace with projected climate changes. A salutary example of unattainability of the required pace is the Range Shifts scimitar-horned oryx (Oryx dammah, Fig. 1). To track its suit- able climate, this species would have had to move thousands of Although large mammals in fragmented, human-dominated kilometers, from the Sahel to the Kalahari Desert, an impossible habitats, like those prevailing in South Africa, will be precluded shift without human assistance. The species has become extinct from shifting to a new habitat in response to current climate in what was its current natural habitat in the last decade. In cir- change, large mammals in more-pristine habitats such as bears in cumstances in which natural range shifts are not feasible, either northern Canada, and smaller mammals every where, may be able as a result of unattainable traveling distances or loss of habitat to track suitable climates. In the temperate zone, for example, a 1 connectivity, assisted colonization may provide a conservation 31,32 °C increase in mean annual temperature corresponds to a shift in option. Yet, moving species to areas where they do not cur- 24,25 isotherms of ~160 km in latitude or 160 m in elevation. Thus, rently occur is not without risk. The introduced species can carry biota that can do so, including mammals, are expected to follow disease, displace native species and thereby challenge ecosystem the shifting climatic zones and move polewards in latitude and stability or alter the genetic structure of local populations. An in- 17,26 upwards in elevation. Numerous recent reports have docu- depth knowledge of species’ biology and accurate climate change mented shifts in the geographical distribution of extant biota (for predictions is required before assisted colonization can become a 33,34 reviews see refs. 24, 27, and 28). More than half of the species routine conservation option. 116 Temperature volume 1 issue 1 For assisted colonization to be a feasible conservation option attempted to incorporate physiological factors to address the cli- 60,61 62,63 for a species, we need an understanding of the fundamental matic tolerances of terrestrial ectotherms and mammals, niche (where species can occur) and realized niche (where species but they require an understanding of species’ physiological 64-66 do occur), and the likely location of those niches in the future. responses to climate, an understanding that we are far from Bioclimatic envelope, or niche-based, models are static models having attained for most species. Although these physiologically- that correlate current species distributions with climate variables tuned models still have limitations, for example in not taking and project future distributions according to each species’ “cli- non-climatic factors into account, they are likely to be more 35-37 matic envelope” . Some models were developed sufficiently robust than those bioclimatic envelope models that are based long ago for their predictions to be tested against actual observa- only on correlations between observed distributions and current 45,67,68 tions, and they have proved their value. For example, in a meta- climate variables. analysis of range shifts, latitudinal shifts matched the expected Micro-Evolution range shifts if a species were to track its bioclimatic envelope. While of proven utility, the assumptions on which these mod- els are based can be questioned regarding their ability to predict Future extinction risk is likely to be overestimated if species 38-41 the potential impact of climate change. Bioclimatic enve- exhibit adaptive genotypic changes in response to environmental lope models typically do not address stochastic events like local change. Evolutionary change often is considered too slow, given droughts and heat waves, which may impose the dominant cli- the rate of the climate change event, to allow genetic adaptation, 42,43 3,4 mate stress on species in the future. They also do not address but is likely to have accompanied range shifts in the past. A spatial variability. It is the microclimate experienced by an ani- changing climate moves the so-called “fitness optimum” for 44-47 3,4 mal that has direct influence on an animal’s thermal status. different populations throughout the species range, making All thermal aspects of those microclimates need to be quantified the fundamental niche flexible over time. Range shifts already before they can be incorporated into climate change models. are having genetic consequences in the current event. By mix- Although they do not incorporate measures of evaporation, min- ing populations that are shifting, a range shift increases genetic iature black globe thermometers can be attached to large mam- variation, thereby increasing the population’s chance of adapting mals to provide a quantitative measurement of heat loads of their to changing conditions. Northwards range shifts in the northern microclimates. hemisphere, for example, may have the advantage of introduc- Another shortfall of current bioclimatic envelope models is ing genotypes that are better adapted to warmer conditions, thus that they do not account for non-climatic influences on spe- promoting the adaptation of existing cooler-adapted populations 69,70 cies’ distributions, such as terrain and biotic interactions (but see to climate change. Conversely, range shifts also can decrease ref. 49). Climate-induced species interactions are likely to have genetic variability that has occurred historically as a result of out- 50,51 important consequences for future species distributions. For breeding of distinct populations. For example, climate change example, the climate-driven northward range expansion of the may result in genetic mixing among subspecies of the black bear, red fox (Vulpes vulpes) has been associated with a decrease in the which could inhibit or even reverse sub-speciation. distribution range of the arctic fox (Alopex lagopus) as a result of The genetic adaptation that will be required to survive cli- 52 70,72 3,73,74 an increased interspecific competition. Since individual plant mate change is not the slow process of speciation, but and animal species differ in their response to changing climatic heritable shifts in allele frequencies in a population (without spe- conditions, species may shift their ranges independently of each ciation) known as “micro-evolution”. Micro-evolution already 75,76 other, resulting in changes in community structure and possi- has occurred, in directions predicted by climate change, par- 26,53-55 bly in ecosystem disruption. For example, decreased rain- ticularly for short-lived species with fast generation times (for fall altered the plant community and ultimately led to a decline examples, see refs. 77-82). Surprisingly, there have been shifts in desert bighorn sheep (Ovis canadensis nelsoni) population in in genetic variability even in populations of the relatively long- California. These species interactions thus need to be incorpo- lived Canadian lynx (Lynx canadensis) that have been associated rated into bioclimatic envelope models to better predict future with snow depth and winter precipitation. It remains uncertain, species distributions, which is the aim of a new scope of ecologi- though, whether micro-evolution can result in a change in the 58 84 cal research termed “global change ecology” . climate tolerance of any species sufficient to prevent extinction. We and others believe, however, that the major limitation A morphological feature related to climate tolerance that is of predictions derived from bioclimatic envelope models is the determined genetically is an animal’s coat color. Analyses by assumption that species lack sufficient phenotypic plasticity to Maloney et al. support the view that progressive increases in adjust to climates beyond those in which they occur currently. ambient temperature explain the recent 20-y shift in the ratio of Models typically assume, for each species, that the realized niche dark to light-colored Soay sheep on the archipelago of St Kilda, is the fundamental niche: the species occupies today all habi- United Kingdom, contrary to the original explanation based on 86,87 tats fulfilling the thermal conditions that it can tolerate, and it an association of coat color with body mass. The advantage therefore cannot survive at a current habitat if conditions depart enjoyed historically by dark-colored sheep in absorbing solar from those in which that species survives now. Yet, plasticity may radiation better would carry less benefit in warmer environ- allow animals to adjust to changing climatic conditions without ments. Similarly, there is thermoregulatory significance of pelt changing their location. Some bioclimatic envelope models have color for springbok (Antidorcas marsupialis), with black springbok www.landesbioscience.com Temperature 117 96 97 2 °C and a decrease in precipitation. Réale et al. cal- culated that 13% of the observed phenological changes in parturition date could be attributed to micro-evolu- tion. However, since the investigators initially did not account for systematic environmental variation across years, even that 13% may be an overestimate of the role of genetic change. Potentially, more than 60% of the observed changes in parturition date of the squirrel must be attributed to phenotypic plasticity. Short-lived mammalian species, like the red squirrel, have the advantage of fast generation times, which may improve their chance of survival as each generation pro- 70,77,78,99,100 vides scope for micro-evolution. Conversely, large mammals with long generation times, and indeed those small mammal species, like bats, which have long generation times, are predicted to have less ability to respond genetically to any new selective pressures, making them more susceptible to extinction than are species with short generation times. The issue is compounded because large species have greater range requirements. There are many species of mammals with longevities such that individuals alive now ought Figure  2. The pelt color variations of the black, common and white springbok. still to be alive in 2030, and a few species for which Nychthemeral rhythm of body temperature (mean ± SD) for four black (red line), individuals alive now could be alive in 2100. Clearly, seven common (blue line) and four white (yellow line) springbok during a hot (A) the survival of those individuals, and probably those and cold (B) season. Black bars represent night periods (adapted from Hetem et 88 species, cannot depend on genetic adaptation. Instead, al. ). for those that also cannot shift their ranges, survival is likely to be entirely dependent on sufficient phenotypic benefiting, compared with their white conspecifics, by being plasticity to buffer effects of climate change. able to reduce metabolic costs in winter, as a result of increased Phenotypic Plasticity absorption of solar radiation (Fig. 2B). Increased absorption of solar radiation, however, may disadvantage the black springbok in the heat (Fig. 2A). As with the Soay sheep, we expect the black By definition, phenotypic plasticity is the process by which a color morphs to decline as their habitats warm, if populations are single genotype gives rise to different phenotypes in different cir- 104-106 left unmanaged. cumstances. The plasticity is known as an epigenetic effect. Although coat color has a genetic basis amenable to micro- Phenotypic plasticity in animals exposed to a change in environ- evolution in populations of mixed color morphs, and numerous ment may involve acclimation, acclimatization, and learning studies have interpreted such anatomical changes as micro-evolu- and can take place through phenology, developmental plasticity, tionary responses to climate change, the majority of studies have physiological adjustments and behavioral flexibility. Unlike provided no evidence that the observed changes have a genetic genetic adaptation, phenotypic plasticity allows the animal 89,90 basis. There is a general lack of evidence for or against genetic itself, rather than its future lineage (except in the case of mater- adaptations to climate change, resulting at least partially because nal effects; see below), to respond to environmental change. molecular techniques remain inadequate to properly reveal how The mechanism of plasticity can involve changes to the way that 91,92 genetic sequences relate to ecologically important traits, an DNA is packaged in the nucleus and alters the probability of a 93 9 inadequacy that is hopefully temporary. However, methods to particular gene being expressed. The best known mechanisms quantify a genetic component of adjustment to climate change of epigenetics are DNA methylation, histone modification, and are likely to remain difficult to implement, especially in long- more recently it has become obvious that small non-coding lived mammals. To date, there have been only 12 studies pub- RNA’s have both transcriptional effects on gene expression and lished that have tested for the genetic basis of climate-related post-transcriptional effects that alter the fate of the RNA from biological changes in mammals, and only one of these found gene transcription, prior to translation into RNA. evidence for a genetically-based response. The most convinc- Phenological changes ing example of micro-evolutionary response to climate change In addition to estimating the contribution of micro-evolution, is a short-lived mammal, the North American red squirrel the red squirrel study provided the first measurement of the role (Tamiasciurus hudsonicus), in Yukon from 1989 to 2001, a period of phenotypic plasticity in climate-induced development of a over which mean lifetime parturition date advanced by six days functional trait, but it was not the first to document changes per generation, associated with a mean spring temperature rise of in phenology, that is the timing of seasonal events, in response to 118 Temperature volume 1 issue 1 changing climatic conditions (see refs. 17,24,26,28,109). It still is pronghorn and may ultimately lead to a life-history strategy of the case that most known examples of phenotypic changes linked faster development. Similarly, the Soay sheep mentioned above to climate change relate to phenology. For example, in response are also breeding at an earlier age as their climate warms, result- to progressive environmental change over a 28-y period on the ing in a general decrease in mean body size in that population. Isle of Rum, United Kingdom, red deer (Cervus elaphus) have Anatomical variation displayed phenotypic plasticity in the phenological traits of estrus Although the majority of reports of phenotypic responses to date, parturition date, antler cast and clean date and the start and climate change, adaptive or not, relate to phenology, there are end of the rut, with most of the variation being attributable to reports relating to other traits. A decline in body mass is con- earlier plant growth. sidered the third universal response (after phenology and range When phenological changes are observed, they often are taken shifts) to warming associated with climate change. The rela- as evidence that species are adjusting to changing environmen- tionship between body mass and thermoregulation is complex. tal conditions in ways that help mitigate the effects of climate Relative to animals of larger body mass, animals of the same change. Yet the responses in nearly half of a set of studies report- shape with lower body mass, for geometric reasons, have a higher ing phenotypic changes in phenology, body mass, or litter size surface area-to-mass ratio, and therefore have more difficulty in mammals actually were associated with a decline in fitness. preventing body heat loss in cold environments. That physical For example, the advanced breeding of Chillingham cattle (Bos relationship is congruent with Bergmann’s rule that predicts a primigenius taurus) in response to warming led to more calves positive correlation between the body mass of terrestrial endo- being born in winter, which resulted in an increase in calf mor- therms and latitude, and, by inference, an inverse correlation tality. The responses in only one third of the studies qualified between body mass and environmental temperature. With as adaptive phenotypic changes in phenology on the criterion global warming, species with lower body mass would lose that that both the direction and the rate of change were appropriate. disadvantage progressively, so a relative increase in proportion of Because species may show rates of phenological change different smaller animals would be expected in a warmer world. There to those of other species on which they depend, asynchrony or a are some data supporting that expectation. As mentioned, over 17,112-114 mistiming of key ecological events can result. For example, a 20-y period of progressive winter warming, the average body the calving date of caribou (Rangifer tarandus) on Greenland has mass of the Soay sheep on St. Kilda has declined between ~0.3% been advancing more slowly, with warming, than has the onset (senescents) and ~0.8% (yearlings) of mean body mass per year. of plant growth, creating a trophic mismatch and increasing calf The proposed mechanism is that the milder winters resulted in mortality. Numerous studies have demonstrated the ecologi- less reliance on fat reserves, which in turn enables more of the 112,116 120 cal and metabolic costs of such mistimed ecological events, small individuals to survive the winter. However, a decline in which ultimately may lead to a decrease in biodiversity. body mass does not appear to be a universal response of mam- One possible cause of mismatch between phenological mals to climate change. Data from museum specimens collected responses in connected species is the different environmental during the last quarter of the twentieth century reveal that body cues to which different species respond. Whereas most plants size of otters (Lutra lutra) in Norway has increased, presumably and insects respond to seasonal changes in temperature, most as a result of increased food availability. Indeed, only 7% of vertebrate species are more sensitive to changes in photoperiod, recently-observed changes in mammalian body masses provide although, as was the case for red deer on Rum, better nutrition support for an advantage to smaller mammals. Also, the physi- can also advance reproductive events. Thus, those vertebrates cal principles outlined above have a reverse effect when ambient with a photoperiod-sensitive reproductive cycle that remain at temperature exceeds body temperature, a situation which will their historic locations may face a mismatch between reproduc- become increasingly common with climate change. There the tion and food availability, while those dispersing latitudinally higher surface area-to-mass ratio increases environmental heat will have to adjust to an unfamiliar annual cycle of photoperiod load. In those environments, thermal balance also will depend 70,76 in their new habitat. Those species that are unable to match on the capacity for evaporative cooling, which may be unrelated the timing of key life-history events to the phenology of the to body mass. Despite a 4-fold difference in body mass between species on which they depend will be forced to show plasticity Arabian oryx (Oryx leucoryx) and Arabian sand gazelle (Gazella in other life-history traits if they are to maintain their lifetime subgutturosa marica), both species showed an increased amplitude reproductive success. For example, flexibility in phenology of of body temperature rhythm (increased heterothermy) when they the Antarctic fur seal (Arctocephalus gazelle) is important in their were exposed to the same extreme heat and aridity (Fig. 3). highly variable thermal environment but is limited because of the Although understanding the physiological mechanisms is 70,113 long interval between conception and weaning of the pups. As essential for predicting responses to climate change, a dispro- their environment warms the female Antarctic fur seals appear portional number (> 80%) of studies of phenotypic responses to to be adapting their life cycles by not breeding in years of low climate change has focused on anatomical plasticity, with fewer 118 125 krill supply, thus increasing adult survival and fitness. Another studies on physiological and behavioral responses. Such pre- species that is changing its life-history strategy in response to sto- ponderance may reflect the ease of measurement of anatomical chastic environmental conditions is the pronghorn (Antilocapra features like body mass. Gathering physiological and behavioral americana). Frequent severe weather events result in an increase data, on the other hand, is labor-intensive and requires long peri- in male mortality, which favors precocial maturation in male ods of observation and monitoring. Given that natural selection www.landesbioscience.com Temperature 119 Figure  3. Nychthemeral rhythm of body temperature (mean ± SD) for Figure  4. Nychthemeral rhythm of activity for five Arabian oryx dur- five free-living Arabian oryx (gray line) and four free-living Arabian sand ing both the warm wet (A) and hot dry (B) periods. Oryx shifted from gazelle (black line) during both the warm wet (A) and hot dry (B) periods. a continuous 24-h activity with crepuscular peaks during the warm wet Black bars represent night periods (reprinted from Hetem et al. ). period to nocturnal activity during the hot dry period. Activity counts are expressed as a percentage of maximum counts for that animal. Black bars represent night periods (adapted from Hetem et al. ). works primarily at the level of physiology and behavior, it is concerning that we understand so little, for all mammals, about the direct links between physiology and vulnerability to climate (for review see refs. 133 and 134). These studies have contrib- change. We need to improve our understanding of the physi- uted substantially to our understanding of the key mechanisms ological and behavioral mechanisms that determine an animal’s of thermal adjustments and limitations, including finding that thermal tolerance and its capacity for acclimatization in order in those ectotherms thermal tolerance is limited by the capacity to better predict the impact of climate change on a particular of circulatory and ventilatory tissues. We are yet to establish 54,126-128 species. how thermal sensitivity applies to acclimatization in endotherms, Physiological acclimatization especially the large mammals, and how it applies might be sub- Though physiological mechanisms are responsible for the stantially different to its application in ectotherms. In theory, capacity of animals to adjust to new environments, there are endotherms may be more sensitive than ectotherms to rising limits to the capacity of physiological systems to respond to ambient temperatures, because endothermy evolved during cold changing environmental conditions, both because of limited climatic conditions and because enhanced organismic com- environmental resources and because of biochemical and physical plexity often is accompanied by increased thermal sensitivity. constraints. The physiological response of an organism therefore Generalist species, characterized by wide thermal tolerance acts as a “filter” between a change in environmental conditions windows but also with large geographic ranges and greater physi- and fitness, which ultimately determines species persistence and ological plasticity, are less likely to be affected by climate change ecosystem biodiversity. To predict accurately the direct physi- than are species that are physiologically specialized with respect 113,137-139 ological effects of climate change on a species, we need, first, to the thermal environment. Endotherms, as thermal spe- an understanding of the thermal physiological sensitivity of the cialists, then are likely to be particularly vulnerable to climate species, including how close to its thermal limits, or “prescriptive change. The width of the thermoneutral zone (TNZ) of endo- zone” , the species is living. Second, we need an understanding therms, including large mammals, may provide a useful index of of the relationship between climate and the thermoregulation of thermal specialization and has recently been used to assess the the species, including the degree to which the species can adjust, vulnerability of endotherms to climate change. Tropical mam- 126,132,133 141 or acclimatize. Because of the clearly-defined thermal mals display a narrower TNZ than do their arctic counterparts, niches which occur in the marine environment, most studies that primarily because of an elevated lower limit in tropical species. have investigated the physiological principles underlying thermal Mammalian species with narrow TNZ, such as tropical arboreal limits and thermal sensitivity have focused on marine ectotherms marsupials, indeed do appear to be more at risk from climate 120 Temperature volume 1 issue 1 change. For example, the white lemuroid possum (Hemibelideus artiodactyls to cope with aridity and heat stress predicted to 151,158 lemuroides), a species endemic to the mountain forests of north- occur with climate change. ern Queensland, risks extinction as a result of the recent 0.8 °C Maternal effects increase in ambient temperature there. Conversely, mamma- Our discussion of physiological acclimatization in response to lian species with wide thermoneutral zones, such as the hibernat- climate change relates to how function in an individual might 143,144 ing mammalian species in the Canadian Arctic region, are change, potentially to its benef it, as it encounters climate change. predicted by some researchers to show an increase in abundance That encounter might affect not just the animal itself, but also its and distribution in response to climate change. Yet, in a recent offspring, through the phenomenon known as “maternal effects”: meta-analysis of responses of 81 mammalian species, hibernating the conditions to which a female animal is exposed during her species and those which display torpor were no less affected by pregnancy can inf luence the life-history traits in her offspring. climate change than were those which do not. Variation in the These maternal effects involve epigenetic changes in the fetus and upper limit of tolerance seems to be more relevant in the context are controlled by hormones that regulate the expression of phe- of climate change, yet such variation appears to be much less than notypic variation in traits like body mass, growth and survival. that of the lower limit. Stress and reproductive hormone levels in free-living populations As is the case with the white lemuroid possum, species that correlate with life-history traits and may provide useful biomark- currently live in hot environments may be the most vulnerable ers of how mammals might be adapting to climate change. to climate change, because they are already living close to their Numerous species of antelope in the northern hemisphere dis- upper limits of thermal tolerance and have limited scope for play plasticity in offspring birth mass in response to changing cli- 133,145 55 further acclimatization. The Arabian oryx inhabiting the matic conditions. Although these maternal effects may promote extreme environment of the Arabian Desert may be living at the the survival and enhance the reproductive success of the mother, 146,147 edge of its physiological limits. In arid environments, the such plasticity in birth mass has long-term consequences for the threat of increased ambient temperature is compounded, or even offspring. Like many morphological traits, body mass at birth is exceeded, by the threat of reduced water availability resulting a “non-labile” trait as it is expressed only once in an individual’s 148 161 from climate change. Although many factors consequent upon lifetime. Most “non-labile” traits are traits that show plasticity the increase in temperatures and aridity with climate change may only during development. However, such developmental plastic- threaten survival at community and individual levels, other fac- ity can be adaptive only if the trends for changes in climatic con- tors are irrelevant if individual animals cannot maintain homeo- ditions at the time of development remain similar throughout the stasis of body temperature and body fluids, as their habitats offspring’s lifetimes. become hotter and drier. Desert-adapted artiodactyls have to Behavioral f lexibility trade off thermoregulation, osmoregulation, and energy acquisi- Thermoregulatory behavior constitutes a set of rapid, tion. In the Arabian ory x when conf lict between regulatory sys- extremely f lexible, and precise mechanisms that can enhance an tems occurs, priority is given to osmoregulation. When water animal’s performance, and presumably its fitness, by incorporat- is scarce evaporative cooling is reduced (presumably to conserve ing both anatomical and physiological traits to optimize body 162-164 body water) at the expense of homeothermy, resulting in higher temperature homeostasis. Behaviors that potentially reduce core body temperature in hot conditions. Similarly, when energy thermoregulatory costs include appropriate microclimate selec- supply is limited endotherms reduce metabolic heat production, tion, postural adjustments and the restriction of daily activities to 150 16,165 resulting in lower core body temperature. Though it may save time periods when heat loads and water loss are lower. Since water and/or energy, the resulting heterothermy increases the risk behavioral changes generally are less costly than are autonomic of mortality and morbidity if tissue temperatures depart from responses, behavioral adjustments are likely to be preferred. 167,168 the tolerable range. Whether the heterothermy that has been However, to date, only two models, both in ectotherms, have observed in conditions of food and water shortage is a controlled evaluated the role of behavioral thermoregulation in buffering thermoregulatory event that might serve as an adjustment to cli- the impact of climate change revealing that behavioral f lexibility mate change, or whether it results from failure of homeothermy, will be important in species persistence. Whether such behavioral 147,151 remains debatable. adjustments actually are occurring in mammals, with benefit, A second autonomic mechanism that the Arabian oryx used remains to be investigated. 167 169 to conserve body water and facilitate homeostasis at high envi- At least theoretically, like ectotherms, endotherms should ronmental heat loads was selective brain cooling. Mammals be able to buffer some of the additional thermal stress of cli- possessing a carotid rete employ selective brain cooling that mate change through appropriate thermoregulatory behavior. reduces hypothalamic temperature. Because hypothalamic tem- Terrestrial animals, because of their mobility and capacity for perature provides the main drive for evaporative heat loss, the complex behaviors, can exploit the thermal mosaic of their habi- 162,163 hypothalamic cooling conserves water by transferring heat loss to tat to select a preferred microclimate. Importantly, the avail- 153-156 non-evaporative means. The evolution of the carotid rete is able microclimates can differ substantially from the macroclimate proposed to have promoted thermoregulatory f lexibility and thus used in many modeling exercises, provided there is sufficient 7,44,170 facilitated the invasion of arid zones by artiodactyls, which have thermal heterogeneity within a habitat. But a microhabitat a carotid rete, during the highly-seasonal post-Eocene period. selected for its thermal properties may have an increased risk of Plasticity in rete function may well provide an adjustment for predation, parasites, competition, or a decreased availability of www.landesbioscience.com Temperature 121 162,165,171 176 resources, including energy, mates, food, or water. For decreased, and those that remain are in poor body condition. example, in an arid high-elevation desert, the North American Polar bears are dependent heavily on Arctic spring ice, because elk (Cervus elaphus), preferentially selected areas where their costs that is where they discover the seals (on ice to give birth) that 177,178 of thermoregulation were reduced, despite having limited access are their primary food source at this time. The Arctic ice is to high quality forage in such areas. In contrast, in a forest disappearing under the impact of global warming, and, if polar habitat the thermoregulatory costs of different habitats were less bears continue with their current lifestyle, the world population pronounced and elk selected areas on the basis of access to high is likely to drop by two-thirds by 2050. Polar bears may well quality forage, rather than lower thermoregulatory cost. survive if they have the capacity to make a major change in life- The interplay between competing homeostatic processes style (which the fossil record shows they have done previously), will become increasingly important under the thermal threat of namely to abandon the ice, and their current food source, and climate change, and optimization of homeostasis increasingly to become land-based. Another species forced to change its difficult. The moose (Alces alces) provides an example of the behavior and become land-based is the Pacific walrus (Odobenus potential costs associated with behavioral thermoregulation of a rosmarus divergens). Walruses use sea ice as a breeding ground, as large mammal in the context of climate change. In the past 20 well as a resting platform between foraging dives, but the recent y, the moose population in Minnesota, USA, has halved and the decline in Arctic sea ice has forced them to abandon the sea ice population in the Isle Royale National Park, USA, has declined and haul out instead along the shores of Alaska and Russia. by 75%. Moose are particularly sensitive to heat and seek shelter Coastal haul outs often are associated with mortalities from tram- when ambient temperatures exceed 14 °C. Over the past 40 y, pling, exhaustion and the separation of calves from their moth- as the average summer temperature has increased by 2 °C, moose ers. Furthermore, there may be energetic costs as walruses are have forfeited valuable foraging time in preference for lethargy forced to spend more time at sea traveling between coastal haul and microhabitat selection in the form of immersion in cool out sites and offshore foraging areas than when offshore sea ice is water. Forfeiting foraging has led to malnutrition and decreases available. Unlike the walruses, which have to travel more, some fat reserves, which are essential for winter survival. Malnutrition humpback whales (Megaptera novaeangliae) are abandoning their also is likely to increase their risk of succumbing to parasites, migration habits and remaining in southeast Alaska throughout disease and predation by wolves, all factors which are believed to winter, seemingly in response to climate-induced increased avail- 174 182 have contributed to the recent decline in the moose population. ability of herring. Presumably the energetic cost of thermoreg- With further increases in summer temperatures predicted for the ulation in the cold waters is offset by metabolic savings of not future, it seems likely that the moose will be extirpated from its having to undertake one of the longest documented mammalian historic southern range within the next 50 y. Recent warming migrations, with food locally available. The humpback whales already has resulted in populations of pika (Ochotona princeps) will not be the only species for which migration patterns will be being extirpated from the lower elevations of their distribution affected by climate change. range. Pika stop foraging during the hottest part of the day, Future Research a behavior likely to result in decreased foraging time as ambient temperatures continue to increase. Because of the increased exposure to high heat loads, those Though we know so little about it, it will be on their physi- species that feed strictly by day are at increased risk of having their ological and behavioral plasticity that the future of large mam- energy budgets constrained by increasing daytime temperatures, mals, threatened by climate change, will depend. Plasticity of particularly if they are unable to compensate for reduced diurnal physiological and behavioral mechanisms allows the expression activity by increasing nocturnal activity. By increasing nocturnal of latent talents, which can provide mammals with the capac- 129,185 activity, the usually-diurnal Arabian oryx was able to compensate ity to adjust to new environments, and are fundamental to 127,130 completely when its diurnal activity was reduced as a result of determining the consequences of climate change. Future shade-seeking in extreme daytime heat (Fig. 4). The Arabian research in climate change biology will require the measurement oryx were not prevented by natural predators from shifting freely of physiological and behavioral characteristics of many identi- 70,100 between diurnal and nocturnal activity, but large mammals else- fied individual mammals for long periods, probably decades. where will have an expensive trade-off to make because they may Since the responses to climate change are likely to be multifac- be exposed to a greater nocturnal predation pressure should they eted responses to complex interrelated stresses, the approach will attempt to avoid high diurnal temperatures by becoming noctur- have to be that of field physiology, namely the investigation of nal. Nevertheless, species that show flexibility in their activity the mechanisms that an animal uses while going about its daily patterns are less likely to be affected adversely by climate change business in its natural habitat. The studies required fall within 129,130,187 than are those species which are strictly diurnal, or even strictly the sub-disciplines of conservation physiology and evo- 19 188 nocturnal. If they are to survive climate change, large long-lived lutionary physiology. The growth of these sub-disciplines has mammals will need to show f lexibility in their behavioral reper- resulted not just from the clear need for such an approach, but toire, and not just behavior related to foraging. from the growing availability of suitable technology, such as the Without a radical change in their behavior, the future sur- use of stable isotopes for field measurement of metabolic rate and 100 189 vival of polar bears (Ursus maritimus) is considered bleak. Over water turnover, and osmotic minipumps to deliver substances 190 191 the past 28 y the number of polar bears in Hudson’s Bay has to and equipment to sample blood from free-living animals. 122 Temperature volume 1 issue 1 The primary new technology, however, has been biotelemetry 187,192-194 or biologging. Physiological variables such as body tem- perature, activity and energetic expenditure of terrestrial mam- mals now can be measured relatively easily in free-living animals. We need to make such sophisticated physiological measurements in individuals of several species inhabiting a variety of environ- ments, measurements that would fall into the recently-defined field of macrophysiology, defined as “the investigation of varia- tion in physiological traits over large geographical and tempo- ral scales and the ecological implications of this variation” . Incorporating the resulting macrophysiological data into biocli- matic envelope models will allow us to better predict how species will respond to climate change. Knowing which species demon- strate sufficient physiological plasticity to cope with the conse- quences of climate change will allow for more informed decisions as to which species are particularly vulnerable to climate change. About the Authors Figure 5. Photograph of the authors. Disclosure of Potential Conf licts of Interest In the face of climate change, large mammals will depend largely on their physiological phenotypic plasticity to survive, No potential conf licts of interest are disclosed. but there have been few appropriate studies of the physiologi- Acknowledgments cal responses of free-living terrestrial mammals in their natural habitats. Performing such studies, in which they measure the We thank the South African National Research Foundation effects of thermal stress and reduced water and food availability (NRF), the Oppenheimer Memorial Trust, the Carnegie on behavioral patterns and physiological responses, is the main Corporation of New York, the global change SysTem for research focus of the authors. They have developed innovative Analysis, Research and Training (START), the University of the techniques for long-term remote measurement of body tempera- Witwatersrand, and the Australian Research Council for finan- ture, locomotor activity, drinking patterns, thermoregulatory cial support. We thank Dr Leith Meyer and the Central Animal behavior and local microclimate around an animal, which they Services of the University of the Witwatersrand for providing vet- are using to investigate how free-living mammals, ranging in erinary expertise in our f ield studies, and the managers and own- size from monkeys to elephants, respond to climate and habitat ers of numerous f ield sites for allowing us access to their facilities, changes (Fig. 5). and providing invaluable support. rd 6. Rosenzweig C, Karoly D, Vicarelli M, Neofotis P, 12. Sala OE, Chapin FS 3 , Armesto JJ, Berlow E, References Wu Q, Casassa G, Menzel A, Root TL, Estrella N, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke 1. Stocker TF, Qin D, Plattner G-K, Alexander LV, Seguin B, et al. Attributing physical and biological LF, Jackson RB, Kinzig A, et al. Global biodiversity Allen SK, Bindoff NL, Bréon F-M, Church JA, impacts to anthropogenic climate change. Nature scenarios for the year 2100. 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Proc Biol Sci 2008; 275:1469- wintering off Central America: insights from water http://dx.doi.org/10.1890/13-1273.1 78; PMID:18397867; http://dx.doi.org/10.1098/ temperature into the longest mammalian migration. 173. Dussault C, Ouellet JP, Courtois R, Huot J, Breton L, rspb.2008.0137 Biol Lett 2007; 3:302-5; PMID:17412669; http:// Larochelle J. Behavioural responses of moose to ther- dx.doi.org/10.1098/rsbl.2007.0067 mal conditions in the boreal forest. Ecoscience 2004; 11:321-8 www.landesbioscience.com Temperature 127 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Temperature Taylor & Francis

Responses of large mammals to climate change

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Taylor & Francis
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Copyright © 2014 Landes Bioscience
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2332-8959
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10.4161/temp.29651
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Abstract

Review Temperature 1:2, 115–127; July/August/September 2014; © 2014 Landes Bioscience Responses of large mammals to climate change 1, 1 1,2 1,2 Robyn S Hetem *, Andrea Fuller , Shane K Maloney , and Duncan Mitchell Brain Function Research Group; School of Physiology; University of the w itwatersrand; Faculty of Health Science; Parktown, South Africa; School of Anatomy, Physiology, and Human Biology; University of w estern Australia; Crawley, Australia Keywords: climate change physiology, phenotypic plasticity, physiological acclimation, behavioral f lexibility, range shift, microevolution, temperature Most large terrestrial mammals, including the charismatic species so important for ecotourism, do not have the luxury of rapid micro-evolution or sufficient range shifts as strategies for adjusting to climate change. The rate of climate change is too fast for genetic adaptation to occur in mammals with longevities of decades, typical of large mammals, and land- scape fragmentation and population by humans too widespread to allow spontaneous range shifts of large mammals, leaving only the expression of latent phenotypic plasticity to counter effects of climate change. The expression of pheno- typic plasticity includes anatomical variation within the same species, changes in phenology, and employment of intrin- sic physiological and behavioral capacity that can buffer an animal against the effects of climate change. w hether that buffer will be realized is unknown, because little is known about the efficacy of the expression of plasticity, particularly for large mammals. Future research in climate change biology requires measurement of physiological characteristics of many identified free-living individual animals for long periods, probably decades, to allow us to detect whether expres- sion of phenotypic plasticity will be sufficient to cope with climate change. Introduction sensitivity to environmental change, its resilience to perturbations and its potential to adapt to change’. Vulnerable species or ani- The 2013 Intergovernmental Panel on Climate Change mal populations have only three options when faced with climate synthesis report predicts an increase in global temperatures of change. First, they may shift their distribution range, to habitats between 1.5 °C and 4.5 °C during the 21st Century, which will where the climate is within the species’ tolerance limits. Second, take us to the warmest global climate in more than two million they may remain in a location but adjust to new climatic regimes years. Although the rate of the current warming episode probably either through a change in the genetic composition of a popu- does not exceed the normal background rate of climate change, lation or by phenotypic plasticity, which results in a different continued warming over the next few decades will exceed the phenotype from an existing genotype via changes in epigenetic 2 9 background rate of change by more than an order of magnitude. control of gene expression. Either of these outcomes may bring The rate of future climate change will be unprecedented in the about changes in the timing of events (phenology), anatomical Earth’s history. It probably will be that rate of climate change, variation (e.g., color patterns, body shape and size), or changes rather than the eventual magnitude or duration of the episode, in the behavior or physiology of a species, which could reduce 4 10 that will prove to be critical for biota. Indeed, the typical rate of the impact of climate change. Finally, if neither range shifts nor niche evolution that has been observed in more than 500 species adjustment is possible, global or local extinction (extirpation) is about 10 000 times slower than the rate that will be required may result. Whatever options are realized, climate change will 5 11-14 to keep track with climate change projections for 2100. Though have a significant impact on biodiversity, and current conser- worse is to come, it is delusional to envisage climate change only vation strategies, which attempt to conserve communities and 15-18 as a future challenge. Its biological consequences already are evi- ecosystems as they exist, will be unsustainable. dent. Of the nearly 30 000 documented trends in physical sys- For many large mammals, especially those living in human- tems and biological characteristics of plants and animals between dominated landscapes, range shifts are unlikely options for 1970 and 2004, 90% have been in the direction consistent with coping with climate change. Because the research has not been environmental temperature increases. done, we do not know whether large mammals can express suf- According to Huey et al. ‘the vulnerability of a species to ficient genetic shifts or phenotypic plasticity to adjust to the cur- environmental change depends on the species’ exposure and rent climate change event. We do know that large mammals are *Correspondence to: Robyn S Hetem; Email: robyn.hetem@wits.ac.za Submitted: 06/16/2014; Revised: 7/15/2014; Accepted: 07/19/2014; Published Online: 07/21/2014 http://dx.doi.org/10.4161/temp.29651 www.landesbioscience.com Temperature 115 more likely to be adversely effected by climate change than their smaller counterparts. Here we review what we do know, and need to know, about the possible responses of large terrestrial mammals. We contextualize our discussion of large mammals within established principles of climate change biology. Extinction Global warming has been a common occurrence on Earth for the last 3.5 billion years. Modeling of the current episode predicts a temperature rise of the same order of magnitude as that evident at the end of the Permian, when mass volcanism increased global temperatures by 6 °C and resulted in the extinc- tion of nearly 95% of species. We cannot be sure that it was the warming that was responsible for all of those extinctions, but the fossil record is unequivocal that extinction and extirpation have been common outcomes for species facing past climate change events of comparable magnitude. A pivotal study by Thomas et Figure  1. Small map: Observed current distribution of the scimitar- al. predicted that, under mid-range climate change scenarios, a horned oryx (Oryx dammah). Large map: Predicted habitat distribution quarter of terrestrial plants and animals may be extinct by 2050. for the scimitar-horned oryx in 2050. Light gray indicates habitats that are presently climatically suitable but are predicted to be unsuitable in By extrapolating such predictions to a global scale, the authors 2050. Moderate gray indicates habitats that are presently climatically predicted that well over one million species, among which will suitable that are predicted to remain suitable in 2050. Dark gray indicates be many large terrestrial mammal species, could be threatened habitats that are presently climatically unsuitable that are predicted to with extinction as a result of climate change. Their models pre- 22 be suitable by 2050 (adapted from Thuiller et al. ). dict that 45% of terrestrial species are likely to be committed to extinction by 2050 if their dispersal is limited. Among the large terrestrial mammals seemingly destined to examined have shifted their range into adjacent habitats between become extinct are the charismatic species so important for eco- 1970 and 2000, presumably in response to climate change. tourism. Africa is rich in such species, and serves as an example Observed range shifts averaged 11 m per decade upwards and of the future likely under climate change; 25–40% of a repre- nearly 17 km per decade polewards, with range shifts correlat- sentative sample of 277 of its mammalian species is likely to be ing positively with the rate of warming. Global meta-analyses critically endangered or extinct by 2080. The charismatic spe- have revealed that 80% of range shifts have been consistent with 24,28,29 cies of South Africa are likely to be particularly vulnerable to climate change predictions. However, the recorded shifts climate change, as will be large mammals in human-dominated include few, if any, large mammals. landscapes elsewhere, because the consequences of high human Shifting range in response to climate change requires suitable population density will prevent their dispersal. The extinction new habitats to be accessible, and for the required traveling dis- risk of South African mammals is estimated to be as high as 69% tances to be within the capacity of the species that is shifting by 2050. Indeed, long-term population monitoring in the coun- range. The rapid rate of climate change will mean that nearly try’s f lagship Kruger National Park already has revealed declines 10% of mammals in the western hemisphere will be unable to 23 30 in seven out of 11 ungulate species between 1977 and 1996. move fast enough to keep pace with projected climate changes. A salutary example of unattainability of the required pace is the Range Shifts scimitar-horned oryx (Oryx dammah, Fig. 1). To track its suit- able climate, this species would have had to move thousands of Although large mammals in fragmented, human-dominated kilometers, from the Sahel to the Kalahari Desert, an impossible habitats, like those prevailing in South Africa, will be precluded shift without human assistance. The species has become extinct from shifting to a new habitat in response to current climate in what was its current natural habitat in the last decade. In cir- change, large mammals in more-pristine habitats such as bears in cumstances in which natural range shifts are not feasible, either northern Canada, and smaller mammals every where, may be able as a result of unattainable traveling distances or loss of habitat to track suitable climates. In the temperate zone, for example, a 1 connectivity, assisted colonization may provide a conservation 31,32 °C increase in mean annual temperature corresponds to a shift in option. Yet, moving species to areas where they do not cur- 24,25 isotherms of ~160 km in latitude or 160 m in elevation. Thus, rently occur is not without risk. The introduced species can carry biota that can do so, including mammals, are expected to follow disease, displace native species and thereby challenge ecosystem the shifting climatic zones and move polewards in latitude and stability or alter the genetic structure of local populations. An in- 17,26 upwards in elevation. Numerous recent reports have docu- depth knowledge of species’ biology and accurate climate change mented shifts in the geographical distribution of extant biota (for predictions is required before assisted colonization can become a 33,34 reviews see refs. 24, 27, and 28). More than half of the species routine conservation option. 116 Temperature volume 1 issue 1 For assisted colonization to be a feasible conservation option attempted to incorporate physiological factors to address the cli- 60,61 62,63 for a species, we need an understanding of the fundamental matic tolerances of terrestrial ectotherms and mammals, niche (where species can occur) and realized niche (where species but they require an understanding of species’ physiological 64-66 do occur), and the likely location of those niches in the future. responses to climate, an understanding that we are far from Bioclimatic envelope, or niche-based, models are static models having attained for most species. Although these physiologically- that correlate current species distributions with climate variables tuned models still have limitations, for example in not taking and project future distributions according to each species’ “cli- non-climatic factors into account, they are likely to be more 35-37 matic envelope” . Some models were developed sufficiently robust than those bioclimatic envelope models that are based long ago for their predictions to be tested against actual observa- only on correlations between observed distributions and current 45,67,68 tions, and they have proved their value. For example, in a meta- climate variables. analysis of range shifts, latitudinal shifts matched the expected Micro-Evolution range shifts if a species were to track its bioclimatic envelope. While of proven utility, the assumptions on which these mod- els are based can be questioned regarding their ability to predict Future extinction risk is likely to be overestimated if species 38-41 the potential impact of climate change. Bioclimatic enve- exhibit adaptive genotypic changes in response to environmental lope models typically do not address stochastic events like local change. Evolutionary change often is considered too slow, given droughts and heat waves, which may impose the dominant cli- the rate of the climate change event, to allow genetic adaptation, 42,43 3,4 mate stress on species in the future. They also do not address but is likely to have accompanied range shifts in the past. A spatial variability. It is the microclimate experienced by an ani- changing climate moves the so-called “fitness optimum” for 44-47 3,4 mal that has direct influence on an animal’s thermal status. different populations throughout the species range, making All thermal aspects of those microclimates need to be quantified the fundamental niche flexible over time. Range shifts already before they can be incorporated into climate change models. are having genetic consequences in the current event. By mix- Although they do not incorporate measures of evaporation, min- ing populations that are shifting, a range shift increases genetic iature black globe thermometers can be attached to large mam- variation, thereby increasing the population’s chance of adapting mals to provide a quantitative measurement of heat loads of their to changing conditions. Northwards range shifts in the northern microclimates. hemisphere, for example, may have the advantage of introduc- Another shortfall of current bioclimatic envelope models is ing genotypes that are better adapted to warmer conditions, thus that they do not account for non-climatic influences on spe- promoting the adaptation of existing cooler-adapted populations 69,70 cies’ distributions, such as terrain and biotic interactions (but see to climate change. Conversely, range shifts also can decrease ref. 49). Climate-induced species interactions are likely to have genetic variability that has occurred historically as a result of out- 50,51 important consequences for future species distributions. For breeding of distinct populations. For example, climate change example, the climate-driven northward range expansion of the may result in genetic mixing among subspecies of the black bear, red fox (Vulpes vulpes) has been associated with a decrease in the which could inhibit or even reverse sub-speciation. distribution range of the arctic fox (Alopex lagopus) as a result of The genetic adaptation that will be required to survive cli- 52 70,72 3,73,74 an increased interspecific competition. Since individual plant mate change is not the slow process of speciation, but and animal species differ in their response to changing climatic heritable shifts in allele frequencies in a population (without spe- conditions, species may shift their ranges independently of each ciation) known as “micro-evolution”. Micro-evolution already 75,76 other, resulting in changes in community structure and possi- has occurred, in directions predicted by climate change, par- 26,53-55 bly in ecosystem disruption. For example, decreased rain- ticularly for short-lived species with fast generation times (for fall altered the plant community and ultimately led to a decline examples, see refs. 77-82). Surprisingly, there have been shifts in desert bighorn sheep (Ovis canadensis nelsoni) population in in genetic variability even in populations of the relatively long- California. These species interactions thus need to be incorpo- lived Canadian lynx (Lynx canadensis) that have been associated rated into bioclimatic envelope models to better predict future with snow depth and winter precipitation. It remains uncertain, species distributions, which is the aim of a new scope of ecologi- though, whether micro-evolution can result in a change in the 58 84 cal research termed “global change ecology” . climate tolerance of any species sufficient to prevent extinction. We and others believe, however, that the major limitation A morphological feature related to climate tolerance that is of predictions derived from bioclimatic envelope models is the determined genetically is an animal’s coat color. Analyses by assumption that species lack sufficient phenotypic plasticity to Maloney et al. support the view that progressive increases in adjust to climates beyond those in which they occur currently. ambient temperature explain the recent 20-y shift in the ratio of Models typically assume, for each species, that the realized niche dark to light-colored Soay sheep on the archipelago of St Kilda, is the fundamental niche: the species occupies today all habi- United Kingdom, contrary to the original explanation based on 86,87 tats fulfilling the thermal conditions that it can tolerate, and it an association of coat color with body mass. The advantage therefore cannot survive at a current habitat if conditions depart enjoyed historically by dark-colored sheep in absorbing solar from those in which that species survives now. Yet, plasticity may radiation better would carry less benefit in warmer environ- allow animals to adjust to changing climatic conditions without ments. Similarly, there is thermoregulatory significance of pelt changing their location. Some bioclimatic envelope models have color for springbok (Antidorcas marsupialis), with black springbok www.landesbioscience.com Temperature 117 96 97 2 °C and a decrease in precipitation. Réale et al. cal- culated that 13% of the observed phenological changes in parturition date could be attributed to micro-evolu- tion. However, since the investigators initially did not account for systematic environmental variation across years, even that 13% may be an overestimate of the role of genetic change. Potentially, more than 60% of the observed changes in parturition date of the squirrel must be attributed to phenotypic plasticity. Short-lived mammalian species, like the red squirrel, have the advantage of fast generation times, which may improve their chance of survival as each generation pro- 70,77,78,99,100 vides scope for micro-evolution. Conversely, large mammals with long generation times, and indeed those small mammal species, like bats, which have long generation times, are predicted to have less ability to respond genetically to any new selective pressures, making them more susceptible to extinction than are species with short generation times. The issue is compounded because large species have greater range requirements. There are many species of mammals with longevities such that individuals alive now ought Figure  2. The pelt color variations of the black, common and white springbok. still to be alive in 2030, and a few species for which Nychthemeral rhythm of body temperature (mean ± SD) for four black (red line), individuals alive now could be alive in 2100. Clearly, seven common (blue line) and four white (yellow line) springbok during a hot (A) the survival of those individuals, and probably those and cold (B) season. Black bars represent night periods (adapted from Hetem et 88 species, cannot depend on genetic adaptation. Instead, al. ). for those that also cannot shift their ranges, survival is likely to be entirely dependent on sufficient phenotypic benefiting, compared with their white conspecifics, by being plasticity to buffer effects of climate change. able to reduce metabolic costs in winter, as a result of increased Phenotypic Plasticity absorption of solar radiation (Fig. 2B). Increased absorption of solar radiation, however, may disadvantage the black springbok in the heat (Fig. 2A). As with the Soay sheep, we expect the black By definition, phenotypic plasticity is the process by which a color morphs to decline as their habitats warm, if populations are single genotype gives rise to different phenotypes in different cir- 104-106 left unmanaged. cumstances. The plasticity is known as an epigenetic effect. Although coat color has a genetic basis amenable to micro- Phenotypic plasticity in animals exposed to a change in environ- evolution in populations of mixed color morphs, and numerous ment may involve acclimation, acclimatization, and learning studies have interpreted such anatomical changes as micro-evolu- and can take place through phenology, developmental plasticity, tionary responses to climate change, the majority of studies have physiological adjustments and behavioral flexibility. Unlike provided no evidence that the observed changes have a genetic genetic adaptation, phenotypic plasticity allows the animal 89,90 basis. There is a general lack of evidence for or against genetic itself, rather than its future lineage (except in the case of mater- adaptations to climate change, resulting at least partially because nal effects; see below), to respond to environmental change. molecular techniques remain inadequate to properly reveal how The mechanism of plasticity can involve changes to the way that 91,92 genetic sequences relate to ecologically important traits, an DNA is packaged in the nucleus and alters the probability of a 93 9 inadequacy that is hopefully temporary. However, methods to particular gene being expressed. The best known mechanisms quantify a genetic component of adjustment to climate change of epigenetics are DNA methylation, histone modification, and are likely to remain difficult to implement, especially in long- more recently it has become obvious that small non-coding lived mammals. To date, there have been only 12 studies pub- RNA’s have both transcriptional effects on gene expression and lished that have tested for the genetic basis of climate-related post-transcriptional effects that alter the fate of the RNA from biological changes in mammals, and only one of these found gene transcription, prior to translation into RNA. evidence for a genetically-based response. The most convinc- Phenological changes ing example of micro-evolutionary response to climate change In addition to estimating the contribution of micro-evolution, is a short-lived mammal, the North American red squirrel the red squirrel study provided the first measurement of the role (Tamiasciurus hudsonicus), in Yukon from 1989 to 2001, a period of phenotypic plasticity in climate-induced development of a over which mean lifetime parturition date advanced by six days functional trait, but it was not the first to document changes per generation, associated with a mean spring temperature rise of in phenology, that is the timing of seasonal events, in response to 118 Temperature volume 1 issue 1 changing climatic conditions (see refs. 17,24,26,28,109). It still is pronghorn and may ultimately lead to a life-history strategy of the case that most known examples of phenotypic changes linked faster development. Similarly, the Soay sheep mentioned above to climate change relate to phenology. For example, in response are also breeding at an earlier age as their climate warms, result- to progressive environmental change over a 28-y period on the ing in a general decrease in mean body size in that population. Isle of Rum, United Kingdom, red deer (Cervus elaphus) have Anatomical variation displayed phenotypic plasticity in the phenological traits of estrus Although the majority of reports of phenotypic responses to date, parturition date, antler cast and clean date and the start and climate change, adaptive or not, relate to phenology, there are end of the rut, with most of the variation being attributable to reports relating to other traits. A decline in body mass is con- earlier plant growth. sidered the third universal response (after phenology and range When phenological changes are observed, they often are taken shifts) to warming associated with climate change. The rela- as evidence that species are adjusting to changing environmen- tionship between body mass and thermoregulation is complex. tal conditions in ways that help mitigate the effects of climate Relative to animals of larger body mass, animals of the same change. Yet the responses in nearly half of a set of studies report- shape with lower body mass, for geometric reasons, have a higher ing phenotypic changes in phenology, body mass, or litter size surface area-to-mass ratio, and therefore have more difficulty in mammals actually were associated with a decline in fitness. preventing body heat loss in cold environments. That physical For example, the advanced breeding of Chillingham cattle (Bos relationship is congruent with Bergmann’s rule that predicts a primigenius taurus) in response to warming led to more calves positive correlation between the body mass of terrestrial endo- being born in winter, which resulted in an increase in calf mor- therms and latitude, and, by inference, an inverse correlation tality. The responses in only one third of the studies qualified between body mass and environmental temperature. With as adaptive phenotypic changes in phenology on the criterion global warming, species with lower body mass would lose that that both the direction and the rate of change were appropriate. disadvantage progressively, so a relative increase in proportion of Because species may show rates of phenological change different smaller animals would be expected in a warmer world. There to those of other species on which they depend, asynchrony or a are some data supporting that expectation. As mentioned, over 17,112-114 mistiming of key ecological events can result. For example, a 20-y period of progressive winter warming, the average body the calving date of caribou (Rangifer tarandus) on Greenland has mass of the Soay sheep on St. Kilda has declined between ~0.3% been advancing more slowly, with warming, than has the onset (senescents) and ~0.8% (yearlings) of mean body mass per year. of plant growth, creating a trophic mismatch and increasing calf The proposed mechanism is that the milder winters resulted in mortality. Numerous studies have demonstrated the ecologi- less reliance on fat reserves, which in turn enables more of the 112,116 120 cal and metabolic costs of such mistimed ecological events, small individuals to survive the winter. However, a decline in which ultimately may lead to a decrease in biodiversity. body mass does not appear to be a universal response of mam- One possible cause of mismatch between phenological mals to climate change. Data from museum specimens collected responses in connected species is the different environmental during the last quarter of the twentieth century reveal that body cues to which different species respond. Whereas most plants size of otters (Lutra lutra) in Norway has increased, presumably and insects respond to seasonal changes in temperature, most as a result of increased food availability. Indeed, only 7% of vertebrate species are more sensitive to changes in photoperiod, recently-observed changes in mammalian body masses provide although, as was the case for red deer on Rum, better nutrition support for an advantage to smaller mammals. Also, the physi- can also advance reproductive events. Thus, those vertebrates cal principles outlined above have a reverse effect when ambient with a photoperiod-sensitive reproductive cycle that remain at temperature exceeds body temperature, a situation which will their historic locations may face a mismatch between reproduc- become increasingly common with climate change. There the tion and food availability, while those dispersing latitudinally higher surface area-to-mass ratio increases environmental heat will have to adjust to an unfamiliar annual cycle of photoperiod load. In those environments, thermal balance also will depend 70,76 in their new habitat. Those species that are unable to match on the capacity for evaporative cooling, which may be unrelated the timing of key life-history events to the phenology of the to body mass. Despite a 4-fold difference in body mass between species on which they depend will be forced to show plasticity Arabian oryx (Oryx leucoryx) and Arabian sand gazelle (Gazella in other life-history traits if they are to maintain their lifetime subgutturosa marica), both species showed an increased amplitude reproductive success. For example, flexibility in phenology of of body temperature rhythm (increased heterothermy) when they the Antarctic fur seal (Arctocephalus gazelle) is important in their were exposed to the same extreme heat and aridity (Fig. 3). highly variable thermal environment but is limited because of the Although understanding the physiological mechanisms is 70,113 long interval between conception and weaning of the pups. As essential for predicting responses to climate change, a dispro- their environment warms the female Antarctic fur seals appear portional number (> 80%) of studies of phenotypic responses to to be adapting their life cycles by not breeding in years of low climate change has focused on anatomical plasticity, with fewer 118 125 krill supply, thus increasing adult survival and fitness. Another studies on physiological and behavioral responses. Such pre- species that is changing its life-history strategy in response to sto- ponderance may reflect the ease of measurement of anatomical chastic environmental conditions is the pronghorn (Antilocapra features like body mass. Gathering physiological and behavioral americana). Frequent severe weather events result in an increase data, on the other hand, is labor-intensive and requires long peri- in male mortality, which favors precocial maturation in male ods of observation and monitoring. Given that natural selection www.landesbioscience.com Temperature 119 Figure  3. Nychthemeral rhythm of body temperature (mean ± SD) for Figure  4. Nychthemeral rhythm of activity for five Arabian oryx dur- five free-living Arabian oryx (gray line) and four free-living Arabian sand ing both the warm wet (A) and hot dry (B) periods. Oryx shifted from gazelle (black line) during both the warm wet (A) and hot dry (B) periods. a continuous 24-h activity with crepuscular peaks during the warm wet Black bars represent night periods (reprinted from Hetem et al. ). period to nocturnal activity during the hot dry period. Activity counts are expressed as a percentage of maximum counts for that animal. Black bars represent night periods (adapted from Hetem et al. ). works primarily at the level of physiology and behavior, it is concerning that we understand so little, for all mammals, about the direct links between physiology and vulnerability to climate (for review see refs. 133 and 134). These studies have contrib- change. We need to improve our understanding of the physi- uted substantially to our understanding of the key mechanisms ological and behavioral mechanisms that determine an animal’s of thermal adjustments and limitations, including finding that thermal tolerance and its capacity for acclimatization in order in those ectotherms thermal tolerance is limited by the capacity to better predict the impact of climate change on a particular of circulatory and ventilatory tissues. We are yet to establish 54,126-128 species. how thermal sensitivity applies to acclimatization in endotherms, Physiological acclimatization especially the large mammals, and how it applies might be sub- Though physiological mechanisms are responsible for the stantially different to its application in ectotherms. In theory, capacity of animals to adjust to new environments, there are endotherms may be more sensitive than ectotherms to rising limits to the capacity of physiological systems to respond to ambient temperatures, because endothermy evolved during cold changing environmental conditions, both because of limited climatic conditions and because enhanced organismic com- environmental resources and because of biochemical and physical plexity often is accompanied by increased thermal sensitivity. constraints. The physiological response of an organism therefore Generalist species, characterized by wide thermal tolerance acts as a “filter” between a change in environmental conditions windows but also with large geographic ranges and greater physi- and fitness, which ultimately determines species persistence and ological plasticity, are less likely to be affected by climate change ecosystem biodiversity. To predict accurately the direct physi- than are species that are physiologically specialized with respect 113,137-139 ological effects of climate change on a species, we need, first, to the thermal environment. Endotherms, as thermal spe- an understanding of the thermal physiological sensitivity of the cialists, then are likely to be particularly vulnerable to climate species, including how close to its thermal limits, or “prescriptive change. The width of the thermoneutral zone (TNZ) of endo- zone” , the species is living. Second, we need an understanding therms, including large mammals, may provide a useful index of of the relationship between climate and the thermoregulation of thermal specialization and has recently been used to assess the the species, including the degree to which the species can adjust, vulnerability of endotherms to climate change. Tropical mam- 126,132,133 141 or acclimatize. Because of the clearly-defined thermal mals display a narrower TNZ than do their arctic counterparts, niches which occur in the marine environment, most studies that primarily because of an elevated lower limit in tropical species. have investigated the physiological principles underlying thermal Mammalian species with narrow TNZ, such as tropical arboreal limits and thermal sensitivity have focused on marine ectotherms marsupials, indeed do appear to be more at risk from climate 120 Temperature volume 1 issue 1 change. For example, the white lemuroid possum (Hemibelideus artiodactyls to cope with aridity and heat stress predicted to 151,158 lemuroides), a species endemic to the mountain forests of north- occur with climate change. ern Queensland, risks extinction as a result of the recent 0.8 °C Maternal effects increase in ambient temperature there. Conversely, mamma- Our discussion of physiological acclimatization in response to lian species with wide thermoneutral zones, such as the hibernat- climate change relates to how function in an individual might 143,144 ing mammalian species in the Canadian Arctic region, are change, potentially to its benef it, as it encounters climate change. predicted by some researchers to show an increase in abundance That encounter might affect not just the animal itself, but also its and distribution in response to climate change. Yet, in a recent offspring, through the phenomenon known as “maternal effects”: meta-analysis of responses of 81 mammalian species, hibernating the conditions to which a female animal is exposed during her species and those which display torpor were no less affected by pregnancy can inf luence the life-history traits in her offspring. climate change than were those which do not. Variation in the These maternal effects involve epigenetic changes in the fetus and upper limit of tolerance seems to be more relevant in the context are controlled by hormones that regulate the expression of phe- of climate change, yet such variation appears to be much less than notypic variation in traits like body mass, growth and survival. that of the lower limit. Stress and reproductive hormone levels in free-living populations As is the case with the white lemuroid possum, species that correlate with life-history traits and may provide useful biomark- currently live in hot environments may be the most vulnerable ers of how mammals might be adapting to climate change. to climate change, because they are already living close to their Numerous species of antelope in the northern hemisphere dis- upper limits of thermal tolerance and have limited scope for play plasticity in offspring birth mass in response to changing cli- 133,145 55 further acclimatization. The Arabian oryx inhabiting the matic conditions. Although these maternal effects may promote extreme environment of the Arabian Desert may be living at the the survival and enhance the reproductive success of the mother, 146,147 edge of its physiological limits. In arid environments, the such plasticity in birth mass has long-term consequences for the threat of increased ambient temperature is compounded, or even offspring. Like many morphological traits, body mass at birth is exceeded, by the threat of reduced water availability resulting a “non-labile” trait as it is expressed only once in an individual’s 148 161 from climate change. Although many factors consequent upon lifetime. Most “non-labile” traits are traits that show plasticity the increase in temperatures and aridity with climate change may only during development. However, such developmental plastic- threaten survival at community and individual levels, other fac- ity can be adaptive only if the trends for changes in climatic con- tors are irrelevant if individual animals cannot maintain homeo- ditions at the time of development remain similar throughout the stasis of body temperature and body fluids, as their habitats offspring’s lifetimes. become hotter and drier. Desert-adapted artiodactyls have to Behavioral f lexibility trade off thermoregulation, osmoregulation, and energy acquisi- Thermoregulatory behavior constitutes a set of rapid, tion. In the Arabian ory x when conf lict between regulatory sys- extremely f lexible, and precise mechanisms that can enhance an tems occurs, priority is given to osmoregulation. When water animal’s performance, and presumably its fitness, by incorporat- is scarce evaporative cooling is reduced (presumably to conserve ing both anatomical and physiological traits to optimize body 162-164 body water) at the expense of homeothermy, resulting in higher temperature homeostasis. Behaviors that potentially reduce core body temperature in hot conditions. Similarly, when energy thermoregulatory costs include appropriate microclimate selec- supply is limited endotherms reduce metabolic heat production, tion, postural adjustments and the restriction of daily activities to 150 16,165 resulting in lower core body temperature. Though it may save time periods when heat loads and water loss are lower. Since water and/or energy, the resulting heterothermy increases the risk behavioral changes generally are less costly than are autonomic of mortality and morbidity if tissue temperatures depart from responses, behavioral adjustments are likely to be preferred. 167,168 the tolerable range. Whether the heterothermy that has been However, to date, only two models, both in ectotherms, have observed in conditions of food and water shortage is a controlled evaluated the role of behavioral thermoregulation in buffering thermoregulatory event that might serve as an adjustment to cli- the impact of climate change revealing that behavioral f lexibility mate change, or whether it results from failure of homeothermy, will be important in species persistence. Whether such behavioral 147,151 remains debatable. adjustments actually are occurring in mammals, with benefit, A second autonomic mechanism that the Arabian oryx used remains to be investigated. 167 169 to conserve body water and facilitate homeostasis at high envi- At least theoretically, like ectotherms, endotherms should ronmental heat loads was selective brain cooling. Mammals be able to buffer some of the additional thermal stress of cli- possessing a carotid rete employ selective brain cooling that mate change through appropriate thermoregulatory behavior. reduces hypothalamic temperature. Because hypothalamic tem- Terrestrial animals, because of their mobility and capacity for perature provides the main drive for evaporative heat loss, the complex behaviors, can exploit the thermal mosaic of their habi- 162,163 hypothalamic cooling conserves water by transferring heat loss to tat to select a preferred microclimate. Importantly, the avail- 153-156 non-evaporative means. The evolution of the carotid rete is able microclimates can differ substantially from the macroclimate proposed to have promoted thermoregulatory f lexibility and thus used in many modeling exercises, provided there is sufficient 7,44,170 facilitated the invasion of arid zones by artiodactyls, which have thermal heterogeneity within a habitat. But a microhabitat a carotid rete, during the highly-seasonal post-Eocene period. selected for its thermal properties may have an increased risk of Plasticity in rete function may well provide an adjustment for predation, parasites, competition, or a decreased availability of www.landesbioscience.com Temperature 121 162,165,171 176 resources, including energy, mates, food, or water. For decreased, and those that remain are in poor body condition. example, in an arid high-elevation desert, the North American Polar bears are dependent heavily on Arctic spring ice, because elk (Cervus elaphus), preferentially selected areas where their costs that is where they discover the seals (on ice to give birth) that 177,178 of thermoregulation were reduced, despite having limited access are their primary food source at this time. The Arctic ice is to high quality forage in such areas. In contrast, in a forest disappearing under the impact of global warming, and, if polar habitat the thermoregulatory costs of different habitats were less bears continue with their current lifestyle, the world population pronounced and elk selected areas on the basis of access to high is likely to drop by two-thirds by 2050. Polar bears may well quality forage, rather than lower thermoregulatory cost. survive if they have the capacity to make a major change in life- The interplay between competing homeostatic processes style (which the fossil record shows they have done previously), will become increasingly important under the thermal threat of namely to abandon the ice, and their current food source, and climate change, and optimization of homeostasis increasingly to become land-based. Another species forced to change its difficult. The moose (Alces alces) provides an example of the behavior and become land-based is the Pacific walrus (Odobenus potential costs associated with behavioral thermoregulation of a rosmarus divergens). Walruses use sea ice as a breeding ground, as large mammal in the context of climate change. In the past 20 well as a resting platform between foraging dives, but the recent y, the moose population in Minnesota, USA, has halved and the decline in Arctic sea ice has forced them to abandon the sea ice population in the Isle Royale National Park, USA, has declined and haul out instead along the shores of Alaska and Russia. by 75%. Moose are particularly sensitive to heat and seek shelter Coastal haul outs often are associated with mortalities from tram- when ambient temperatures exceed 14 °C. Over the past 40 y, pling, exhaustion and the separation of calves from their moth- as the average summer temperature has increased by 2 °C, moose ers. Furthermore, there may be energetic costs as walruses are have forfeited valuable foraging time in preference for lethargy forced to spend more time at sea traveling between coastal haul and microhabitat selection in the form of immersion in cool out sites and offshore foraging areas than when offshore sea ice is water. Forfeiting foraging has led to malnutrition and decreases available. Unlike the walruses, which have to travel more, some fat reserves, which are essential for winter survival. Malnutrition humpback whales (Megaptera novaeangliae) are abandoning their also is likely to increase their risk of succumbing to parasites, migration habits and remaining in southeast Alaska throughout disease and predation by wolves, all factors which are believed to winter, seemingly in response to climate-induced increased avail- 174 182 have contributed to the recent decline in the moose population. ability of herring. Presumably the energetic cost of thermoreg- With further increases in summer temperatures predicted for the ulation in the cold waters is offset by metabolic savings of not future, it seems likely that the moose will be extirpated from its having to undertake one of the longest documented mammalian historic southern range within the next 50 y. Recent warming migrations, with food locally available. The humpback whales already has resulted in populations of pika (Ochotona princeps) will not be the only species for which migration patterns will be being extirpated from the lower elevations of their distribution affected by climate change. range. Pika stop foraging during the hottest part of the day, Future Research a behavior likely to result in decreased foraging time as ambient temperatures continue to increase. Because of the increased exposure to high heat loads, those Though we know so little about it, it will be on their physi- species that feed strictly by day are at increased risk of having their ological and behavioral plasticity that the future of large mam- energy budgets constrained by increasing daytime temperatures, mals, threatened by climate change, will depend. Plasticity of particularly if they are unable to compensate for reduced diurnal physiological and behavioral mechanisms allows the expression activity by increasing nocturnal activity. By increasing nocturnal of latent talents, which can provide mammals with the capac- 129,185 activity, the usually-diurnal Arabian oryx was able to compensate ity to adjust to new environments, and are fundamental to 127,130 completely when its diurnal activity was reduced as a result of determining the consequences of climate change. Future shade-seeking in extreme daytime heat (Fig. 4). The Arabian research in climate change biology will require the measurement oryx were not prevented by natural predators from shifting freely of physiological and behavioral characteristics of many identi- 70,100 between diurnal and nocturnal activity, but large mammals else- fied individual mammals for long periods, probably decades. where will have an expensive trade-off to make because they may Since the responses to climate change are likely to be multifac- be exposed to a greater nocturnal predation pressure should they eted responses to complex interrelated stresses, the approach will attempt to avoid high diurnal temperatures by becoming noctur- have to be that of field physiology, namely the investigation of nal. Nevertheless, species that show flexibility in their activity the mechanisms that an animal uses while going about its daily patterns are less likely to be affected adversely by climate change business in its natural habitat. The studies required fall within 129,130,187 than are those species which are strictly diurnal, or even strictly the sub-disciplines of conservation physiology and evo- 19 188 nocturnal. If they are to survive climate change, large long-lived lutionary physiology. The growth of these sub-disciplines has mammals will need to show f lexibility in their behavioral reper- resulted not just from the clear need for such an approach, but toire, and not just behavior related to foraging. from the growing availability of suitable technology, such as the Without a radical change in their behavior, the future sur- use of stable isotopes for field measurement of metabolic rate and 100 189 vival of polar bears (Ursus maritimus) is considered bleak. Over water turnover, and osmotic minipumps to deliver substances 190 191 the past 28 y the number of polar bears in Hudson’s Bay has to and equipment to sample blood from free-living animals. 122 Temperature volume 1 issue 1 The primary new technology, however, has been biotelemetry 187,192-194 or biologging. Physiological variables such as body tem- perature, activity and energetic expenditure of terrestrial mam- mals now can be measured relatively easily in free-living animals. We need to make such sophisticated physiological measurements in individuals of several species inhabiting a variety of environ- ments, measurements that would fall into the recently-defined field of macrophysiology, defined as “the investigation of varia- tion in physiological traits over large geographical and tempo- ral scales and the ecological implications of this variation” . Incorporating the resulting macrophysiological data into biocli- matic envelope models will allow us to better predict how species will respond to climate change. Knowing which species demon- strate sufficient physiological plasticity to cope with the conse- quences of climate change will allow for more informed decisions as to which species are particularly vulnerable to climate change. About the Authors Figure 5. Photograph of the authors. Disclosure of Potential Conf licts of Interest In the face of climate change, large mammals will depend largely on their physiological phenotypic plasticity to survive, No potential conf licts of interest are disclosed. but there have been few appropriate studies of the physiologi- Acknowledgments cal responses of free-living terrestrial mammals in their natural habitats. Performing such studies, in which they measure the We thank the South African National Research Foundation effects of thermal stress and reduced water and food availability (NRF), the Oppenheimer Memorial Trust, the Carnegie on behavioral patterns and physiological responses, is the main Corporation of New York, the global change SysTem for research focus of the authors. They have developed innovative Analysis, Research and Training (START), the University of the techniques for long-term remote measurement of body tempera- Witwatersrand, and the Australian Research Council for finan- ture, locomotor activity, drinking patterns, thermoregulatory cial support. 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Journal

TemperatureTaylor & Francis

Published: Sep 30, 2014

Keywords: behavioral flexibility; climate change physiology; micro-evolution; microevolution; phenotypic plasticity; physiological acclimation; physiological acclimatization; range shift; temperature

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