Exertion-induced fatigue and thermoregulation in the cold

Cold exposure facilitates body heat loss which can reduce body temperature, unless mitigated by enhanced heat conservation or increased heat production. When behavioral strategies inadequately defend body temperature, vasomotor and thermogenic responses are elicited, both of which are modulated if not mediated by sympathetic nervous activation. Both exercise and shivering increase metabolic heat production which helps offset body heat losses in the cold. However, exercise also increases peripheral blood flow, in turn facilitating heat loss, an effect that can persist for some time after exercise ceases. Whether exercise alleviates or exacerbates heat debt during cold exposure depends on the heat transfer coefficient of the environment, mode of activity and exercise intensity. Prolonged exhaustive exercise leading to energy substrate depletion could compromise maintenance of thermal balance in the cold simply by precluding continuation of further exercise and the associated thermogenesis. Hypoglycemia impairs shivering, but this appears to be centrally mediated, rather than a limitation to peripheral energy metabolism. Research is equivocal regarding the importance of muscle glycogen depletion in explaining shivering impairments. Recent research suggests that when acute exercise leads to fatigue without depleting energy stores, vasoconstrictor responses to cold are impaired, thus body heat conservation becomes degraded. Fatigue that was induced by chronic overexertion sustained over many weeks, appeared to delay the onset of shivering until body temperature fell lower than when subjects were rested, as well as impair vasoconstrictor responses. When heavy physical activity is coupled with underfeeding for prolonged periods, the resulting negative energy balance leads to loss of body mass, and the corresponding reduction in tissue insulation, in turn, compromises thermal balance by facilitating conductive transfer of body heat from core to shell. The possibility that impairments in thermoregulatory responses to cold associated with exertional fatigue are mediated by blunted sympathetic nervous responsiveness to cold is suggested by some experimental observations and merits further study.     

The complex drivers of thermal acclimation and breadth in ectotherms

Thermal acclimation capacity, the degree to which organisms can alter their optimal performance temperature and critical thermal limits with changing temperatures, reflects their ability to respond to temperature variability and thus might be important for coping with global climate change. Here, we combine simulation modelling with analysis of published data on thermal acclimation and breadth (range of temperatures over which organisms perform well) to develop a framework for predicting thermal plasticity across taxa, latitudes, body sizes, traits, habitats and methodological factors. Our synthesis includes > 2000 measures of acclimation capacities from > 500 species of ectotherms spanning fungi, invertebrates, and vertebrates from freshwater, marine and terrestrial habitats. We find that body size, latitude, and methodological factors often interact to shape acclimation responses and that acclimation rate scales negatively with body size, contributing to a general negative association between body size and thermal breadth across species. Additionally, we reveal that acclimation capacity increases with body size, increases with latitude (to mid‐latitudinal zones) and seasonality for smaller but not larger organisms, decreases with thermal safety margin (upper lethal temperature minus maximum environmental temperatures), and is regularly underestimated because of experimental artefacts. We then demonstrate that our framework can predict the contribution of acclimation plasticity to the IUCN threat status of amphibians globally, suggesting that phenotypic plasticity is already buffering some species from climate change.     

Influence of altitude, habitat and microhabitat on thermal adaptation of cicadas from Southwest Texas (Hemiptera: Cicadidae)

The thermal responses of 12 cicada species inhabiting Big Bend National Park, Texas, USA are investigated to determine the influence of altitude, habitat and microhabitat. The park provides an opportunity to analyze the thermal responses in animals from a variety of habitats and altitudinal gradients within a limited geographic range. The data suggest that thermal responses of cicadas are adaptations to their specific habitats. No thermal responses are significantly correlated with body size. The maximum voluntary tolerance temperature (an upper behavioral thermoregulatory point) and heat torpor temperatures show significant correlations with altitude. Variability in thermal responses can also be related to the characteristics of the microhabitat selected or the behavioral pattern of a species.     

Increased temperature reduces herbivore host‐plant quality

Globally increasing temperatures may strongly affect insect herbivore performance, as their growth and development is directly linked to ambient temperature as well as host‐plant quality. In contrast to direct effects of temperature on herbivores, indirect effects mediated via thermal effects on host‐plant quality are only poorly understood, despite having the potential to substantially impact performance and thereby to alter responses to the changing climatic conditions. We here use a full‐factorial design to explore the direct (larvae were reared at 17 °C or 25 °C) and indirect effects (host plants were reared at 17 °C or 25 °C) of temperature on larval growth and life‐history traits in the temperate‐zone butterfly Pieris napi. Direct temperature effects reflected the common pattern of prolonged development and increased body mass at lower temperatures. At the higher temperature, efficiency of converting food into body matter was much reduced being accompanied by an increased food intake, suggesting compensatory feeding. Indirect temperature effects were apparent as reduced body mass, longer development time, an increased food intake, and a reduced efficiency of converting food into body matter in larvae feeding on plants grown at the higher temperature, thus indicating poor host‐plant quality. The effects of host‐plant quality were more pronounced at the higher temperature, at which compensatory feeding was much less efficient. Our results highlight that temperature‐mediated changes in host‐plant quality are a significant, but largely overlooked source of variation in herbivore performance. Such effects may exaggerate negative effects of global warming, which should be considered when trying to forecast species' responses to climate change.     

Comparative thermal adaptation in cicadas (Hemiptera: Cicadidae) inhabiting Mediterranean ecosystems

The thermal responses of cicadas inhabiting the Mediterranean ecosystems in Europe, North America, South Africa, and Australia are investigated. A total of 37 species and two subspecies from 17 genera representing eight tribes and three subfamilies of cicadas are investigated. The analysis includes species that are restricted to the Mediterranean ecosystem as well as those which also inhabit additional environments. The data suggest that cicadas adapt to the climate type regardless of particular types of plants within the various Mediterranean communities. Similarly, cicada thermal responses are independent of body size or taxonomic affinities. There is a wider range of body temperatures for the maximum voluntary tolerance temperature than for heat torpor or minimum flight temperatures. This diversity seems to be determined by the subdivision of the habitat used and the behavior of the species. All species possess relatively elevated heat torpor temperatures adapting to the general thermal characteristics of the Mediterranean ecosystem. The data suggest that cicadas adapt to the Mediterranean climate type regardless of the diversity of particular types of plants within the various communities, of body size or of taxonomic position.     

Thermal energy conduction in a honey bee comb due to cell-heating bees

Theoretical analysis and numerical calculations are performed to characterize the unsteady two-dimensional conduction of thermal energy in an idealized honey bee comb. The situation explored corresponds to a comb containing a number of brood cells occupied by pupae. These cells are surrounded by other cells containing pollen which, in turn, are surrounded (above) by cells containing honey and (below) by vacant cells containing air. Up to five vacant cells in the brood region can be occupied by cell-heating bees which, through the isometrical contraction of their flight muscles, can generate sufficient energy to raise their body temperatures by a few degrees. In this way, the cell-heating bees alter the heat flux and temperature distributions in the brood region so as to maintain conditions that benefit the pupae. The calculations show that the number of cell-heating bees significantly affects the magnitude, time rate of change, and spatial distribution of temperature throughout the comb. They also reveal a vertically aligned asymmetry in the spatial distribution of temperature that is due to the large heat capacity and thermal conductivity of honey relative to air, whereby air-filled cells experience larger temperature increases than honey-filled cells. Analysis shows that convection and radiation represent negligible modes of thermal energy transfer at all levels in the problem considered. Also, because of its small thickness, the wax wall of a comb cell simultaneously presents negligible resistance to conduction heat transfer normal to it and very large resistance along it. As a consequence the walls of a cell play no thermal role, but simply serve as mechanical supports for the materials they contain.     

An assessment of skin temperature gradients in a tropical primate using infrared thermography and subcutaneous implants

Infrared thermography has become a useful tool to assess surface temperatures of animals for thermoregulatory research. However, surface temperatures are an endpoint along the body's core-shell temperature gradient. Skin and fur are the peripheral tissues most exposed to ambient thermal conditions and are known to serve as thermosensors that initiate thermoregulatory responses. Yet relatively little is known about how surface temperatures of wild mammals measured by infrared thermography relate to subcutaneous temperatures. Moreover, this relationship may differ with the degree that fur covers the body. To assess the relationship between temperatures and temperature gradients in peripheral tissues between furred and bare areas, we collected data from wild mantled howling monkeys (Alouatta palliata) in Costa Rica. We used infrared thermography to measure surface temperatures of the furred dorsum and bare facial areas of the body, recorded concurrent subcutaneous temperatures in the dorsum, and measured ambient thermal conditions via a weather station. Temperature gradients through cutaneous tissues (subcutaneous-surface temperature) and surface temperature gradients (surface-ambient temperature) were calculated. Our results indicate that there are differences in temperatures and temperature gradients in furred versus bare areas of mantled howlers. Under natural thermal conditions experienced by wild animals, the bare facial areas were warmer than temperatures in the furred dorsum, and cutaneous temperature gradients in the face were more variable than the dorsum, consistent with these bare areas acting as thermal windows. Cutaneous temperature gradients in the dorsum were more closely linked to subcutaneous temperatures, while facial temperature gradients were more heavily influenced by ambient conditions. These findings indicate that despite the insulative properties of fur, for mantled howling monkeys surface temperatures of furred areas still demonstrate a relationship with subcutaneous temperatures. Given that most mammals possess dense fur, this provides insight for using infrared imaging in thermoregulatory studies of wild animals lacking bare skin.     

Ambient Temperature Influences Australian Native Stingless Bee (Trigona carbonaria) Preference for Warm Nectar

The interaction between flowers and insect pollinators is an important aspect of the reproductive mechanisms of many plant species. Several laboratory and field studies indicate that raising flower temperature above ambient can be an advantage in attracting pollinators. Here we demonstrate that this preference for warmer flowers is, in fact, context-dependent. Using an Australian native bee as a model, we demonstrate for the first time a significant shift in behaviour when the ambient temperature reaches 34°C, at which point bees prefer ambient temperature nectar over warmer nectar. We then use thermal imaging techniques to show warmer nectar maintains the flight temperature of bees during the period of rest on flowers at lower ambient temperatures but the behavioural switch is associated with the body temperature rising above that maintained during flight. These findings suggest that flower-pollinator interactions are dependent upon ambient temperature and may therefore alter in different thermal environments.     

Neurotransmitter mediation of morphine hypothermia in rats.

Subcutaneous (sc) injections of morphine (10 mg/kg) caused transient falls in body temperature of rats. The hypothermic responses to morphine were inhibited by the prior intracerebroventricular (icv) administration of methysergide or phentolamine. Methysergide treatment also prevented hypothermic responses to icv 5-hydroxytryptamine (5-HT), but not responses to icv norepinephrine or dopamine. Phentolamine inhibited responses to icv norepinephrine and dopamine, but not to 5-HT. Haloperidol, which inhibited responses to icv dopamine, did not alter the hypothermia induced by sc or icv morphine. The results indicate that both 5-HT and norepinephrine participate as central mediators of morphine-induced hypothermia.     

Development time and body size in Eupolyphaga sinensis along a latitudinal gradient from China

The responses of organisms to temperature variations may be via short term responses of the phenotype (phenotypic plasticity), or they could involve long-term evolutionary change and adaptation (via selection) to the genotype. These could involve changes to the mean size of the animal or to the thermal reaction norm. We examined the effects of various temperatures (of 22, 25, 28, and 31 °C) on development time, adult body size and preadult survivorship in three populations of the cockroach, Eupolyphaga sinensis (Walker), collected at different latitudes. We found substantial temperature-induced plasticity in development time, body size, and preadult survivorship, indicating that developmental temperatures have strong impacts on growth and life history traits of E. sinensis. Genetic differences for development time, body size, and preadult survivorship were detected among populations, and the three traits exhibited highly significant variations in the responses of different populations to various temperature conditions, indicating genetic differences among populations in terms of thermal reaction norms. We also found that two populations seem to support the beneficial acclimation hypothesis whereas the third mid-latitude population does not. The results are likely because of differences in season length and voltinism, indicating that not only temperature regime but also its interactions with generation time (and development time), voltinism, and season length are likely to have considerable effects on insect development time and body size. Overall, changes in development time, body size, and preadult survivorship in E. sinensis can all be regarded as adaptations to changing thermal regimes.     

Contribution of thermal and nonthermal factors to the regulation of body temperature in humans.

The set point has been used to define the regulated level of body temperature, suggesting that displacements of core temperature from the set point initiate heat production (HP) and heat loss (HL) responses. Human and animal experiments have demonstrated that the responses of sweating and shivering do not coincide at a set point but rather establish a thermoeffector threshold zone. Neurophysiological studies have demonstrated that the sensor-to-effector pathways for HP and HL overlap and, in fact, mutually inhibit each other. This reciprocal inhibition theory, presumably reflecting the manner in which thermal factors contribute to homeothermy in humans, does not incorporate the effect of nonthermal factors on temperature regulation. The present review examines the actions of these nonthermal factors within the context of neuronal models of temperature regulation, suggesting that examination of these factors may provide further insights into the nature of temperature regulation. It is concluded that, although there is no evidence to doubt the existence of the HP and HL pathways reciprocally inhibiting one another, it appears that such a mechanism is of little consequence when comparing the effects of nonthermal factors on the thermoregulatory system, since most of these factors seem to exert their influence in the region after the reciprocal cross-inhibition. At any given moment, both thermal and several nonthermal factors will be acting on the thermoregulatory system. It may, therefore, not be appropriate to dismiss the contribution of either when discussing the regulation of body temperature in humans.     

Behavioral responses to immune-system activation in an anuran (the cane toad, Bufo marinus): field and laboratory studies

The challenges posed by parasites and pathogens evoke behavioral as well as physiological responses. Such behavioral responses are poorly understood for most ectothermic species, including anuran amphibians. We quantified effects of simulated infection (via injection of bacterial lipopolysaccharide [LPS]) on feeding, activity, and thermoregulation of cane toads Bufo marinus within their invasive range in tropical Australia. LPS injection reduced feeding rates in laboratory trials. For toads in outdoor enclosures, LPS injection reduced activity and shifted body temperature profiles. Although previous research has attributed such thermal shifts to behavioral fever (elevated body temperatures may help fight infection), our laboratory studies suggest instead that LPS-injected toads stopped moving. In a thermal gradient, LPS-injected toads thus stayed close to whichever end of the gradient (hot or cold) they were first introduced; the introduction site (rather than behavioral thermoregulation) thus determined body temperature regimes. Shifts in thermal profiles of LPS-injected toads in outdoor enclosures also were a secondary consequence of inactivity. Thus, the primary behavioral effects of an immune response in cane toads are reduced rates of activity and feeding. Thermoregulatory modifications also occur but only as a secondary consequence of inactivity.     

EVOLUTION IN A CONSTANT ENVIRONMENT: THERMAL FLUCTUATIONS AND THERMAL SENSITIVITY OF LABORATORY AND FIELD POPULATIONS OF MANDUCA SEXTA

Adaptation to temporal variation in environmental conditions is widespread. Whether evolution in a constant environment alters adaptation to temporal variation is relatively unexplored. We examine how constant and diurnally fluctuating temperature conditions affect life-history traits in two populations of the tobacco hornworm, Manduca sexta : a field population that routinely experiences fluctuating temperatures; and a laboratory population (derived from this field population in the 1960s) maintained at a constant temperature for more than 250 generations. Our experiments demonstrate that diurnal fluctuations significantly alter body size and development time in both populations, and confirm that these populations differ in their responses to a mean temperature. However, we found no evidence for population divergence in responses to diurnal temperature fluctuations. We suggest that mean and extreme temperatures may act as more potent selective forces on thermal reaction norms than temperature variation per se.     

EVOLUTION OF SPRINT SPEED IN LACERTID LIZARDS: MORPHOLOGICAL,PHYSIOLOGICAL, AND BEHAVIORAL COVARIATION

Organismal performance abilities occupy a central position in phenotypic evolution; they are determined by suites of interacting lower-level traits (e.g., morphology and physiology) and they are a primary focus of natural selection. The mechanisms by which higher levels of organismal performance are achieved during evolution are therefore fundamentally important for understanding correlated evolution in general and coadaptation in particular. Here we address correlated evolution of morphological, physiological, and behavioral characteristics that influence interspecific variation in sprint speed in a clade of lacertid lizards. Phylogenetic analyses using independent contrasts indicate that the evolution of high maximum sprinting abilities (measured on a photocell-timed racetrack) has occurred via the evolution of (1) longer hind limbs relative to body size, and (2) a higher physiologically optimum temperature for sprinting. For ectotherms, which experience variable body temperatures while active, sprinting abilities in nature depend on both maximum capacities and relative performance levels (i.e., percent of maximum) that can be attained. With respect to temperature effects, relative performance levels are determined by the interaction between thermal physiology and thermoregulatory behavior. Among the 13 species or subspecies of lizards in the present study, differences in the optimal temperature for sprinting (body temperature at which lizards run fastest) closely matched interspecific variation in median preferred body temperature (measured in a laboratory photothermal gradient), indicating correlated evolution of thermal physiology and thermal preferences. Variability of the preferred body temperatures maintained by each species is, across species, negatively correlated with the thermal-performance breadth (range of body temperatures over which lizards can run relatively fast). This pattern leads to interspecific differences in the levels of relative sprint speed that lizards are predicted to attain while active at their preferred temperatures. The highest levels of predicted relative performance are achieved by species that combine a narrow, precise distribution of preferred temperatures with the ability to sprint at near-maximum speeds over a wide range of body temperatures. The observed among-species differences in predicted relative speed were positively correlated with the interspecific variation in maximum sprinting capacities. Thus, species that attain the highest maximum speeds are (1) also able to run at near-maximum levels over a wide range of temperatures and (2) also maintain body temperatures within a narrow zone near the optimal temperature for sprinting. The observed pattern of correlated evolution therefore has involved traits at distinct levels of biological organization, that is, morphology, physiology, and behavior; and trade-offs are not evident. We hypothesize that this particular trait combination has evolved in response to coadaptational selection pressures. We also discuss our results in the context of possible evolutionary responses to global climatic change.     

The influence of hypoxia on the thermal sensitivity of skin colouration in the bearded dragon, Pogona vitticeps

One physiological mechanism used by reptiles to remain within thermal optima is their ability to reversibly alter skin colour, imparting changes in overall reflectance, and influencing the rate of heat gain from incident radiation. The ability to lighten or darken their skin is caused by the movement of pigment within the dermal chromatophore cells. Additionally, lizards, as ectotherms, significantly lower their preferred body temperatures when experiencing stressors such as hypoxia. This decrease in preferred temperature has been proposed to be the result of a downward adjustment of the thermal set-point, the temperature around which the body temperature is typically defended. We tested the hypothesis that lightening of the skin in lizards would be modified by hypoxia in a manner consistent with the known reduction in preferred temperatures. Skin colouration values of the dorsal skin of bearded dragons were analysed at three different levels of oxygen (20.8, 9.9 and 4.9 kPa) and at temperatures spanning the preferred temperature range (30, 32, 34, 36, 38 and 40 C). Hypoxic lizards lightened their skin at lower ambient temperatures more than normoxic ones, and in an oxygen-dependent fashion. The orchestrated adjustment of skin reflectance suggests that this physiological trait is being regulated at a new and lower set-point. Evidence from this study demonstrates that skin colouration plays a role in body temperature regulation and that the reduction in temperature set-point so prevalent in hypoxia is also manifested in this physiological trait.     

Thermal ecology and physiology of an elongate and semi-fossorial arthropod,the bark centipede

Organismal performance is strongly linked to temperature because of the fundamental thermal dependence of chemical reaction rates. However, the relationship between the environment and body temperature can be altered by morphology and ecology. In particular, body size and body shape can impact thermal inertia, as high surface area to volume ratios will possess low thermal mass. Habitat type can also influence thermal physiology by altering the opportunity for thermoregulation. We studied the thermal ecology and physiology of an elongate invertebrate, the bark centipede (Scolopocryptops sexspinosus). We characterized field body temperature and environmental temperature distributions, measured thermal tolerance limits, and constructed thermal performance curves for a population in southern Georgia. We found evidence that bark centipedes behaviorally thermoregulate, despite living in sheltered microhabitats, and that performance was maintained over a broad range of temperatures (over 20 °C). However, both the thermal optimum for performance and upper thermal tolerance were much higher than mean body temperature in the field. Together, these results suggest that centipedes can thermoregulate and maintain performance over a broad range of temperatures but are sensitive to extreme temperatures. More broadly, our results suggest that wide performance breadth could be an adaptation to thermal heterogeneity in space and time for a species with low thermal inertia.     

Thermoregulation and the effect of body temperature on call temporal parameters in the cicada Diceroprocta olympusa (Homoptera: Cicadidae)

We investigated the thermoregulatory behavior, thermal responses (minimum flight, maximum voluntary tolerance and heat torpor temperatures) and the effect of body temperature (T(b)) on call parameters in the cicada Diceroprocta olympusa (Walker). Regression of T(b) as a function of ambient (T(a)) or perch temperatures (T(p)) suggests thermoregulation is occurring. Thermoregulation occurs through behavioral changes that alter the uptake of solar radiation. T(p) is a better predictor of T(b) than is T(a). Thermal responses (minimum flight temperature 20.4 degrees C, maximum voluntary tolerance temperature 37 degrees C, and heat torpor temperature 46.7 degrees C) may be related to the humid, grassland habitat of the species. In contrast to other acoustic insects, no significant relationship was found between the temporal parameters of the calling song and T(b) within the population of D. olympusa.     

Influence of seasonal timing on thermal ecology and thermal reaction norm evolution in Wyeomyia smithii

Evolutionary changes in the seasonal timing of life-history events can alter a population's exposure to seasonally variable environmental factors. We illustrate this principle in Wyeomyia smithii by showing that: (1) geographic divergence in diapause timing reduces differences among populations in the thermal habitat experienced by nondiapause stages; and (2) the thermal habitat of the growing season is more divergent at high compared with low temperatures with respect to daily mean temperatures. Geographic variation in thermal reaction norms for development time was greater in a warm compared with a cool rearing treatment, mirroring the geographic trend in daily mean temperature. Geographic variation in body size was unrelated to geographic temperature variation, but was also unrelated to development time or fecundity. Our results suggest that proper interpretation of geographic trends may often require detailed knowledge of life-history timing.     

What do warming waters mean for fish physiology and fisheries?

Environmental signals act primarily on physiological systems, which then influence higher-level functions such as movement patterns and population dynamics. Increases in average temperature and temperature variability associated with global climate change are likely to have strong effects on fish physiology and thereby on populations and fisheries. Here we review the principal mechanisms that transduce temperature signals and the physiological responses to those signals in fish. Temperature has a direct, thermodynamic effect on biochemical reaction rates. Nonetheless, plastic responses to longer-term thermal signals mean that fishes can modulate their acute thermal responses to compensate at least partially for thermodynamic effects. Energetics are particularly relevant for growth and movement, and therefore for fisheries, and temperature can have pronounced effects on energy metabolism. All energy (ATP) production is ultimately linked to mitochondria, and temperature has pronounced effects on mitochondrial efficiency and maximal capacities. Mitochondria are dependent on oxygen as the ultimate electron acceptor so that cardiovascular function and oxygen delivery link environmental inputs with energy metabolism. Growth efficiency, that is the conversion of food into tissue, changes with temperature, and there are indications that warmer water leads to decreased conversion efficiencies. Moreover, movement and migration of fish relies on muscle function, which is partially dependent on ATP production but also on intracellular calcium cycling within the myocyte. Neuroendocrine processes link environmental signals to regulated responses at the level of different tissues, including muscle. These physiological processes within individuals can scale up to population responses to climate change. A mechanistic understanding of thermal responses is essential to predict the vulnerability of species and populations to climate change.