As ecosystems undergo global changes, there is increasing interest in understanding how organisms respond to changing environments. Recent evidence drawn from available vertebrate studies suggests that most of the phenotypic responses to climate change would be due to plasticity. We hypothesize that organisms that have evolved in unpredictable environments inform us about the mechanisms of phenotypic plasticity which provide an adaptive response to climate instability. As climate changes increase climatic hazards, these resilience mechanisms are expected to spread within species, populations and communities. We review studies that have demonstrated the importance of phenotypic plasticity in different life-history traits in overcoming climate uncertainty. We focus on organisms from unstable, recurrently energetically restrictive environments which possess a variety of morphological, physiological and/or behavioural adaptations to climate-driven selective pressures. First, we treat plastic morphological changes in response to fluctuating food availability. Adjustment of morphometric traits and/or organ size to energy supply would be essential in harsh environments. Second, we review the role of flexible energy-saving mechanisms, such as daily torpor, hibernation and energy storage, in overcoming climate-driven energetic shortages. Lastly, we address the role of plastic modulation of reproduction in fine-tuning the energy allocation to offspring production according to environmental conditions, with an emphasis on opportunistic breeding. Overall, we predict that species (or genotypes) possessing these efficient physiological mechanisms of resilience to unpredictable water and food fluctuations will be selectively advantaged in the face of increasing climatic instability.
There is some urgency in the necessity to incorporate physiological data into mechanistic, trait-based, demographic climate change models. Physiological responses at the individual level provide the mechanistic link between environmental changes and individual performances and hence population dynamics. Here we consider the causal relationship between ambient temperature (Ta) and metabolic rate (MR), namely, the Arrhenius effect, which is directly affected by global warming through increases in average global air temperatures and the increase in the frequency and intensity of extreme climate events. We measured and collated data for several small, free-ranging tropical arboreal mammals and evaluated their vulnerability to Arrhenius effects and putative heat stress associated with climate change. Skin temperatures (Tskin) were obtained from free-ranging tarsiers (Tarsius syrichta) on Bohol Island, Philippines. Core body temperature (Tb) was obtained from the greater hedgehog tenrec (Setifer setosus) and the gray brown mouse lemur (Microcebus ravelobensis) from Ankarafantsika, Madagascar. Tskin for another mouse lemur, Microcebus griseorufus, was obtained from the literature. All four species showed evidence of hyperthermia during the daytime rest phase in the form of either Tskin or Tb that was higher than the normothermic Tb during the nighttime active phase. Potentially, tropical arboreal mammals with the lowest MRs and Tb, such as tarsiers, are the most vulnerable to sustained heat stress because their Tb is already close to Ta. Climate change may involve increases in MRs due to Arrhenius effects, especially during the rest phase or during torpor and hibernation. The most likely outcome of increased Arrhenius effects with climate change will be an increase in energy expenditure at the expense of other critical functions such as reproduction or growth and will thus affect fitness. However, we propose that these hypothetical Arrhenius costs can be, and in some species probably are, offset by the use of hyperthermic daily torpor, that is, hypometabolism at high Ta.
SUMMARYAs ecosystems undergo changes worldwide, physiological flexibility is likely to be an important adaptive response to increased climate instability. Extreme weather fluctuations impose energetical constraints such as unpredictable food shortage. We tested how grey mouse lemurs (Microcebus murinus) could adjust their daily heterothermy and locomotor activity to these 'energetic accidents' with a food restriction experiment. The experimental design consisted of acute calorie restriction (2weeks, 80% restriction) in the middle of winter, after a fattening season with low (11weeks, 40% restriction) versus high (ad libitum) food availability. This design aimed at simulating the combined effects of the quality of the fattening season (acclimation effect) and a sudden, severe food shortage during the lean season. Hour of start and duration of torpor were the most flexible components of energy savings, increasing in response to the acute food shortage with facilitation by chronic restriction (acclimation effect). Modulations of locomotor activity did not support the hypothesis of energy savings, as total locomotor activity was not reduced. Nonetheless, acutely restricted individuals modified their temporal pattern of locomotor activity according to former food availability. We provide the first experimental evidence of different temporal levels of flexibility of energy-saving mechanisms in a heterotherm exposed to food shortage. The acclimation effect of past food scarcity suggests that heterothermic organisms are better able to respond to unpredicted food scarcity during the lean season. The flexible control of energy expenditure conferred by heterothermy may facilitate the plastic response of heterothermic species to more frequent climatic hazards. Supplementary material available online at
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