Using thermoregulatory profiles to assess climate change vulnerability in an arboreal tropical bat: heterothermy may be a pre-adaptive advantage

Welman, Shaun; Tuen, Andrew Alek; Lovegrove, Barry G.

doi:10.3354/cr01496

Cited by 11 publications

(12 citation statements)

References 79 publications

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“…A reduction of metabolic rate (MR) is accompanied by reduced water consumption through respiration, defecation, urine formation and metabolic heat dissipation [26][27][28], which could permit torpid animals to tolerate greater heat loads than euthermic ones. Nonetheless, how mammals perform and thermoregulate at high temperatures remains poorly understood [14,25,[29][30][31]], yet is essential to predict their responses to rising temperatures. Global warming confronts many small mammals more regularly with fatal mismatches between environmental conditions and their physiological limitations.…”

Section: Introductionmentioning

confidence: 99%

Tropical bats counter heat by combining torpor with adaptive hyperthermia

Reher

Dausmann

2021

Proc. R. Soc. B.

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Many tropical mammals are vulnerable to heat because their water budget limits the use of evaporative cooling for heat compensation. Further increasing temperatures and aridity might consequently exceed their thermoregulatory capacities. Here, we describe two novel modes of torpor, a response usually associated with cold or resource bottlenecks, as efficient mechanisms to counter heat. We conducted a field study on the Malagasy bat Macronycteris commersoni resting in foliage during the hot season, unprotected from environmental extremes. On warm days, the bats alternated between remarkably short micro-torpor bouts and normal resting metabolism within a few minutes. On hot days, the bats extended their torpor bouts over the hottest time of the day while tolerating body temperatures up to 42.9°C. Adaptive hyperthermia combined with lowered metabolic heat production from torpor allows higher heat storage from the environment, negates the need for evaporative cooling and thus increases heat tolerance. However, it is a high-risk response as the torpid bats cannot defend body temperature if ambient temperature increases above a critical/lethal threshold. Torpor coupled with hyperthermia and micro-torpor bouts broaden our understanding of the basic principles of thermal physiology and demonstrate how mammals can perform near their upper thermal limits in an increasingly warmer world.

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Section: Introductionmentioning

confidence: 99%

Tropical bats counter heat by combining torpor with adaptive hyperthermia

Reher

Dausmann

2021

Proc. R. Soc. B.

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“…Anthropogenic habitat loss has myriad effects on animal physiology and behavior (Ellis, McWhorter, & Maron, 2012; Seebacher & Franklin, 2012). Altered physical environments affect animal diets (Cristóbal‐Azkarate & Arroyo‐Rodríguez, 2007), exposure to disease (Ekanayake et al., 2006; Goldberg, Gillespie, Rwego, Estoff, & Chapman, 2008), thermoregulation (Kearney, Shine, & Porter, 2009; Welman, Tuen, & Lovegrove, 2017), and social interactions (Clarke, Collins, & Zucker, 2002; Mbora, Wieczkowski, & Munene, 2009), potentially limiting reproductive success and/or survival (Ellis et al., 2012; Seebacher & Franklin, 2012). However, some species are more resilient than others.…”

Section: Introductionmentioning

confidence: 99%

Gut microbiome, diet, and conservation of endangered langurs in Sri Lanka

et al. 2020

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Understanding the mechanisms by which organisms respond to environmental change is critical to conservation biology. Recent research indicates that the gut microbiome may mediate mammalian responses to the environment and can be used as a biomarker to understand host ecological strategies. Here, we explore the relationship between the gut microbiome, host dietary niche, and potential resilience to habitat alteration using two closely related, sympatric non-human primate species: the tufted gray langur (Semnopithecus priam) and the purple-faced langur (Semnopithecus vetulus). The gray langur is suspected to be a habitat generalist less perturbed by anthropogenic disturbance, while the purple-faced langur is suspected to be a specialist more sensitive to disturbance. To test these characterizations, we assessed the gut microbiome using 16S rRNA gene amplicon sequencing of fecal samples collected from Kaludiyapokuna Forest Reserve, Sri Lanka (gray langur n = 50 samples, purple-faced langur n = 7 samples). Our results demonstrate that despite strong gut microbial similarities, gray langurs had a more diverse gut microbiome that harbored Prevotella and Akkermansia, taxa involved in starch degradation, while the purplefaced langur gut microbiome harbored Roseburia, Clostridium, and Ruminococcus, taxa involved in processing plant structural carbohydrates. Compared to related species in other locations, both Sri Lankan langurs harbored more pathogenic bacteria. These differences suggest that gray langurs have more generalist diets, making them more resilient to anthropogenic change, but also indicate that they are not impervious to human encroachment. Our findings suggest that microbiome analyses are an important tool for langur ecology and conservation, and should be integrated into ongoing studies.

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“…Above this threshold, only evaporative cooling can regulate T b , which is unfavourable in a dry region if water reserves are unable to be replenished (Mitchell et al 2018 ). Entering torpor at high T a reduces metabolic heat and water production, allowing higher rates of heat from the environment to be stored in the body via facultative hyperthermia (Lovegrove et al 2014 ; Welman et al 2017 ; Reher and Dausmann 2021 ). Compared to the bats roosting in the cave at near stable conditions, it appears the forest bats in our study used this strategy to mitigate heat and water stress.…”

Section: Discussionmentioning

confidence: 99%

Disparate roost sites drive intraspecific physiological variation in a Malagasy bat

et al. 2021

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Many species are widely distributed and individual populations can experience vastly different environmental conditions over seasonal and geographic scales. With such a broad ecological reality, datasets with limited spatial and temporal resolution may not accurately represent a species and could lead to poorly informed management decisions. Because physiological flexibility can help species tolerate environmental variation, we studied the physiological responses of two separate populations of Macronycteris commersoni, a bat widespread across Madagascar, in contrasting seasons. The populations roost under the following dissimilar conditions: either a hot, well-buffered cave or within open foliage, unprotected from the local weather. We found that flexible torpor patterns, used in response to prevailing ambient temperature and relative humidity, were central to keeping energy budgets balanced in both populations. While bats’ metabolic rate during torpor and rest did not differ between roosts, adjusting torpor frequency, duration and timing helped bats maintain body condition. Interestingly, the exposed forest roost induced extensive use of torpor, which exceeded the torpor frequency of overwintering bats that stayed in the cave for months and consequently minimised daytime resting energy expenditure in the forest. Our current understanding of intraspecific physiological variation is limited and physiological traits are often considered to be fixed. The results of our study therefore highlight the need for examining species at broad environmental scales to avoid underestimating a species’ full capacity for withstanding environmental variation, especially in the face of ongoing, disruptive human interference in natural habitats.

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Using thermoregulatory profiles to assess climate change vulnerability in an arboreal tropical bat: heterothermy may be a pre-adaptive advantage

Cited by 11 publications

References 79 publications

Tropical bats counter heat by combining torpor with adaptive hyperthermia

Tropical bats counter heat by combining torpor with adaptive hyperthermia

Gut microbiome, diet, and conservation of endangered langurs in Sri Lanka

Disparate roost sites drive intraspecific physiological variation in a Malagasy bat

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