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Low desiccation and thermal tolerance constrains a terrestrial amphibian to a rare and disappearing microclimate niche.

ABSTRACT: Drier and hotter conditions caused by climate change threaten species that exist close to their physiological limits, as well as those with limited ability to move. Habitat specialists may also be particularly vulnerable if they have specific abiotic requirements. Here we assess whether thermal and hydric constraints can explain the highly restricted and declining distributions of the critically endangered terrestrial-breeding frog, Geocrinia alba. We also evaluate the species' vulnerability to climate change based on the similarity of current microclimatic conditions to their physiological limits. We found that G. alba had low thresholds of thermal and desiccation tolerance relative to other anuran species. The estimated thermal optimum (T_opt ) and critical thermal maxima (CT_max ) were 23.3°C and 29.6°C, respectively, and adult frogs had an absorption threshold (AT, the lowest water potential at which water can be absorbed from a substrate) of -50 kPa, the lowest recorded for an amphibian. Comparing environmental conditions and water loss in the field using agar models showed that riparian habitats where frogs occur provide a unique microclimate in the landscape, offering significantly lower desiccation risk during extreme summer conditions compared to immediately adjacent riparian and terrestrial habitats. Monitoring of microclimate conditions within occupied frog habitats over 2 years showed that in extreme dry and hot years the AT was exceeded at six of eight sites, and T_opt was exceeded at two of eight sites. Given their specific physiological limits, the apparent rarity of suitable microclimates and a regional drying-warming trend, we suggest that G. alba occupies a potentially disappearing niche and may be indicative of other habitat specialists that rely on ephemeral drainages. More broadly, this study highlights that desiccation thresholds may tightly constrain amphibian distributions and need to be considered along with thermal tolerance thresholds when predicting the impacts of climate change.

SUBMITTER: Hoffmann EP

PROVIDER: S-EPMC8084025 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:We tested the hypothesis that differences in temperature and desiccation tolerances of eggs of the container-dwelling mosquitoes Aedes albopictus and Aedes aegypti influence whether invading A. albopictus coexist with or exclude A. aegypti in Florida. In the laboratory, egg mortality through 30 days for A. albopictus was strongly temperature and humidity dependent, with low humidity and high temperature producing greatest mortality. In contrast, mortality through 30 days and through 60 days for A. aegypti was very low and independent of temperature and humidity. Mortality through 90 days for A. aegypti showed significant effects of both temperature and humidity. In the field, the proportion of vases occupied by A. albopictus was significantly lower at four of six sites at the start of the wet season (after a dry period) versus well into the wet season (after containers had held water for weeks). The proportion of vases occupied by A. aegypti was independent of when during the wet season vases were sampled. These results imply that dry periods cause disproportionately greater mortality of A. albopictus eggs compared to A. aegypti eggs. Container occupancy at tire and cemetery sites was significantly related to two principal components derived from longterm average climate data. Occupancy of containers by A. albopictus was greatest at cool sites with little or no dry season, and decreased significantly with increasing mean temperature and increasing number of dry months. In contrast, occupancy of containers by A. aegypti was lowest at cool sites with little or no dry season, and increased significantly with increasing mean temperature and increasing dry season length, and decreased significantly with total precipitation and number of wet months. We suggest that local coexistence of these species is possible because warm, dry climates favor A. aegypti and alleviate effects of competition from A. albopictus via differential mortality of A. albopictus eggs.

Project description:BackgroundCells and organisms typically cannot survive in the absence of water. However, some animals including nematodes, tardigrades, rotifers, and some arthropods are able to survive near-complete desiccation. One class of proteins known to play a role in desiccation tolerance is the late embryogenesis abundant (LEA) proteins. These largely disordered proteins protect plants and animals from desiccation. A multitude of studies have characterized stress-protective capabilities of LEA proteins in vitro and in heterologous systems. However, the extent to which LEA proteins exhibit such functions in vivo, in their native contexts in animals, is unclear. Furthermore, little is known about the distribution of LEA proteins in multicellular organisms or tissue-specific requirements in conferring stress protection. Here, we used the nematode C. elegans as a model to study the endogenous function of an LEA protein in an animal.ResultsWe created a null mutant of C. elegans LEA-1, as well as endogenous fluorescent reporters of the protein. LEA-1 mutant animals formed defective dauer larvae at high temperature. We confirmed that C. elegans lacking LEA-1 are sensitive to desiccation. LEA-1 mutants were also sensitive to heat and osmotic stress and were prone to protein aggregation. During desiccation, LEA-1 expression increased and became more widespread throughout the body. LEA-1 was required at high levels in body wall muscle for animals to survive desiccation and osmotic stress, but expression in body wall muscle alone was not sufficient for stress resistance, indicating a likely requirement in multiple tissues. We identified minimal motifs within C. elegans LEA-1 that were sufficient to increase desiccation survival of E. coli. To test whether such motifs are central to LEA-1's in vivo functions, we then replaced the sequence of lea-1 with these minimal motifs and found that C. elegans dauer larvae formed normally and survived osmotic stress and mild desiccation at the same levels as worms with the full-length protein.ConclusionsOur results provide insights into the endogenous functions and expression dynamics of an LEA protein in a multicellular animal. The results show that LEA-1 buffers animals from a broad range of stresses. Our identification of LEA motifs that can function in both bacteria and in a multicellular organism in vivo suggests the possibility of engineering LEA-1-derived peptides for optimized desiccation protection.

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Low desiccation and thermal tolerance constrains a terrestrial amphibian to a rare and disappearing microclimate niche.

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