Universal model for water costs of gas exchange by animals and plants

Abstract

For terrestrial animals and plants, a fundamental cost of living is water vapor lost to the atmosphere during exchange of metabolic gases. Here, by bringing together previously developed models for specific taxa, we integrate properties common to all terrestrial gas exchangers into a universal model of water loss. The model predicts that water loss scales to gas exchange with an exponent of 1 and that the amount of water lost per unit of gas exchanged depends on several factors: the surface temperature of the respiratory system near the outside of the organism, the gas consumed (oxygen or carbon dioxide), the steepness of the gradients for gas and vapor, and the transport mode (convective or diffusive). Model predictions were largely confirmed by data on 202 species in five taxa-insects, birds, bird eggs, mammals, and plants-spanning nine orders of magnitude in rate of gas exchange. Discrepancies between model predictions and data seemed to arise from biologically interesting violations of model assumptions, which emphasizes how poorly we understand gas exchange in some taxa. The universal model provides a unified conceptual framework for analyzing exchangeassociated water losses across taxa with radically different metabolic and exchange systems.ll terrestrial animals and plants exchange O 2 and CO 2 with the atmosphere and thereby incur costs in the currency of water vapor (1-4). The inevitability of water loss stems from universal characteristics of terrestriality-(i) adequate gas exchange requires large surface areas of high-conductance tissues, usually invaginated; (ii) high-conductance tissues saturate internal exchange spaces with water vapor; and (iii) those surfaces must be ventilated by the atmosphere, at least intermittently. Consequently, water vapor tends to escape into surrounding drier air. Terrestrial organisms-here defined to include air-breathing marine mammals-thus face a gas-water tradeoff in which higher rates of gas exchange give higher rates of water loss. For individual organisms, this tradeoff shapes patterns of ventilation and behavior. For populations and species, the tradeoff influences diverse phenomena, including the evolution of hibernation, dormancy, and diapause (5-8), the evolution of nasal physiology in vertebrate homeotherms (9-11), and the evolution and ecology of plants with different modes of carbon fixation (C3, C4, and CAM) (12). In general, the severity of the tradeoff for any species will depend on the fraction of total water lost through the gas-exchange system, which in turn is related to the temperature and aridity of its habitat (13).The diversity of gas-exchange systems among taxa has spawned a large set of models for predicting respiratory and stomatal water losses (14-21). Although the models are all quite similar, they have failed to provide unification and generality as a group, because each uses different terminology and is built on taxonspecific details. Broader conceptualization of the problem may give insight into how diverse organisms function across biome...

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