The trade-off between heat tolerance and metabolic cost drives the bimodal life strategy at the air-water interface

Abstract

The principle of oxygen and capacity limitation of thermal tolerance in ectotherms suggests that the long-term upper limits of an organism's thermal niche are equivalent to the upper limits of the organism's functional capacity for oxygen provision to tissues. Air-breathing ectotherms show wider thermal tolerances, since they can take advantage of the higher availability of oxygen in air than in water. Bimodal species move from aquatic to aerial media and switch between habitats in response to environmental variations such as cyclical or anomalous temperature fluctuations. Here we tested the prediction that bimodal species cope better with thermal stress than truly aquatic species using the crab Pachygrapsus marmoratus as a model species. When in water, oxygen consumption rates of P. marmoratus acutely rise during warming. Beyond a temperature threshold of 23 °C the crab's aerobic metabolism in air remains lower than in water. In parallel, the haemolymph oxygen partial pressure of submerged animals progressive decreases during warming, while it remains low but constant during emersion. Our results demonstrate the ability of a bimodal breathing ectotherm to extend its thermal tolerance during air-breathing, suggesting that there are temperature-related physiological benefits during the evolution of the bimodal life style.

The importance of thermal history: costs and benefits of heat exposure in a tropical, rocky shore oyster

“…Fourthly, to accurately forecast species resilience and changes in distribution, the present results showcase the need to downscale our perspective from large scale macrophysiological patterns to local microclimatic levels, generated at the scale appropriate to each species and community (Helmuth et al, 2006Harley, 2008;Seabra et al, 2011;Potter et al, 2013). Specifically, in the case of intertidal habitats, substratum slope, orientation and topography operate to create a complex thermal landscape and determine the degree of thermal exposure of intertidal species (Williams and Morritt, 1995;Burrows et al, 2008;Harley, 2008;Helmuth et al, 2011;Seabra et al, 2011;Stafford et al, 2015;Fusi et al, 2016). Individuals that have settled on sun-exposed or shaded surfaces are, for example, subjected to different thermal gradients over a very small scale, even down to centimetres (Williams and Morritt, 1995;Helmuth and Hofmann, 2001;Chapperon and Seuront, 2011;Seabra et al, 2011) and this may reflect differential mortality of individuals when anomalous or extreme climatic events occur (Chan et al, 2006;Ngan, 2006;Harley, 2008;Schneider et al, 2010;Williams et al, 2011;Cartwright and Williams, 2014).…”

“…Secondly, colonisation of harsh environments appears to infer an adaptive value with a magnified resilience to climatic variability. Natural habitats, such as intertidal coasts, are not homogeneous in terms of temperature profiles, and thermal niches of different breadth and variance co-occur at small spatial scales (Williams and Morritt, 1995;Helmuth, 1998;Helmuth et al, 2006;Chapperon and Seuront, 2011;Fusi et al, 2016). Consequently, individuals co-habiting the same general environment but exposed to such spatial and temporal complexity at different scales may well experience very different microclimatic conditions (Denny et al, 2011).…”

“…Intertidal communities constitute one of the most widely distributed and tractable systems to understand how species can acclimate or adapt to extremely dynamic environments (Helmuth, 1998;Helmuth and Hofmann, 2001;Helmuth et al, 2002Helmuth et al, , 2006Chapperon and Seuront, 2011;Giomi et al, 2014;Fusi et al, 2016). In recent years, the interaction of major environmental drivers, combined with the biotic components of the intertidal habitat, has received great attention as a model system for determining the suite of responses species can exhibit to environmental challenges (Barry et al, 1995;Helmuth, 1998;Helmuth and Hofmann, 2001;Helmuth et al, 2002Helmuth et al, , 2006Harley and Helmuth, 2003;Burrows et al, 2008;Mislan et al, 2009;Chapperon and Seuront, 2011;Sokolova et al, 2012;Mislan et al, 2014).…”

Thermal limits in native and alien freshwater peracarid Crustacea: The role of habitat use and oxygen limitation

“…The problem of insufficient oxygen under warm conditions may be more immediate in water than in air as aquatic gas exchange is challenging due to the lower rate of oxygen diffusion in water and the larger effort required for ventilation as water has a higher density and viscosity (Verberk & Atkinson, ). Similarly, this challenge of breathing underwater is thought to explain the recurrent evolution of air breathing in crustaceans from tropical waters that may be more prone to severe hypoxia (Fusi et al., ; Giomi et al., ). Moreover, oxygen availability is more variable in an aquatic setting, declining at night and increasing during the day by primary producers, and options for thermoregulation to adaptively modulate body temperature are limited.…”

Land–Atmosphere Exchange of Water and Heat in the Arid Mountainous Grasslands of Central Asia during the Growing Season

“…Water and heat are the major natural resources in terrestrial ecosystems [1][2][3], and their interactions are highly relevant to net primary productivity [4][5][6]. A clear understanding of the characteristics of the land-atmosphere exchange of water and heat in ecosystems forms the scientific basis for the rational development and utilization of natural resources [7][8][9].…”