Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence.
Over the last decade, numerous studies have investigated the role of oxygen in setting thermal tolerance in aquatic animals, and there has been particular focus on arthropods. Arthropods comprise one of the most species-rich taxonomic groups on Earth, and display great diversity in the modes of ventilation, circulation, blood oxygen transport, with representatives living both in water (mainly crustaceans) and on land (mainly insects). The oxygen and capacity limitation of thermal tolerance (OCLTT) hypothesis proposes that the temperature dependent performance curve of animals is shaped by the capacity for oxygen delivery in relation to oxygen demand. If correct, oxygen limitation could provide a mechanistic framework to understand and predict both current and future impacts of rapidly changing climate. In arthropods, most studies testing the OCLTT hypothesis have considered tolerance to thermal extremes. These studies likely operate from the philosophical viewpoint that if the model can predict these critical thermal limits, then it is more likely to also explain loss of performance at less extreme, non-lethal temperatures, for which much less data is available. Nevertheless, the extent to which lethal temperatures are influenced by limitations in oxygen supply remains unresolved. Here we critically evaluate the support and universal applicability for oxygen limitation being involved in lethal temperatures in crustaceans and insects. The relatively few studies investigating the OCLTT hypothesis at low temperature do not support a universal role for oxygen in setting the lower thermal limits in arthropods. With respect to upper thermal limits, the evidence supporting OCLTT is stronger for species relying on underwater gas exchange, while the support for OCLTT in air-breathers is weak. Overall, strongest support was found for increased anaerobic metabolism close to thermal maxima. In contrast, there was only mixed support for the prediction that aerobic scope decreases near critical temperatures, a key feature of the OCLTT hypothesis. In air-breathers, only severe hypoxia (<2 kPa) affected heat tolerance. The discrepancies for heat tolerance between aquatic and terrestrial organisms can to some extent be reconciled by differences in the capacity to increase oxygen transport. As air-breathing arthropods are unlikely to become oxygen limited under normoxia (especially at rest), the oxygen limitation component in OCLTT does not seem to provide sufficient information to explain lethal temperatures. Nevertheless, many animals may simultaneously face hypoxia and thermal extremes and the combination of these potential stressors is particularly relevant for aquatic organisms where hypoxia (and hyperoxia) is more prevalent. In conclusion, whether taxa show oxygen limitation at thermal extremes may be contingent on their capacity to regulate oxygen uptake, which in turn is linked to their respiratory medium (air vs. water). Fruitful directions for future research include testing multiple predictions of OCLTT in the same species. Additionally, we call for greater research efforts towards studying the role of oxygen in thermal limitation of animal performance at less extreme, sub-lethal temperatures, necessitating studies over longer timescales and evaluating whether oxygen becomes limiting for animals to meet energetic demands associated with feeding, digestion and locomotion.
Department of Animal Ecology and Ecophysiology, Radboud University Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands. Electronic address: wilco@aquaticecology.nl.
Wilco C E P
WC
Verberk
Zoophysiology, Department of Bioscience, Aarhus University, C.F. Møllers Allé 3, Building 1131, DK-8000 Aarhus, Denmark.
Johannes
J
Overgaard
Zoophysiology, Department of Bioscience, Aarhus University, C.F. Møllers Allé 3, Building 1131, DK-8000 Aarhus, Denmark.
Rasmus
R
Ern
Zoophysiology, Department of Bioscience, Aarhus University, C.F. Møllers Allé 3, Building 1131, DK-8000 Aarhus, Denmark.
Mark
M
Bayley
Zoophysiology, Department of Bioscience, Aarhus University, C.F. Møllers Allé 3, Building 1131, DK-8000 Aarhus, Denmark.
Tobias
T
Wang
Department of Conservation Ecology and Entomology, Centre for Invasion Biology, Stellenbosch University, South Africa.
Leigh
L
Boardman
Department of Conservation Ecology and Entomology, Centre for Invasion Biology, Stellenbosch University, South Africa.
John S
JS
Terblanche
D000064:Acclimatization / Q000187:drug effects / Q000502:physiology*; D000818:Animals; D059001:Aquatic Organisms / Q000502:physiology; D001181:Arthropods / Q000378:metabolism / Q000502:physiology*; D001833:Body Temperature Regulation / Q000187:drug effects; D002980:Climate; D003445:Crustacea / Q000502:physiology; D007313:Insecta / Q000502:physiology; D010100:Oxygen / Q000494:pharmacology / Q000502:physiology*; D010101:Oxygen Consumption / Q000502:physiology; D013696:Temperature
D010100:Oxygen
Cardiovascular capacity; Circulation; Climate warming; Crustaceans; Heat tolerance; Hyperoxia; Hypoxia; Insects; OCLTT; Respiration physiology; Thermal biology; Ventilation