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Climate-driven oxygen limitation in freshwater macroinvertebrates

Final Report Summary - RESPIRE (Climate-driven oxygen limitation in freshwater macroinvertebrates)

In ectotherms, metabolism increases with temperature and a shortage of oxygen has been argued to set thermal tolerance limits, rather than temperature effects per se. This oxygen limitation hypothesis provides one of the few mechanistic frameworks to understand and predict the vulnerability of species to global warming, although to date its generality has remained unclear. The RESPIRE project has provided the first confirmative test that heat tolerance is indeed set by oxygen.

The degree to which low levels of oxygen reduce heat tolerance and high levels improve heat tolerance differs across 29 aquatic invertebrate species studied during the project. These taxa span the two main classes of freshwater habitat (lentic vs. lotic) and include the full range of respiratory modes seen in aquatic ectotherms (9 tegument breathers, 13 gill breathers, 7 air breathers using either a physical gill or a plastron). In producing such data, the project has greatly improved our understanding of how species attributes related to their phylogeny and physiology interact to set thermal limits (objective 2). As an example, in the case of aquatic nymphs of the stonefly Dinocras cephalotes, individual larvae differ in their thermal sensitivity for oxygen consumption rates (expressed by Q10 values). Thermal limits were approximately 1 degrees of Celsius lower for individuals with high thermal sensitivity (Q10 value of 3) compared to individuals with low thermal sensitivity (Q10 value of 1). In a different species, the damselfly Calopteryx virgo, we again found a reduction in heat tolerance under low levels of oxygen in aquatic nymphs. However, hyperoxia did not improve heat tolerance in this species. Interestingly, these asymmetrical effects of hypoxia and hyperoxia on heat tolerance have also been found in terrestrial insects and could be related to the differences in respiratory mode. Aquatic nymphs such as Dinocras cephalotes rely mainly on tegument respiration, while terrestrial insects have open tracheal systems which allow them to supply oxygen directly to their tissues. Aquatic gill-breathing nymphs, including those of Calopteryx virgo, may thus occupy an intermediate position between terrestrial insects with an open tracheal system and aquatic tegument breathers. We also used Calopteryx virgo to explore the potential for a mechanistic link between O2 conditions and thermal plasticity, by exposing nymphs to heat twice, using different levels of O2 in the second exposure. We established for the first time that aquatic nymphs do heat harden (they improved their heat tolerance on the second exposure) and such a hardening effect was elicited most strongly by hypoxia, not heat. This constitutes additional evidence for the oxygen limitation hypothesis.

To extend experimental results to field conditions (objective 3), spatial and temporal variation in temperature and oxygen levels have been studied in the field and field occurrences of species have been examined in collaboration with Cardiff University to determine how oxygen and temperature interactively shape species field distributions. A large dataset on two species of mayfly (Ephemerella ignita and Ephemera danica) was assembled and analysed, which covers a wide range of streams and catchments, where physicochemical and biotic data have been collected over a number of years. In both species, we found an interaction between oxygen and temperature such that species occur in warm waters only when oxygen levels are sufficiently high, again corroborating the central hypothesis. Moreover, differences in heat tolerance measured in the lab showed E. ignita to be more sensitive to heat and for this species the effect of oxygen on the field distribution was also stronger showing good concordance between lab data and field data. We also analysed an existing data set on the occurrence of two closely related fish species spanning over 30 years and were able to show that different levels of oxygenation can alter the competitive interactions between fish species. High iron concentrations cause respiratory impairment and spatial and temporal differences in iron concentrations matched patterns in relative dominance: under high iron conditions the Ninespined stickleback prevailed whilst under low iron conditions the Threespine stickleback prevailed.

Effects of increased temperature can be understood via its effects on both oxygen supply and demand. Species attributes modulate these temperature effects. This mechanistic model provides an insight into how oxygen limitation gives rise to the lethal and non-lethal limits of a species (objective 4). The results of the RESPIRE project suggest that it may be feasible to mitigate climate change effects via water quality improvements. Similarly, it provides a clear insight into the interaction between climate change and eutrophication, as eutrophication is facilitating hypoxia. As such the RESPIRE project has high societal relevance and direct applied value for the aims of European Water Framework Directive (EWFD), which stimulates efforts to achieve good ecological quality in surface waters, improving environmental robustness in the face of climate change.