Oxygen limited thermal tolerance is seen in a plastron breathing insect, and can be induced in a bimodal gas exchanger

Abstract

Thermal tolerance has been hypothesized to result from a mismatch between oxygen supply and demand. However, the generality of this hypothesis has been challenged by studies on various animal groups, including air-breathing adult insects. Recently, comparisons across taxa have suggested that differences in gas exchange mechanisms could reconcile the discrepancies found in previous studies. Here, we test this suggestion by comparing the behaviour of related insect taxa with different gas exchange mechanisms, with and without access to air. We demonstrate oxygen-limited thermal tolerance in air-breathing adults of the plastron-exchanging water bug Aphelocheirus aestivalis. Ilyocoris cimicoides, a related, bimodal gas exchanger, did not exhibit such oxygen-limited thermal tolerance and relied increasingly on aerial gas exchange with warming. Intriguingly, however, when denied access to air, oxygen-limited thermal tolerance could also be induced in this species. Patterns in oxygen-limited thermal tolerance were found to be consistent across life-history stages in these insects, with nymphs employing the same gas exchange mechanisms as adults. These results advance our understanding of oxygen limitation at high temperatures; differences in the degree of respiratory control appear to modulate the importance of oxygen in setting tolerance limits.

Physiological responses to short-term thermal stress in mayfly (Neocloeon triangulifer) larvae in relation to upper thermal limits

“…For example, Verberk and Bilton (2011) showed that CT max estimates could be increased with oxygen supplementation or decreased by oxygen depletion in the stonefly Dinocras cephalotes. This finding was also observed (Verberk and Bilton, 2013) in four additional species, and further work (Verberk and Bilton, 2015) showed that in the air-breathing aquatic insect Ilyocoris cimicoides, hypoxic water did not influence heat tolerance, whereas hypoxic water reduced heat tolerance in a plastron (dissolved oxygen)-breathing Aphelocheirus aestivalis. To our knowledge, no studies in aquatic insects have previously explored whether oxygen limitation occurs at more ecologically relevant chronic thermal limits.…”

Respiratory function of the plastron in the aquatic bug,Aphelocheirus aestivalis(Hemiptera, Aphelocheiridae)

“…By comparison, Thorpe and Crisp's data were 1.67 and 9.92 nmol s −1 g −1 , respectively, giving a scope of 5.9. A recent study of metabolic rate in inactive A. aestivalis at 5-15°C extrapolates to 2.62 nmol s −1 g −1 (=100 pmol s −1 ) at 20°C (Verberk and Bilton, 2015).…”

“…Conclusions about plastron function have been largely theoretical, although good measurements of plastron structure of the river bug Aphelocheirus aestivalis (Hinton, 1976) and rates of O 2 consumption have been measured for several species of plastron bugs (Kölsch and Krause, 2011;Thorpe and Crisp, 1949;Verberk and Bilton, 2015). According to a recent analysis (Seymour and Matthews, 2013), respiration rates of resting bugs range from 27 to 55% of the prediction of resting metabolic rates based on an interspecific allometric analysis of 391 species of insects in general (Chown et al, 2007).…”

Can respiratory physiology predict thermal niches?

“…Temperature‐induced mismatches between oxygen‐delivery capacity and oxygen demand and the heat thresholds that bring a species to hypoxemic conditions have been suggested to underlie thermal tolerance limits in ectotherm species . Consequently, thermal specialists could be especially limited by their capacity to increase oxygen uptake to meet demand in warm conditions …”