Respiratory control in aquatic insects dictates their vulnerability to global warming

Abstract

Forecasting species responses to climatic warming requires knowledge of how temperature impacts may be exacerbated by other environmental stressors, hypoxia being a principal example in aquatic systems. Both stressors could interact directly as temperature affects both oxygen bioavailability and ectotherm oxygen demand. Insufficient oxygen has been shown to limit thermal tolerance in several aquatic ectotherms, although, the generality of this mechanism has been challenged for tracheated arthropods. Comparing species pairs spanning four different insect orders, we demonstrate that oxygen can indeed limit thermal tolerance in tracheates. Species that were poor at regulating oxygen uptake were consistently more vulnerable to the synergistic effects of warming and hypoxia, demonstrating the importance of respiratory control in setting thermal tolerance limits.

Oxygen safety margins set thermal limits in an insect model system

“…In addition, CT max estimates suggest that pupae are less susceptible to changes in ambient oxygen because hypoxia had no effect on CT max . These findings support the notion that insects with greater oxygen safety margin show a smaller effect of hypoxia on CT max (Verberk and Bilton, 2013). Unlike in D. cephalotes (Verberk and Bilton, 2011), thermal sensitivity of oxygen consumption rates (Q 10 ) are not correlated with CT max in B. mori (Fig.…”

“…Larvae may be able to use abdominal pumping and tracheal compression to maintain tissue oxygenation in the face of decreasing ambient P O2 and increasing temperature (Greenlee et al, 2013), whereas pupae are likely to be more constrained and rely more on diffusion-based gas exchange. Although initially tested by comparison of breathing modes among species (Verberk and Bilton, 2013), our results also lend support to the idea that respiratory control determines thermal limits. If respiratory control is defined as the ability to precisely regulate oxygen uptake in the face of external changes in oxygen availability at rest, one might expect B. mori larvae to have a higher oxygen safety margin than pupae because they have more behavioural options (i.e.…”

“…two-stage gas exchange, discussed in Klok et al, 2004), the respiratory milieu (e.g. Giomi et al, 2014;reviewed in Hsia et al, 2013) and the degree to which an animal is capable of regulating its gas exchange at rest, especially in the face of changing oxygen availability, may explain the difference between marine invertebrates that show support for OCLTT and air-breathing invertebrates that generally do not (Verberk and Bilton, 2013). For example, Verberk and Bilton (2013) showed across four insect orders that the degree of respiratory control within a particular species determined the extent of the oxygen limitation [measured as a reduction in critical thermal maximum (CT max ) with hypoxia].…”

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.…”

Cardiorespiratory ontogeny and response to environmental hypoxia of larval spiny lobster, Sagmariasus verreauxi

“…Increased metabolic demands at higher temperatures outweigh changes in oxygen availability and can surpass the capacity of the cardiac and ventilation systems to supply oxygen to the tissues leading to a reduction in whole body aerobic scope and thus reduced overall performance potential (Frederich and Pörtner, 2000;Pörtner, 2001Pörtner, , 2010. The challenge of balancing oxygen supply is also confounded by other environmental stressors such as decreasing dissolved oxygen levels (hypoxia) (Nilsson et al, 2010;Verberk and Bilton, 2013). Coastal waters are becoming depleted of oxygen due to eutrophication, and oxygen levels of the world's oceans are projected to decline due to changes in stratification and circulation patterns (Diaz and Rosenberg, 2008;Keeling et al, 2010).…”