The speed and metabolic cost of digesting a blood meal depends on temperature in a major disease vector

Abstract

The energetics of processing a meal is crucial for understanding energy budgets of animals in the wild. Given that digestion and its associated costs may be dependent on environmental conditions, it is necessary to obtain a better understanding of these costs under diverse conditions and identify resulting behavioural or physiological trade-offs. This study examines the speed and metabolic costs -in cumulative, absolute and relative energetic terms -of processing a bloodmeal for a major zoonotic disease vector, the tsetse fly Glossina brevipalpis, across a range of ecologically relevant temperatures (25, 30 and 35°C). Respirometry showed that flies used less energy digesting meals faster at higher temperatures but that their starvation tolerance was reduced, supporting the prediction that warmer temperatures are optimal for bloodmeal digestion while cooler temperatures should be preferred for unfed or post-absorptive flies. 13C-Breath testing revealed that the flies oxidized dietary glucose and amino acids within the first couple of hours of feeding and overall oxidized more dietary nutrients at the cooler temperatures, supporting the premise that warmer digestion temperatures are preferred because they maximize speed and minimize costs. An independent test of these predictions using a thermal gradient confirmed that recently fed flies selected warmer temperatures and then selected cooler temperatures as they became post-absorptive, presumably to maximize starvation resistance. Collectively these results suggest there are at least two thermal optima in a given population at any time and flies switch dynamically between optima throughout feeding cycles.

Prey‐specific impact of cold pre‐exposure on kill rate and reproduction

“…Many studies consider interaction strengths to be fairly fixed when applied in ecological models (e.g., Berlow et al, 2009), although it is well known that temperature affects predation rates (Dell, Pawar, & Savage, 2011;Laws, 2017). However, it is little studied how temperature and thermal history affects predator-prey interactions as well as parameters essential for these interactions such as predator locomotion and metabolic physiology (Clusella-Trullas, Terblanche, & Chown, 2010;McCue, Boardman, Clusella-Trullas, Kleynhans, & Terblanche, 2016;Williams et al, 2016). Further studies on the effects of thermal history on predator physiological and behavioural performance would be useful to disentangle the mechanisms that govern predator-prey dynamics.…”

Progressive behavioural, physiological and transcriptomic shifts over the course of prolonged starvation in ticks

“…Hematophagous arthropods are carriers for a myriad of diseases, and tolerance of extended periods between bloodmeals is critical to their survival and of epidemiologic importance (Philip & Burgdorfer, ). Starvation tolerance varies widely among the blood‐feeding arthropods, with survival times of hours [bat flies (Fritz, )], days [mosquitoes (Zhao et al., ) and tsetse flies (McCue, Boardman, Clusella‐Trullas, Kleynhans, & Terblanche, )], weeks to months [fleas (Krasnov, Khokhlova, Fielden, & Burdelova, ), kissing bugs (Cabello, ), and bed bugs (Polanco, Miller, & Brewster, )], and months to years [ticks (Oliver, )]. The ability of ticks to survive prolonged starvation is a hallmark of their biology and is an important component of their strategy for off‐host survival (Needham & Teel, ).…”

Evaluation of different blood-feeding frequencies on Glossina palpalis gambiensis performance in a mass-rearing insectary

“…Daily exposure to the 37 °C feeding membrane could be detrimental as temperatures above 30 °C may affect survival and fecundity [1,26]. Although a feeding frequency of six times per week optimized the number of blood-fed flies, it is important to note that the tetse fly needs on average 2 days to completely digest a blood meal [27]. Therefore, daily feeding seems to be overoptimized from a physiological point of view, as well as unnecessary.…”