Mating under climate change: Impact of simulated heatwaves on the reproduction of model pollinators

Abstract

Climate change is related to an increase in frequency and intensity of extreme events such as heatwaves. It is well established that such events may worsen the current world‐wide biodiversity decline. In many organisms, heat stress is associated with direct physiological perturbations and could lead to a decrease of fitness. In contrast to endotherms, heat stress resistance has been poorly investigated in heterotherms; especially in insects, in which the internal physiological mechanisms available to regulate body temperature are almost negligible making them sensitive to extreme temperature variations. Wild bees are crucial pollinators for wild plants and crops. Among them, bumblebees are experiencing a strong decline across the world. Therefore, the ongoing global decline of these insect pollinators partly due to climate change could cause major economic issues. Here we assess how simulated heatwaves impact fertility and attractiveness (key parameters of sustainability) of bumblebee males. We used three model species: Bombus terrestris, a widespread and warm‐adapted species, B. magnus and B. jonellus, two declining and cold‐adapted species. We highlight that heat shock (40°C) negatively affects sperm viability and sperm DNA integrity only in the two cold‐adapted species. Heat shock can also impact the structure of cephalic labial glands and the production of pheromones only in the declining species. The specific disruption in key reproductive traits we identify following simulated heatwave conditions could provide one important mechanistic explanation for why some pollinators are in decline through climate change. A free Plain Language Summary can be found within the Supporting Information of this article.

Effects of Heat Stress on Mating Behavior and Colony Development in Bombus terrestris (Hymenoptera: Apidae)

“…A previous study in another hymenopteran (i.e., Nasonia vitripennis, a parasitic wasp) also showed that females are not able to distinguish a heat-exposed male from a non-exposed male (Chirault et al, 2015). As previously demonstrated (Martinet et al, 2021b) it has been shown that there is no significant impact of heat shock on the histology of cephalic labial glands and the composition of the produced pheromones in males of B. terrestris (i.e., a warm-adapted species). Our bioassays are consistent with these results.…”

“…This species is highly tolerant to environmental changes and is expanding globally (Inari et al, 2005;Torretta et al, 2006;Rasmont et al, 2015;Martinet et al, 2021a). It has previously been shown that for this heat-tolerant species, no effect of heat exposure was observed on sperm viability, sperm DNA integrity and composition of the attractive secretions of males (Martinet et al, 2021b). However, other nonassessed parameters related to bumblebee reproduction (e.g., sperm mobility, attractiveness of pheromonal mixture) could have a key role in the fertility of males.…”

“…One of the consequences of exposure to heat stress is a loss of fertility (Walsh et al, 2019). In insects, heat exposure can impact the viability, motility, competitiveness, and the DNA integrity of spermatozoa (Sales et al, 2018;McAfee et al, 2020;Martinet et al, 2021b). With the increase in frequency and severity of heat waves (Meehl and Tebaldi, 2004;Hallmann et al, 2017) and hence the heat stress experienced by insects, this impact will worsen in the future and may cause negative population trends (Sales et al, 2018(Sales et al, , 2021.…”

“…However, as emerged males live outside the nest, they cannot benefit from social thermoregulation. This exposure can lead to several physiological perturbations like a decrease in sperm viability and an increase in chromatin degradation (Martinet et al, 2021b). Degradation of sperm quality in bumblebee males can potentially be harmful because most studied bumblebee queens are monandrous (Baer, 2003).…”

“…These species-specific secretions are intended to attract females before mating (Bergström et al, 1981). It has previously been shown that extreme heat temperatures could impact those secretions in heat sensitive bumblebee species (i.e., Martinet et al, 2021b).…”