Fungal infections lead to shifts in thermal tolerance and voluntary exposure to extreme temperatures in both prey and predator insects

Abstract

Pathogens can modify many aspects of host behavior or physiology with cascading impacts across trophic levels in terrestrial food webs. These changes include thermal tolerance of hosts, however the effects of fungal infections on thermal tolerances and behavioral responses to extreme temperatures (ET) across trophic levels have rarely been studied. We examined how a fungal pathogen, Beauveria bassiana, affects upper and lower thermal tolerance, and behavior of an herbivorous insect, Acyrthosiphon pisum, and its predator beetle, Hippodamia convergens. We compared changes in thermal tolerance limits (CTMin and CTMax), thermal boldness (voluntary exposure to ET), energetic cost (ATP) posed by each response (thermal tolerance and boldness) between healthy insects and insects infected with two fungal loads. Fungal infection reduced CTMax of both aphids and beetles, as well as CTMin of beetles. Fungal infection modified the tendency, or boldness, of aphids and predator beetles to cross either warm or cold ET zones (ETZ). ATP levels increased with pathogen infection in both insect species, and the highest ATP levels were found in individuals that crossed cold ETZ. Fungal infection narrowed the thermal tolerance range and inhibited thermal boldness behaviors to cross ET. As environmental temperatures rise, response to thermal stress will be asymmetric among members of a food web at different trophic levels, which may have implications for predator–prey interactions, food web structures, and species distributions.

Infection burdens and virulence under heat stress: ecological and evolutionary considerations

“…Across systems, host heat tolerance can be influenced by infection status ( table 1 ). The underlying mechanisms driving these changes remain largely unexplored [ 14 , 21 ]. Given the wide range of host–parasite interactions that have similar responses, there could be multiple underlying mechanisms.…”

“…Parasites can significantly contract host heat tolerance during extreme warming events (e.g. [ 18 , 19 , 21 , 23 ]). Reduced tolerance to heating is therefore an intrinsic component of the virulence—harm caused by infection (e.g.…”

Warming-induced excess deaths of infected animals depend on pathogen kingdom and evolutionary history

“…1A, logRR>0, RR=1.47, p=0.0046). Previous findings that infection can reduce the ability of hosts to tolerate elevated temperatures [16,43,44] may reflect this increase in pathogen virulence.…”

Respostas fisiológicas e comportamentais de pequenos animais ectotérmicos a variações térmicas no espaço e no tempo

“…1). Under this rationale, recent studies with small insects have shown that some individuals may actually explore voluntarily extreme hot or cold temperatures, and even engage in thermal risks (NAVAS; AGUDELO-CANTERO; PORRAS et al, 2021). The latter has been termed thermal boldness by in an investigation with fruit flies (D. melanogaster).…”

“…Such scenario is even more critical for small ectothermic animals like many insects 3,37,41 , given constraints posed by a small body size (see above). However, small motile insects may also exhibit alternative behaviors when navigating in extreme thermal landscapes (ETLs), including the volunteer exploration of extreme temperatures and thermal risk-taking (namely thermal boldness) 42,43 . Moreover, thermal boldness towards extreme high temperatures may bear little dialog with acute heat tolerance, thus departing from any expectation based on optimality models of thermal adaptation (see Fig.…”