Thermal evolution ameliorates the long‐term plastic effects of warming, temperature fluctuations and heat waves on predator–prey interaction strength

Abstract

How thermal evolution may affect trophic interactions and its implications for trophic system stability remains unstudied. To advance insights in how global warming shapes trophic interactions, we need to consider besides increases in mean temperatures, also daily thermal fluctuations (DTF) and heat waves (HW), and how their effects are modulated by thermal evolution. Using a common‐garden approach, we tested how each thermal factor affected predator metabolic rate and functional response parameters, and used these responses to predict long‐term predator–prey interaction strength between larvae of the damselfly Ischnura elegans and the water flea Daphnia magna. Using high‐ and low‐latitude predator populations with the latter being exposed to higher mean temperatures, higher DTF and more frequent HW, we assessed the potential impact of thermal evolution at the high latitude using a space‐for‐time substitution. In line with thermal adaptation, growth rates were faster and handling times shorter in low‐latitude compared to high‐latitude larvae at 24°C while the opposite was true at 20°C. Warming weakened the long‐term interaction strength, except for the high‐latitude trophic system at DTF and HW where plastic responses therefore may not stabilize the high‐latitude system. This extends the emerging insight that temperature variation may make ectotherms more vulnerable to warming. The contributions of metabolic rate, search rate and handling time in shaping thermal effects on interaction strength differed between latitudes. A key finding was that thermal evolution may further weaken the long‐term interaction strength of the high‐latitude trophic system under increases in mean temperatures, even at DTF and potentially also at HW. Our results underscore the importance of daily thermal fluctuations and heat waves in shaping predator–prey interactions, and may suggest an overall stabilizing contribution of predator thermal evolution ameliorating thermal plastic effects on food web stability. A free Plain Language Summary can be found within the Supporting Information of this article.

Thermal plasticity and evolution shape predator–prey interactions differently in clear and turbid water bodies

“…Previous studies showed that warming may increase predatorprey system stability (Rall et al, 2010;Sentis et al, 2015;Wang et al, 2021). Our current experiment extends these studies by (a)…”

“…To assess effects on the short‐term predation rate and long‐term system stability, we conducted a functional response experiment and an experiment to quantify the prey’s population dynamics for each of the 16 treatment combinations. We then estimated functional response parameters (search rates and handling times) and carrying capacity, and used these estimated parameters together with prey body mass and predator metabolic rates at 20 and 24°C that were quantified in a previous study (Wang et al, 2021) to parametrize population dynamic models and predict system stability.…”

“…Studies on how global change‐related stressors affect trophic interactions in the long term typically only consider acute, plastic responses in predator and prey (Daugaard et al, 2019; Sentis et al, 2015). Nevertheless, there is increasing evidence that evolution also plays an important role in shaping responses to global change (Stoks et al, 2014; Urban et al, 2016; Wang et al, 2021). Thermal evolution can play a crucial role reversing maladaptive thermal responses or enhancing adaptive ones (Diamond & Martin, 2016) but this may not always be the case (Diamond & Martin, 2020).…”

Contributions of mean temperature and temperature variation to population stability and community diversity

“…While our study provides some insights into how changes in mean temperature and temperature variation affect diversity, the nature of the system and the length of the experiment mean several important processes are not accounted for. Among these, the design of our study does not account for how evolutionary changes in species may counteract or exacerbate the effects of changing temperature regime (Hoffmann & Sgró, 2011 ; Wang et al, 2021 ). Previous experiments have also demonstrated how global change‐mediated changes to trophic interactions can lead to altered diversity (Hammill, Johnson, et al, 2018 ), and how combined global changes can lead to reduced diversity (Atwood et al, 2015 ; Kratina et al, 2012 ; Tabi et al, 2019 ).…”

Species‐specific responses to warming alter community composition

“…A recent review of the topic (Colinet et al, 2015) found that insects subjected to fluctuating temperatures within their nonlethal thermal ranges elicit diverse responses. However, empirical studies of the effects of fluctuating temperatures on odonates remain rare (Frances et al, 2017; Verheyen & Stoks, 2019; Wang et al, 2021). We conducted two complementary experiments to address how warming and body size differentials during larval development influence emergence timing, body size, wing morphology and adult assemblage composition in three species of dragonfly.…”