Lower bioenergetic costs but similar immune responsiveness under a heat wave in urban compared to rural damselflies

Abstract

There is mounting evidence that the widespread phenotypic changes in response to urbanization may reflect adaptations caused by rapid evolutionary processes driven by urban‐related stressors. Compared to increased habitat fragmentation and pollution, adaptations towards another typical urban‐related stressor, that is higher and longer lasting very high temperatures (heat waves), are much less studied. Notably, the sensitivities to heat waves of life‐history traits and important fitness‐related physiological traits such as immune responsiveness and bioenergetic variables (energy availability, energy consumption and their balance) have never been contrasted between urban and rural populations. By conducting a laboratory common‐garden experiment, we compared effects of a simulated heat wave on life history (survival and growth rate), immune responsiveness and bioenergetic variables between three urban and three rural populations of the damselfly Coenagrion puella. Because energy‐mediated trade‐off patterns may only be detected under energetically costly manipulations, all larvae were immune‐challenged by simulating ectoparasitism by water mites. As expected, the simulated heat wave caused negative effects on nearly all response variables. The immune responsiveness, on the other hand, increased under the heat wave, consistent with a trade‐off pattern between immune function and growth, and this similarly between urban and rural populations. A key finding was that urban larvae suffered less from the simulated heat wave compared to the rural larvae in terms of a lower heat wave‐induced depletion in energy availability. This suggests an adaptation of urban populations to better cope with the stronger and more frequent heat waves in cities. Notably, this urbanization‐driven evolution in the bioenergetic variables was not apparent in the absence of a heat wave. Given that changes in energy budgets have strong fitness consequences, our findings suggest that the evolved higher ability to cope with heat waves is fundamental for the survival of urban damselfly populations.

Genetic differentiation in pesticide resistance between urban and rural populations of a nontarget freshwater keystone interactor, Daphnia magna

“…We expected that chlorpyrifos resistance in urban Daphnia would be higher at 24°C compared to resistance in rural animals at that temperature, given thermal adaptation can offset pesticide toxicity under warming conditions (Op de Beeck et al, 2017 ; Dinh Van et al, 2013 ). Possibly, such responses would be more strongly elicited under more stressful thermal conditions such as heat spikes or heatwaves (Tüzün & Stoks, 2020 ). We did not apply a heat spike or heatwave in our experimental design as the exposure would need to last up to a minimum of five days (heatwave), which does not conform OECD ( 2004 ) guidelines of an acute toxicity test (48–72h).…”

“…We propose future research to include a longer sublethal exposure to chlorpyrifos in combination with the occurrence of a heatwave, after which the organisms can be monitored for life history and physiological (energy budget, detoxification enzymes, etc.) responses (Tüzün & Stoks, 2020 ; Dinh Van et al, 2016 ). So far, this was beyond the aim of our study.…”

Urban ecophysiology: beyond costs, stress and biomarkers

“…Well-designed experiments will also be able to disentangle the underlying mechanisms of acclimation (or other types of plasticity), heritability or genetic adaptation (see Glossary), or will determine whether the responses are coping strategies or even maladaptive, allowing us to understand the impact of urbanisation. These kinds of experimental studies are still rare (but see Lucas and French, 2012;McLay et al, 2017;Salmón et al, 2018b;Tuzun and Stoks, 2020).…”

Cryptic eco‐evolutionary feedback in the city

“…Daphnia magna show multiple adaptations to urban areas, including increased heat tolerance, faster pace‐of‐life and higher energy reserves (Brans & De Meester, 2018; Brans, Tüzün, et al, 2018)—implying higher activity, and thus reduced vulnerability to predation. In turn, damselfly nymphs of a closely related genus to Ischnura (used here) adapt to the longer growing season in urban ponds through a slower growth rate, alongside increased ability to cope with heat stress (Tüzün et al., 2017; Tüzün & Stoks, 2021)—potentially facilitating higher foraging activities under urban heat. This strong mechanistic understanding of species' individual responses to urbanization informed the authors (correct) predictions of a cryptic evo‐to‐eco feedback.…”