Has behavioural thermoregulation evolved solely to stay alive in insects, nothing more?

Abstract

Temperature is probably the most influential abiotic variable as it drives nearly all physiological rates. Temperature is both easy to measure, especially with our technological level, and complex to apprehend, because it varies widely across temporal and spatial scales. The mere question of what temperature a given ectotherm experiences at the level of its cells and enzymes (i.e. body temperature) has generated tons of excellent works since a century (Angilletta, 2009; Clarke, 2017; Gates, 1980). The process of behavioural thermoregulation is a key tenet in these studies because it bridges organismal performance and temperature heterogeneity. In its broad definition, behavioural thermoregulation is the use of locomotion or behavioural adjustments to meet permissive temperatures in the environment (Lahondère, 2023). For thermal ecologists, behavioural thermoregulation is a stimulating topic as it involves several disciplines including behaviour, physiology, biometeorology and biophysics (Gates, 1980; Helmuth, 1998; Kearney & Porter, 2004; Pincebourde & Woods, 2012).

Behavioural thermoregulation occurs in various ectotherm taxa. Amazingly, studies on reptiles' thermoregulation largely focused on their ability to find the optimal temperature for their performance (e.g. locomotion, activity window) while works on insects mostly investigated their capacity to avoid overheating and improve survival under extreme heat. However, in both cases, the picture is only partial, and only few studies so far have analysed behavioural choices in the context of thermoregulation to both avoid lethal temperatures and maximize performance by selecting the optimal temperature. This is precisely the aim of the study by Leith et al. (2024). In a small herbivore insect, Leith and colleagues assess if behavioural thermoregulation both improves survival and maximize reproduction performance within the mosaic of thermal microenvironments of the host plant.

In an open-air mesocosm, Leith et al. (2024) surveyed body and operative temperatures of treehoppers across different plant structures using infrared imaging. The operative temperature (i.e. the body temperature at a given position without any thermoregulatory effect) was inferred using judicious three-dimensional printed models with colour, size and shape matching the treehopper body. Operative temperatures are used to describe the available microclimates. Among the most astonishing results, Leith et al. reports high heterogeneity of operative temperatures within and across plant individuals at any point in time, by up to almost 20°C. The variability in actual body temperatures is lower, suggesting that the insect actively thermoregulate to some extent, especially to avoid the most stressful temperatures above ~36°C that elicit the rapid heat escape behaviour. However, the thermal preference range remains wide, and the insect is unlikely to select directly its microclimate within this range to optimize mating activity. Indeed, the thermal preference of the treehopper does not vary with sex and mating status (as inferred by playing playbacks of acoustic courtship primers during thermal preference assays), suggesting that mating behaviours do not modify thermal biology metrics.

Finally, the core of this study consists in analysing the effects of thermal quality (i.e. if lethal temperatures are present within the plant) and variability (i.e. the temperature range present across the plant) on the thermoregulation accuracy. The relationship between thermoregulation metrics unambiguously demonstrates that the cost–benefit conceptual model applies in this system: the insect actively select body temperature within its thermal preference range mostly when lethal temperature are present somewhere in the plant, and thermoregulation is even more accurate in a highly heterogeneous thermal environment. Indeed, thermoregulation was mostly effective under high ambient air temperature and when the insect is on a leaf, which are the conditions with higher probability to meet lethal temperatures. Otherwise, the insect mostly thermoconforms suggesting that the treehopper does not thermoregulate behaviourally to meet the narrow range of body temperatures that maximize mating activity.

The study of Leith et al. is highly significant for the field of thermal ecology. Conceptually, studies that allow to partition between the cost–benefit and the inhibited-movement models of thermoregulation remain exceptional. Indeed, the thermal heterogeneity at fine scale is such that it may become unpredictable for the insect which should spend a huge amount of energy to search and exploit body temperatures near optimum for mating—in other words the cost outweighs the benefits of being precise. This cost–benefit model certainly applies to numerous arthropod species that display similar heat escape behaviours such as aphids (Ma et al., 2018). The rapid heat escape behaviour to ovoid exposure to lethal temperature is not without consequences, however. Insects that fall on the ground to escape overheating at the leaf surface are suddenly exposed to soil predators and are at risk of starvation before they relocate themselves on the plant (Ma et al., 2018). An important trade-off should exist therefore between heat avoidance, predation exposure, and feeding constraint which complexifies the picture. Comparative analyses across species differing in behaviour are necessary to better comprehend the drivers of this compromise.

Although survival is improved by behavioural thermoregulation, the population level performance may still be challenged under elevated atmospheric temperatures because most individuals remain at suboptimal temperatures for reproduction. Thus, this study provides mechanistic understanding of recent works reporting that the thermal sensitivity of reproduction more accurately predicts species distributions and vulnerability to climate change (Parratt et al., 2021; van Heerwaarden & Sgrò, 2021). Since a decade or so, we have seen a resurgence of macroecological studies considering microclimates (air temperature) as a potential buffer of species vulnerability to climate change (Zellweger et al., 2020)—this is not enough as neglecting body temperatures within fine scales misses the actual level of exposure to limiting temperatures. This is particularly true in ecosystems where organisms are exposed to solar radiation which generate strong levels of thermal heterogeneity within fine scales (Pincebourde & Suppo, 2016; Saudreau et al., 2017), by contrast to the understorey of forests which are shielded from radiation and display homogeneous thermal environments (Zellweger et al., 2020). Training on heat transfer processes certainly is key to comprehend the mechanisms generating thermal heterogeneity and to adjust appropriate designs (Briscoe et al., 2023). Ecologists working in this area should develop their own “biophysical intuition” to better anticipate the amplitude of body temperature gradients within fine spatial scales.

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