1 Introduction

Climate warming, manifested primarily through increasing temperature and the greater frequency and intensity of heat stress events, such as short-lived extremes or heat waves (Rahmstorf and Coumou, 2011, Sun et al., 2019), has prominent impacts across ecological scales. How extreme heat waves affect biodiversity and ecosystems has yielded mixed findings (Ruthrof et al., 2018, Li et al., 2017, Cope et al., 2023) as extreme high temperatures have been shown to have positive, negative, or neutral effects on the individual fitness of living organisms, such as insects (Skendžić et al., 2021, Ma et al., 2021). However, as insects’ responses to thermal stress may not be consistent throughout ontogeny, the timing and duration of heat events experienced at different life stages may lead to contrasting fitness outcomes (Moore et al., 2022, Valls et al., 2020). Furthermore, differences in thermal tolerance and sensitivity between interacting species may result in differential responses to high temperatures, with trophic interactions in particular likely being disrupted (Moore et al., 2021, Bannerman and Roitberg, 2014). Hence, understanding how extreme high temperature impact on insect species and their trophic interactions is important to understand how they might respond to future climate change.
In addition to extreme temperatures, climate warming may increase the rate of surface evaporation, resulting in a combined stress of high heat and high humidity (Schär, 2016). Such ‘humid heat waves’ have been observed in many parts of the world and are projected to escalate under future climate change scenarios (Gershunov and Guirguis, 2012, Russo et al., 2017, Wang et al., 2021). However, how humidity modulates the effect of extreme temperatures has not been examined widely, leading to considerable uncertainty about the abundance and distribution of species (Chown et al., 2011, Simmons et al., 2023). Within this context, efforts to forecast the persistence of trophic interactions and their dynamics may be limited (Brown et al., 2023, Rozen‐Rechels et al., 2019).
Despite its pronounced influence on regulating insects’ life cycles, evidence for how humidity modulates thermal responses is rather underdeveloped (Brown et al., 2023). Humidity levels are not only related to the availability of water vapour that insects acquire from the environment, but they also affect the ability to regulate water loss through spiracular respiration (Shipp et al., 1988). For example, when exposed to low humidity environments, adult cockroaches (Naupheota cinera ) exhibited a slower rate of water loss due to longer periods of spiracular closure (Schimpf et al., 2009). However, some insects were able to gain moisture when air humidity increased, subsequently lowering the risk of desiccation (e.g., Salin et al., 1999, Johnson, 2010). Importantly, temperature is of fundamental importance in driving many physiological processes including spiracular control, thus the responses of insects to humidity may also be temperature-dependent (Heinrich and Bradley, 2014). As such, if the control of spiracles is an adaptative mechanism to balance the trade-off between water loss and gas exchange against changing environments (Oladipupo et al., 2022), humidity can either positively or negatively affect insect survival when temperatures increase.
Parasitoids are top-down regulators of their host’s population dynamics, they are a key component of terrestrial food webs, and they may be important in biological control (Jeffs and Lewis, 2013, Furlong and Zalucki, 2017). Koinobiont endoparasitoids lay their eggs inside their hosts, and their larvae continue to develop and feed inside the hosts as it grows and reaches the optimal size for adult parasitoid eclosion. There is a growing body of evidence that temperature can have both a direct impact on koinobiont endoparasitoid life history and an indirect impact via the response of their hosts to temperature (e.g., Cavigliasso et al., 2021, Meisner et al., 2014, Abarca and Spahn, 2021). In general, parasitoids are less tolerant of high temperatures than their hosts (Abarca and Spahn, 2021, Furlong and Zalucki, 2017), and hosts may suppress parasitism if parasitoids experience extreme high temperatures during early development stages (Moore et al., 2022). On the other hand, endoparasitoids may adapt to sublethal temperatures, via multiple ontogenetic responses as the result of the host development (Harvey and Strand, 2002, Harvey et al., 1994). For example, Additionally, as hosts are the only source of moisture for endoparasitoid larvae, humidity may indirectly affect parasitoids through the direct impact of humidity on their host. Previous work has shown that interactions between environmental factors, such as fluctuating temperatures and resource quality, influence the life history traits of both hosts and parasitoids in ways that could not be predicted from each factor alone (Mugabo et al., 2019), emphasising why it is important to consider combinations of environmental factors and their impacts on interacting species.
We investigated the effect of humidity on the responses of an insect host and its parasitoid when they were exposed to heat waves of different durations and experienced at different host ages, using the Indian meal moth Plodia interpunctella and its koinobiont endoparasitoid wasp Venturia canescens . We carried out a single generation life-history experiment where hosts were kept individually either in a humid or non-humid environment at a constant temperature of 28 ℃, with or without being parasitized early in the fourth instar. All parasitised and unparasitized hosts subsequently experienced either no heat wave (0 control), a 6-hour, or 72-hour heat wave of 38℃, applied either in the host fourth or fifth instars. We measured key life history parameters (larval development time, and adult emergence and body size) of both hosts and parasitoids to evaluate the combined effects of humidity and heat waves on this trophic interaction (see Figure 1 for experimental design).
We first assessed how the life history of hosts and parasitoids responded to the heat waves individually, and then assessed whether these responses were modified by a high humid environment. Further, we examined the direct effects of heat waves on hosts and parasitoids and the indirect effect through their trophic interaction, and investigated if these direct and indirect pathways were different between humidity levels. We predicted that 1) increasing heat wave duration would negatively affect hosts and parasitoids; 2) parasitoids will be more affected by heat waves than their hosts when they are earlier in their development; 3) humidity will modify heatwave effects on the hosts directly, and modify heatwave effects on parasitoids indirectly.