4 Discussion

To our knowledge, empirical evidence of how humidity regulates the responses of hosts and parasitoids to extreme temperatures is limited. We investigated how the life history traits of hosts and parasitoids were affected by different timing and duration of heat waves, and how the effect of heat waves was modified by different humidity levels. We showed that humidity interacting with heatwaves can strongly affect the life histories of hosts and parasitoids, with a direct effect on hosts and an indirect effect on parasitoids.
Whilst duration of heat waves did not affect host emergence directly, exposing the parasitised hosts to longer heat waves increased the mortality of parasitoids, including complete mortality after 72 hours of heat waves exposed in the early life stage, leading to greater host emergence from parasitized hosts. This supports the general idea finding that parasitoids are less tolerant to heat stress than their hosts (Wenda et al., 2023, Hance et al., 2007), but emphasises that heat wave duration rather than the level of heat wave may be more important. Thus, the detrimental effects on parasitoids experiencing high temperatures for a long period of time can disrupt the trophic interactions, and suggests that pest outbreaks might be more likely if such conditions are experienced in nature. In addition, the juvenile development of survived hosts and parasitoids was longer when exposed to longer heat waves, indicating a risen energy expenditure for hosts and parasitoids to survive from sublethal heat environments. Hosts and parasitoids may able to cope with heat stress by accumulating heat shock proteins and biogenic amines (González‐Tokman et al., 2020), allowing them to acclimate to the new environment, but with an extra energetic cost. This energetic cost may result in prolonged developmental time (Gillespie et al., 2012, Zhang et al., 2019), and reduced fitness in the adult stage (Yu et al., 2022, Nguyen et al., 2013) as a trade-off.
The timing of heat waves is known to be important for host-parasitoid interactions, as some development stages of parasitoids are more sensitive to heat stress than other stages (Zhang et al., 2019, Valls et al., 2020, Simaz and Szűcs, 2021). In accordance with our predictions, our results showed that experiencing longer heat waves at an early stage increased the mortality of parasitoids, but had no effect on unparasitized hosts, suggesting that experiencing heat waves at early stage of ontogeny may be critical to the survival of parasitoids. Moore et al. (2021) found that compared with other larval stages, experiencing heat waves at the embryonic stage resulted in complete mortality of the parasitoid Cotesia congregata . In our system, V .canescens starts to build body mass after c . 5 days following parasitism of P. interpunctella (Harvey et al., 1994), suggesting that the parasitoids may be in the embryonic stage when they experienced heat waves during the 4thinstar. Furthermore, the timing of heat waves could modify the life history of surviving parasitoids (Simaz and Szűcs, 2021, Zhang et al., 2019), as our results also showed that parasitoids experiencing heat waves at a later stage decreased their juvenile development time and increased their hind tibia length. Although the physiological mechanisms underpinning these life history changes of surviving parasitoids were not clear, our results highlighted that the effect of heat stress on the success of parasitism was stage specific.
Of potential critical importance for the maintenance of host-parasitoid interactions experiencing heat stress was our finding that higher humidity increased the survival of parasitoids against heat stress. Furthermore, modification of key the life history traits of both hosts and parasitoids demonstrated a key role of humidity in modulating the effect of heat stress that has largely been unreported. One possible explanation is that humidity affects host suitability for parasitism through regulating its water budget (Johnson, 2010), indirectly causing fitness-related responses in parasitoids. For example, Mainali and Lim (2013) found high (90-95%) humidity increased the adult emergence of an egg parasitoid Ooencyrtus nezarae , due to reduced water loss in host eggs. In our system, V. canescens is a koinobiont endoparasitoid, which feeds on host larvae after parasitisation, and it is critical for the host to reach the final (5th) instar for it to complete its own development and eclose as an adult wasp. The responses of hosts to humidity may further affect their nutritional quality for the development of parasitoids. However, disentangling this effect requires further investigation on how the suitability of hosts for parasitism could be driven by different humidity regimes.
The path analysis showed that heat waves affected hosts directly, but indirectly affected parasitoids through host survived time, at least in terms of adult size. This suggested that heat waves were having an indirect effect on parasitoids via their direct effects on the host. Previous studies found that V. canescens exhibited flexible growth patterns to accommodate the growth of their hosts (Harvey, 1996, Harvey and Vet, 1997), therefore the responses of hosts to heat stress could result in indirect phenotypic responses of parasitoids. To our knowledge, there are few studies examining these direct and indirect effects across two trophic levels. Simaz and Szűcs (2021) found a direct effect of heat waves on both the hostHalyomorpha halys and the parasitoid Trissolcus japonicus , with an indirect effect found beyond the first generation. However, we demonstrated that the direct and indirect effect of heat waves could be found within a single generation, as the responses of host may affect the ontogenetic development of parasitoids. This highlights that humidity may also play an important role in moderating direct and indirect effects of heat wave effects on hosts and parasitoids, which have important implications for their co-existence, extinction risk, and potential for more pest outbreaks under similar conditions in nature.
We attributed the humidity effect to the differences in the average moisture levels between treatments, but variation in humidity, which was not measured in this study, might also affect some critical life history stages such as diapause (Wetherington et al., 2017, Seymour and Jones, 2000). Higher variation in humidity may trigger more humidity-induced diapause in parasitoids (Wetherington et al., 2017), but in the present study this effect was unconsidered. Furthermore, the optimum humidity levels, which may depend on the temperature, in our system is unclear. Gross (1988) found a significant decline in parasitoid emergenceTrichogramma pretiosum over 80% or below 40% RH. Duale (2005) found that the optimum humidity for the development of a parasitoidPediobius furvus was between 60-80% RH. It is possible for a nonlinear effect of humidity on the life history performance of hosts and parasitoids, and so a greater range of humidity x temperature combinations should be explored in future.
The present study has implications for pest management and biological control. Humid environments may increase the development of hosts and possibly increase the fitness of their adult stage, resulting in more frequent and severer pest outbreaks (Stireman et al., 2005, Wetherington et al., 2017). Experiencing long heat waves especially at certain larval stage is detrimental to parasitoids, suggesting that the success of biological control under continuous heat events is stage specific. From this point of view, more evaluations of stage specific effect of heat events may provide practical insights into the successful applications of biological control in the field.