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.