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.