Introduction
The activities of interacting species are often coordinated in time and
any shifts in the timing of ontogenetic or phenological events are
hypothesized to cause fitness declines in interacting species, affecting
population and community dynamics (Cushing 1990; Miller-Rushing et
al. 2010; Yang & Rudolf 2010). Evidence is mounting that climate
change is altering the timing of environmental cues (e.g., temperature
and precipitation) that species use to initiate key life history events,
such as seasonal emergence or activity (Parmesan & Yohe 2003; Forrest
2016). Furthermore, differential responses across species within the
same community indicate that the temporal coordination of species
interactions is changing, which raises concerns that interacting species
are becoming temporally “mismatched” (Visser & Both 2005; Bothet al. 2009; Kharouba et al. 2018). Such mismatches can
lead to major changes in the outcome of species interactions and
population dynamics, but our understanding of the mechanisms linking
phenological asynchrony to their immediate and long-term consequences is
unclear (Van der Putten et al. 2010).
The intricacies of how unequal shifts in emergence phenologies disrupt
the timing of species interactions are critical in order to understand
how climate change can decouple species interactions (Kerby et
al. 2012; Johansson et al. 2015). For many species interactions
the outcome depends, in part, on the developmental stages of interacting
individuals. For instance, predators tend to attack specific
developmental stages of their prey, and pollinators require plants to be
in a certain flowering phase (Stacconi et al. 2015). Thus, the
extent that interaction strength and resulting dynamics change with
shifts in phenology depends on how much the outcome varies across
developmental stages (e.g., the extent traits of individuals change
during development) and how long individuals remain available to
interact (e.g., window of vulnerability) (Memmott et al. 2007;
Miller & Rudolf 2011; Johansson et al. 2015). Besides
contributing to shifts in phenologies, warmer temperatures also
accelerate growth rates, which shortens the amount of time spent within
each developmental stage (Kingsolver et al. 2011). This
ultimately narrows and shifts the window of vulnerability for
predator-prey interactions, or magnifies size differences in competitive
interactions (Benrey & Denno 1997; Rudolf & Singh 2013), potentially
exacerbating the effects of shifts in the emergence phenology of
interacting species (but see (Tuda & Shimada 1995). For example, faster
development rates of prey in warmer temperatures can result in natural
enemies missing their window of opportunity to attack, even if the
relative phenological relationship remains unchanged (Klapwijk et
al. 2010; Ren et al. 2020). Thus, abiotic or biotic
environmental conditions that change growth rates, or the temporal
availability of resources are likely to modify how the strength of
species interactions scales with phenological shifts, though few studies
have quantified these effects.
Phenological shifts are taking place across a variety of community
contexts, several of which are known to alter growth rates and the
temporal availability of interacting species. For example, strength of
intraspecific competition (e.g. resource limitation or host density) and
presence of alternative resource species, can affect growth rates and
temporal availability at a similar magnitude to changes attributed to
global warming (Benrey & Denno 1997; Wolf et al. 2017).
Development rates often slow down when levels of resource competition
are high, prolonging the number of days which prey species remain
vulnerable to attack (Barker & Podger 1970; Benrey & Denno 1997).
Similarly, the presence of alternative resource species, with
complementary development rates or phenologies, can help prolong the
total period during which resources remain available (Wolf et al.2017). However, most phenological studies have ignored community
contexts beyond pairwise interactions, which does not reflect the
reality that consumers typically utilize multiple resource taxa and that
levels of resource competition can show high spatial and temporal
variation (Nakazawa & Doi 2012; Revilla et al. 2014).
Furthermore, ongoing global declines in insect diversity and abundance
make these two aspects of community context particularly imperative to
study (Forister et al. 2019; Salcido et al. 2020). Such
community contexts may act as a buffer against severe changes in the
strength of interactions and promote interaction persistence in the face
of shifting phenologies (Yachi & Loreau 1999; Timberlake et al.2019; Olliff‐Yang et al. 2020), yet it’s uncertain how these
processes will act in future temperatures predicted by climate change.
Therefore, there is a pressing need for studies that integrate relative
interaction timing with concurrent shifts in temperature and community
context.
Here, we use laboratory experiments (Fig. 1) and dynamic simulations to
examine how warming and community context together modify the effects of
phenological shifts on the strength and dynamics of host-parasitoid
interactions. Parasitoids play an important role in determining host
population dynamics and are commonly used as biological control agents,
yet few studies have investigated the impacts of climate change on the
relative timing of host-parasitoid interactions
(Klapwijket al. 2010; Dyer et al. 2013; Jeffs & Lewis 2013). Using
a native Drosophila -parasitoid system from seasonal tropical
forests of North Queensland, Australia (Jeffs et al. 2021), we
experimentally delayed the emergence phenology of parasitoids relative
to their hosts and assessed how resource competition and presence of an
alternative host species modified the effect of delayed emergence in
ambient (24°C) and predicted warming temperatures (28°C) (Shuklaet al. 2019). It is important to note, that previous phenological
studies have focused on how increased temperature acts as the
environmental cue that drives shifts in emergence phenology among
interacting species. However, elevated temperatures often persist
throughout growing seasons. Thus, temperature is not only the cue; it is
also the context in which mismatched ecological interactions must
proceed. Therefore, we decoupled the effects of temperature and
phenology to quantify the effects of different phenological shifts in
current ambient and predicted warming temperatures. Additionally, we
applied parameters derived from the single-generation experiment to
simulate host-parasitoid population dynamics over 100 generations under
our experimental conditions using an age-structured Nicholson-Bailey
host-parasitoid model to examine their impacts on long-term persistence.
Together, this allowed us to assess (1) how temperature alters the
effects of phenological shifts on the outcome of host-parasitoid
interactions, (2) to what extent resource limitation and (3) the
presence of an alternative host species modifies effects of phenological
shifts under warming, and (4) how community contexts and temperature
interact to affect long-term persistence of host-parasitoid
interactions. Combining experimental and modeling approaches helped
identify which conditions were favorable over a single generation, but
detrimental for long-term persistence of host-parasitoid interactions.
The results represent an important step toward understanding how warming
and community context interact to modify the effects of phenological
shifts on the strength and dynamics of species interactions, which is
critical for predicting how ecological communities will respond to
climate change.