Temperature affects the outcome of competition between two sympatric endoparasitoids

Temperature is a major driver of species interactions as it determines many physiological and behavioural parameters of ectothermic organisms such as insects. Examining the effects of elevated temperature and extreme temperature events within and between different trophic levels is crucial for understanding their broader implications for community and ecosystem level processes. We compared parasitism success of two hymenopteran parasitoid species, Diadegma semiclausum and Cotesia vestalis , under different temperature regimes when foraging intra-and interspeci ﬁ cally. Both parasitoid species can be found in the same habitat and are important biological control agents of the cosmopolitan lepidopteran pest Plutella xylostella , the host species in this study. Because parasitoid density may in-ﬂ uence parasitism success through interference competition, we ﬁ rst investigated the effect of parasitoid density (one to four females of the same species) on parasitism success at 22 (cid:1) C. In all assays, parasitoid females were released in cages with a single plant infested with 30 hosts placed in a greenhouse or climate cabinets set at 22, 27 or 33 (cid:1) C and removed after 3 h. All cages were returned to 22 (cid:1) C until pupation of the parasitoids or hosts, which were then counted. When females of the same species foraged together, parasitism success increased with parasitoid density. However, when both species were foraging together, parasitism success of D. semiclausum decreased with increasing temperature at both tested densities, whereas the opposite was found for C. vestalis . Nevertheless, parasitism success of D. semiclausum was always higher than that of C. vestalis , irrespective of parasitoid density or temperature, but competitive superiority of D. semiclausum decreased with increasing temperature. Increases in the magnitude and frequency of extreme temperature events under climate change are likely to have differential effects on species involved in intimate interactions, depending on community species composition, as species may differ in thermal resilience

Anthropogenic climate change and associated extreme climatic events (e.g. heat waves, droughts, rain downpours and fire) strongly impact biodiversity as well as a range of ecological interactions (Boeck et al., 2018;Dee et al., 2020;Dillon et al., 2016;Garcia et al., 2014;Greenville et al., 2018;Harvey et al., 2023). Temperature regulates the rate of biochemical reactions and, thus, is a strong driver of metabolism in ectothermic organisms such as insects (Angilletta, 2009;Brown et al., 2004;Kingsolver & Huey, 2008). The occurrence of extreme temperature events (ETEs), such as heatwaves, is expected to increase in frequency and magnitude. These events are characterized by short periods of unusually high temperature (i.e. >95th percentile of the temperature distribution), and are, therefore, difficult to predict (Thakur et al., 2022;Van de Pol et al., 2017). Exposure to ETEs causes physiological damage leading to potentially long-lasting effects on insect performance (Hance et al., 2007;Harvey et al., 2020;Ma et al., 2021;Stoks et al., 2017). Insects have evolved a diversity of behavioural and physiological mechanisms to cope with gradual climate warming, such as plastic responses or shifts in their geographical distribution to track suitable thermal conditions (Abram et al., 2017;Angilletta, 2009;Parmesan, 2006), whereas mechanisms to cope with ETEs are limited in terms of both physiology and behaviour (Colinet et al., 2015;Gonz alez-Tokman et al., 2020 ;Harvey et al., 2020). Because the range of temperature tolerance is species specific, the effects of exposure to ETEs on species interactions are highly variable and still poorly understood Rosenblatt et al., 2019;Stoks et al., 2017). Studies examining the impacts of ETEs on species and species interactions are urgently needed to better understand the broader ecological impacts of not only gradual climate change but also of ETEs .
Interactions between insect herbivores (hosts) and parasitoids have received considerable attention due to their significant role in regulating herbivore populations (Godfray, 1994;Stireman et al., 2005;Waage, 1982). Adult parasitoids are free-living organisms, while their offspring are intimately associated with a single host (Godfray, 1994). In nature, it is not rare to find several parasitoid species attacking the same host species (Hawkins, 1990). When parasitoid densities are high, there may be strong intra-or interspecific competition among female parasitoids for access to hosts (extrinsic competition; Wajnberg et al., 2008;Cusumano et al., 2016;Ode et al., 2022). Similarly, parasitoid larvae may compete for the same host resources (intrinsic competition; Godfray, 1994;Harvey et al., 2013). The outcome of competition between parasitoids depends on many factors linked to the environmental context and species traits in which the competition occurs. Species traits, such as host foraging efficiency, host specificity, egg load and parasitoid age, can influence how female parasitoids interact (Harvey et al., 2013;Ode et al., 2022). In addition, abiotic and biotic environmental factors, such as temperature and habitat characteristics, can modulate the outcome of competition (Cusumano et al., 2016;Harvey et al., 2013;Poelman et al., 2014;Vayssade et al., 2012).
Optimal foraging models predict that female parasitoids should aim to maximize fitness gain while foraging for hosts, which are often patchily distributed (Hubbard & Cook, 1978;Wajnberg et al., 2008). Parasitoid foraging behaviour is affected by a range of factors, including host density, the presence of other foraging parasitoids and the parasitism status of the host (Godfray, 1994;Vet, 2001;Wajnberg et al., 2008). The marginal value theorem predicts that patch time allocation by foraging parasitoids should increase with increasing host density (Charnov, 1976;McNair, 1982;Nonacs, 2001;Wajnberg et al., 2000). Parasitoid aggregation (i.e. increased parasitoid density) can lead to antagonistic encounters among different individuals, decreasing per capita parasitism success (Hassell, 1971;Hassell & Varley, 1969;Mohamad et al., 2015). Interference competition in parasitoid wasps is thought to play a significant role in driving the evolution of behavioural, physiological and morphological traits in parasitoids, as well as in structuring parasitoid communities (Bonsall et al., 2002;Hood et al., 2021;Ode et al., 2022;Price, 1972;van Alphen & Visser, 1990).
Parasitoids, like all insects, are ectotherms. Thus, temperature plays a vitally important role in their physiology and performance (Colinet et al., 2015;Hance et al., 2007). Temperature alters parasitoid foraging efficiency, walking speed, attack rates and host age preference (le Lann et al., 2014a;Moiroux et al., 2015Moiroux et al., , 2016Augustin et al., 2020). Parasitoid thermal tolerance is mostly species specific, although other factors, such as the geographical origin or the thermal history of an individual, can modify its thermal tolerance (Bowler & Terblanche, 2008;Diamond et al., 2017;Tougeron et al., 2020). For example, parasitoid species whose native geographical ranges are located at lower latitudes may be better adapted to warmer conditions and ETEs than species whose distributions are situated at higher latitudes (Carbonell & Stoks, 2020;le Lann et al., 2021). Divergent thermal tolerance between sympatric parasitoid species has been found to allow their coexistence in situ (le Lann et al., 2011;Mutamiswa et al., 2018). Moreover, many studies have reported diverging thermal tolerance between hosts and their associated parasitoids, with, in most cases, the parasitoid having a lower thermal tolerance than its hosts (Agosta et al., 2018;Furlong & Zalucki, 2017;Moore et al., 2021;Schreven et al., 2017). Divergent thermal tolerance between and across trophic levels may have repercussions for parasitoids attacking the same host when exposed to ETEs. Studies assessing the effects of temperature on parasitoid competition are rare (but see Chen et al., 2019 and references therein). Increased exposure to high temperatures under climate warming and concomitant ETEs might alter the interaction strength in hosteparasitoid networks, potentially resulting in new community assemblages followed by local species extinction and periodic herbivore outbreaks Stoks et al., 2017;Thierry et al., 2019). Understanding the impacts of ETEs on species interactions is of utmost importance to better predict the effects of climate change on communities and ecosystems (Berg & Ellers, 2010;Ma et al., 2021).
This study aimed to assess the effects of adult female parasitoid density and temperature, including simulated temperature extremes, on the outcome of extrinsic intra-and interspecific competition between the solitary endoparasitoids, Diadegma semiclausum (Hymenoptera: Ichneumonidae) and Cotesia vestalis (Hymenoptera: Braconidae) foraging for caterpillars of their shared host, the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). This moth is a major pest of brassicaceous crops worldwide and the two parasitoid species are among its most important natural enemies in the field (Furlong et al., 2013;Sarfraz et al., 2005). An initial experiment was conducted to assess the effects of parasitoid density on both intra-and interspecific competition under a 'normal' summer temperature in the Netherlands (T max ¼ 22 C, average for 1991e2020, KNMI, The Netherlands, https://www.knmi.nl/klimaatviewer/kaarten/temperatuur). A second experiment focused on the impact of increased temperature on the outcome of intra-and interspecific competition (at a fixed parasitoid density). We used three temperatures (22, 27 and 33 C) with the latter two corresponding to temperatures exceeding the 95th percentile of temperature distribution in the Netherlands 1 . We expected that under 'normal' temperature conditions, D. semiclausum would be a superior extrinsic competitor to C. vestalis, as previous studies comparing both species have reported higher parasitism rates for D. semiclausum (Wang & Keller, 2002;Yang et al., 1994), although contrasting parasitism prevalence has been reported between both species in natural ecosystems (Afiunizadeh & Karimzadeh, 2015;Ngowi et al., 2019). We also hypothesized that D. semiclausum but not C. vestalis parasitism rate would be negatively impacted by temperature above 30 C as the former is thought to be less thermotolerant than the latter (Furlong et al., 2013). We expected that with increasing parasitoid density, the number of parasitized hosts should quickly reach an asymptote due to increasing levels of mutual interference between the two species (Hassell, 1971). We discuss the importance of stochastic temperature extremes on competitive interactions among parasitoids and implications of this for species coexistence, host dynamics and community level processes.

Insect Cultures
Plutella xylostella and its parasitoids D. semiclausum and C. vestalis were collected in fields adjacent to Wageningen University campus, the Netherlands. Plutella xylostella and D. semiclausum have been reared at the Laboratory of Entomology since 2017, and C. vestalis since 2018. New individuals were added every year to maintain genetic diversity.
The herbivore and its parasitoids were maintained on Brassica oleracea var. gemmifera cv. Cyrus (hereafter Brussels sprouts) in separate rooms under constant conditions (22 ± 2 C, 40e50% relative humidity, 16:8 h light:dark). Male and female P. xylostella moths were placed in a clean cage with 10% sugar solution and a Brussels sprouts plant for a 48 h oviposition period. After 48 h, the Brussels sprouts plant with P. xylostella eggs was transferred to a clean cage. Newly hatched P. xylostella larvae were allowed to feed ad libitum until pupation with additional plants added. Diadegma semiclausum and C. vestalis were reared using a similar protocol. About 20 adult females, along with a few males, were released in a cage containing a Brussels sprouts plant heavily infested with second-to third-instar P. xylostella larvae (L2 and L3) from the stock colony. The host caterpillars were provided ad libitum with Brussels sprouts plants until their pupation. The newly emerged adult parasitoids were collected daily and placed in a clean cage with 10% sugar solution as a food source and used for rearing or experiments.
Brassica oleracea var. gemmifera cv. Cyrus plants were used as a food source for the larvae in both experiments and were 4e6 weeks old. Experimental parasitoid females were between 2 and 5 days old.

Ethical Note
There is no mandatory ethical procedure for the use of insects in animal experiments in the Netherlands. None the less, the individuals in our experiment were manipulated with care to avoid any unwanted stress or wounds that could have caused a behaviour change. This experiment was carried out using a minimum number of individuals per treatment while ensuring the quality of the statistical analysis and inferences drawn from the collected experimental data. During the experiment, individuals could acclimate to the new thermal conditions (if applicable) with a ramping temperature increase and access to either plant tissue or honey as a food source. After the experiment, individuals from the 22 C treatments were returned to the laboratory rearing. In contrast, insects from the other temperature treatments could not be returned to the colony and were killed by placing them in a À20 C freezer for more than 2 h. Insects are ectotherms, and this method quickly induces chill coma, reducing stress and potential suffering for the individuals. In addition, all the insects used during this study originated from our laboratory colony. This colony is reared at 22 C with a 16:8 h light:dark period, adult insects (moths and parasitoid) have access to 10% sucrose solution, while the parasitized or unparasitized P. xylostella larvae feed ad libitum on B. oleracea plants grown organically at Unifarm, Wageningen University, The Netherlands.

General Design of Experiments
The experimental design is shown in Fig. 1a. Thirty P. xylostella larvae (L2 and L3) were placed on a 4e6-week-old Brussels sprouts plant and allowed to settle and feed on the plant for approximately 1 day. The plant -host complex was placed inside a mesh cage (40 Â 40 cm and 60 cm high, Vermandel, Hulst, the Netherlands) in a greenhouse compartment (22 ± 2 C, 50e70% relative humidity, 16:8 h light:dark). The host densities were the same in all treatments described below. The following day, parasitoids were released in the cage and allowed to forage for 3 h after which they were removed. Cages with the plant and the parasitized caterpillars were maintained in the greenhouse until all caterpillars had developed into adult moths or parasitoids, which usually occurs within 15 days following parasitism, or had died. All cocoons, moth pupae and dead larvae were counted per cage. Each cage was a replicate. As plants differed in size, additional plants were added to make sure that there was ample food in the cage for the development of the caterpillars. All bioassays were performed between 1000 and 1400 hours. Additionally  Only D. semiclausum were also released at a density of eight females per cage. Females were allowed to forage for 3 h and were then removed. Cages with plants and caterpillars were maintained at 22 C until pupation of the insects, which took between 12 and 15 days, at which point all insects (moth pupae, parasitoid cocoons or dead larvae, in the figure depicted as adults) were counted. In (b) the different foraging treatments conducted at 22 (blue), 27 (yellow) or 33 C (red) are depicted. Foraging treatments were: two females of D. semiclausum, two females of C. vestalis, one female of each species and two females of each species. Temperature settings were adjusted 1 h before release of the parasitoids. Following foraging and removal of the parasitoid females, all cages were maintained at 22 C as described for the density experiment. Each box represents a cage.
P. xylostella larvae were left without parasitoids, and larval survival was recorded (i.e. the number of caterpillars recovered as pupae) as a control for 'naturally' occurring mortality.

Experiment 1: Parasitoid Density Effects of Intraspecific Competition at 22 C
We first tested the effect of parasitoid density on foraging success with female wasps of the same species. The densities were one, two and four females per cage for both parasitoid species (Fig. 1a). Diadegma semiclausum was also tested at a density of eight females per cage. Females were released at their respective densities in cages with a single plant infested with 30 hosts on the previous day and were allowed to forage for 3 h. Between 12 and 18 replicates were completed per treatment in five completely randomized time blocks.

Experiment 2: Interspecific Competition and Temperature
A similar protocol as in experiment 1 was used to study the effect of temperature (22, 27 or 33 C) on the outcome of intraand interspecific extrinsic competition (Fig. 1b). We used simulated 'realistic' high-temperature levels recorded in the Netherlands in the period 1991e2020 (KNMI, The Netherlands, https://www.knmi.nl/klimaat-viewer/kaarten/temperatuur).
As the two higher temperature regimes could not be simulated in a greenhouse, temperatures of 27 and 33 C were simulated in two climate-controlled cabinets (Hettcube 600, Hettich Benelux B.V.). We compared foraging efficiency when two parasitoids of the same species were released, one parasitoid of each species and two parasitoids of each species at 22, 27 and 33 C (Fig. 1b). To establish whether the data obtained from experiments in the greenhouse (22 C) and the climate cabinet (27 and 33 C) were similar, we also repeated one of the treatments conducted in the greenhouse (i.e. two D. semiclausum females) at 22 C in the climate cabinet (N ¼ 11). The experiment was conducted following the protocol described above in General Design of Experiments except that the first two steps (Fig. 1a), host settlement and parasitoid foraging, were conducted in the cabinets. Before the foraging assay, a 1 h temperature acclimation phase was added to prevent unwanted thermal stress on the parasitoids and the hosts. Female D. semiclausum and C. vestalis were collected in glass vials plugged with cotton wool and placed inside the mesh cages with the host-infested plants for 1 h. The temperature was either left at 22 C or gradually increased from 22 C to 27 or 33 C. After 1 h acclimation, the parasitoids were released into the mesh cage by removing the cotton wool plug and were allowed to forage for 3 h before being recaptured. Following the foraging period, the plantehost complexes were transferred to a greenhouse compartment (22 C ± 2 C, 50e70% relative humidity, 16:8 h light:dark) and reared until pupation as described above. Each treatment was replicated between 14 and 31 times. Temperature regimes and species combinations were randomly swapped daily among the two cabinets. All bioassays were performed between 1000 and 1400 hours. In addition, unparasitized P. xylostella caterpillars were exposed to the temperature treatments, and their survival was recorded.

Statistical Analyses
Each cage was considered a replicate in the statistical analyses. In total we conducted 333 assays with parasitoids and 35 with P. xylostella only (controls). Initially plants were infested with 30 P. xylostella caterpillars. All insects, host pupae, parasitoid cocoons and dead larvae were counted in each cage approximately 2 weeks after parasitoid foraging (Fig. 1). Recovery was calculated as the total number of pupae, cocoons and dead larvae. We omitted those replicates from the data set in which recovery was less than 10 or more than 30 (N ¼ 13 and 1, respectively). We also omitted assays in which no parasitoid cocoons (N ¼ 2) or only one (N ¼ 5) were produced suggesting poor motivation to parasitize hosts. To investigate general host survival in relation to temperature, we compared the relative recovery rates (recovery out of 30, the number of caterpillars that were initially placed on the plants) of P. xylostella in the control cages (i.e. cages in which no parasitoids were released but that were otherwise treated the same). We also compared relative recovery rates among control cages, cages exposed to only D. semiclausum, only C. vestalis or both, ignoring temperature or density. Our main interest was to compare (1) parasitism success per species calculated as the proportion of parasitoid cocoons of that species out of the 30 hosts that were initially placed on the host plant and (2) competitive superiority, only for treatments in which the two species foraged together, calculated as the number of D. semiclausum cocoons out of the total number of cocoons of D. semiclausum and C. vestalis together. All response variables were compared using generalized linear models (GLMs) assuming a binomial distribution with a logit link. Relative recovery of P. xylostella controls was modelled against temperature. Density and temperature were entered as covariates in the statistical models, unless stated otherwise. To compare parasitism success of the two species in relation to density, we only included the densities of one, two and four females, which were tested for both species. In this analysis, parasitoid species, density and their interaction were entered as model terms. Competitive superiority (proportion of D. semiclausum) was modelled against temperature (as a continuous variable) and density (as a discrete variable). Parasitism success of each species was modelled against temperature and foraging treatment (two females of the same species, one female of either species or two females of either species (as a discrete variable). Models were checked for overdispersion and corrected using a logit link quasibinomial distribution.
All the model assumptions and quality were assessed using graphical displays of Pearson residuals. The analysis was performed in R version 4.0.2 (R Core Team, 2020), using the 'lme4' package (Bates et al., 2015). Post hoc tests (z-tests) were completed with the 'emmeans' package (Lenth et al., 2018).

Recovery Rates
The combined number of P. xylostella moths and pupae in the control assays did not differ between temperature treatments (c 2 2 ¼ 0.89, P ¼ 0.64). On average, P. xylostella pupae and moths totalled 22.4 ± 0.7 (mean ± SE per cage) in the control cages. We also compared recovery rates, i.e. the number of pupae, cocoons, adults and dead larvae found in each cage at the end of the assay, among treatments with only D. semiclausum, only C. vestalis, both parasitoids and P. xylostella controls, ignoring parasitoid densities. Recovery rates differed between these four treatments (c 2 3 ¼ 16.3, P < 0.001). They were significantly higher for P. xylostella controls (23.0 ± 0.7, N ¼ 35) than for treatments with only D. semiclausum (19.6 ± 0.4, N ¼ 109, z ¼ 3.49, P ¼ 0.003) and the competition treatment with both parasitoids (19.3 ± 0.4, N ¼ 122, z ¼ 3.49, P < 0.001). Recovery rates were intermediate for the treatment with only C. vestalis (20.5 ± 0.5, N ¼ 81), which were not significantly different from the rates found for the other three treatment groups (P. xylostella: z ¼ 2.43, P ¼ 0.07; D. semiclausum: z ¼ 1.24, P ¼ 0.60; both parasitoids: z ¼ 1.65, P ¼ 0.35). This result suggests that foraging by D. semiclausum, in particular, causes additional host mortality.

Density
Parasitism success increased when parasitoid densities increased from one to four females (quasibinomial GLM: c 2 1 ¼ 9.49, P ¼ 0.005; Fig. 2). The relationship between density and parasitism success was similar for the two species (species*density interaction: c 2 1 ¼ 0.28, P ¼ 0.63). However, at a given density parasitism success was lower for C. vestalis than for D. semiclausum (c 2 1 ¼ 60.4, P < 0.001; Fig. 2). We also tested parasitism success for D. semiclausum at a density of eight females. At this density parasitism success was significantly lower than at a density of four females (c 2 1 ¼ 5.18, P ¼ 0.02). Moreover, the recovery rate for D. semiclausum at a density of eight females (12.7 ± 0.6, N ¼ 12) was significantly lower than at a density of four females (19.5 ± 1.4, N ¼ 14, c 2 1 ¼ 7.07, P ¼ 0.008). This result suggests that at densities between four and eight females interference competition negatively affects parasitism success of D. semiclausum. Interference between the parasitoids resulted in increased host mortality.

Intraspecific Competition
First, we checked whether results obtained from experiments conducted in the greenhouse were similar to those from experiments conducted in climate cabinets. Parasitism success of D. semiclausum at a density of two females and tested at 22 C did not differ between greenhouse and climate-cabinet experiments (c 2 1 ¼ 0.058, P ¼ 0.80). Based on this result we were confident that we could combine the data from the greenhouse (temperature set at 22 C) with those from the climate cabinet (temperature set at 27 and 33 C).
When the two parasitoid species foraged together, the competitive superiority of D. semiclausum decreased with increasing temperature (c 2 1 ¼ 4.88, P ¼ 0.027; Fig. 3). Doubling the density of parasitoids had no effect on the outcome of the competition (c 2 1 ¼ 1.52, P ¼ 0.21); neither was the interaction term between temperature and density significant (c 2 1 ¼ 1.08, P ¼ 0.29).
We also compared parasitism success of each parasitoid in relation to temperature separately, when foraging alone or with a competitor at two different densities (Fig. 4). For D. semiclausum (Fig. 4a), the interaction term between temperature and the effect of foraging treatment was significant (c 2 1 ¼ 6.58, P ¼ 0.037). When D. semiclausum was foraging intraspecifically there was no effect of temperature on parasitism success (z ¼ 0.835, P ¼ 0.40). However, when D. semiclausum was foraging together with C. vestalis, parasitism success of D. semiclausum decreased with increasing temperature (density 2: z ¼ À0.835, P ¼ 0.049; density 4: z ¼ À2.28, P ¼ 0.022). Foraging success of C. vestalis increased with temperature (c 2 1 ¼ 8.11, P ¼ 0.004; Fig. 4b), irrespective of foraging treatment (interaction between temperature and treatment; c 2 1 ¼ 1.93, P ¼ 0.38). This means that the slopes of the lines in Fig. 4b are not significantly different. However, when we compared in an additional analysis the relationship between temperature and intraspecific foraging success of D. semiclausum and C. vestalis the effect of temperature was not statistically significant (c 2 1 ¼ 3.12, P ¼ 0.076). This suggests that the effect of temperature on foraging success when foraging intraspecifically is only weak in both species. However, compared to the treatment in which C. vestalis was foraging with a conspecific female, parasitism success was lower when C. vestalis was foraging together with D. semiclausum at both densities (two females: z ¼ 4.04, P < 0.002; four females: z ¼ 3.10, P ¼ 0.005) with no difference between the two density competition treatments (z ¼ 0.46, P ¼ 0.88).

DISCUSSION
The results of this investigation revealed that parasitoid density and temperature differentially affected foraging success of C. vestalis and D. semiclausum. We hypothesized that parasitism would quickly reach an asymptote as the density of foraging parasitoids increased. We found that this did not happen at foraging densities between one and four, but only when the density was further increased to eight females (tested only for D. semiclausum). Moreover, C. vestalis parasitized fewer hosts than D. semiclausum, irrespective of parasitoid density. Temperature did not significantly affect foraging success of either parasitoid species when foraging intraspecifically. However, when both species were foraging together, parasitism success of D. semiclausum decreased with increasing temperature, whereas the opposite was found for C. vestalis. This result confirmed our hypothesis predicting that the effect of temperature would be species specific with a negative impact on D. semiclausum. However, in contrast to our hypothesis that there would be no effect of temperature on C. vestalis, there was a positive effect of temperature on parasitism success of this more thermophilic species when competing interspecifically. Overall, these results highlight the importance of insect community context in determining the response of a focal species to high temperatures and ETEs.
Diadegma semiclausum exploited host caterpillars per unit of time more efficiently than C. vestalis, and successfully parasitized up to 41% of the hosts compared to a maximum of 23% for C. vestalis. These results corroborate results from previous studies reporting that foraging efficiency (i.e. parasitism) of D. semiclausum was superior to that of C. vestalis (Wang & Keller, 2002;Yang et al., 1994). Diadegma semiclausum and C. vestalis have different foraging strategies (Wang & Keller, 2002;Yang et al., 1994). Diadegma semiclausum displays broad-area searching behaviour and fixed foraging patterns around P. xylostella feeding sites, while C. vestalis exhibits more plastic foraging patterns and searches in a restricted area around host feeding sites (Wang & Keller, 2002). Diadegma semiclausum also spends more time in a host patch, visits plants more frequently and is better adapted to cope with defensive behaviour of  . Mean parasitism success (±SE) of Diadegma semiclausum (red) and Cotesia vestalis (blue) when foraging at 22 C at different densities of the same species. The densities were one, two or four females per cage for both species. Diadegma semiclausum was also tested at a density of eight females per cage. Parasitoid females were released in cages with a single host-infested plant and were allowed to forage for 3 h. Parasitism success was calculated as the proportion of parasitoid cocoons out of 30, the initial number of caterpillars that were placed on the plants. The dotted lines depict linear relationships between parasitism success and densities between one and four (see text for statistics). Number of replicates (at ascending densities) was as follows: C. vestalis: 15, 15 and 17; D. semiclausum: 14, 18, 14 and 12. P. xylostella hosts than C. vestalis (Wang & Keller, 2002), factors that all contribute to enhancing foraging success (Ode et al., 2022). Furthermore, C. vestalis appears to be more of a generalist endoparasitoid than D. semiclausum, which is apparently specialized on P. xylostella (Hiroyoshi et al., 2017;Sarfraz et al., 2005). This may explain the greater foraging success of D. semiclausum.
Interference competition between foraging parasitoids usually decreases the per capita parasitism rate (Saini & Sharma, 2018;Yang et al., 1994). Parasitism success of both parasitoid species increased linearly at densities between one and four females per cage. Thus, at these densities, interference competition was negligible. Parasitism success of D. semiclausum was also tested at a density of eight females. At this density, parasitism success was reduced by more than 30% compared to that at a density of four females. The lower number of recovered insects at the end of the assay in the eight-density treatment suggests higher host mortality. When disturbed, P. xylostella caterpillars drop along a silk thread and climb back onto the leaf after several minutes. Repeated disturbance may have caused some of the caterpillars to leave the plant altogether resulting in early death. We were not able to study the foraging success of C. vestalis at higher densities due to limited availability of females of this species. It would be interesting to investigate at what density interference competition is compromising success of C. vestalis and whether intraspecific interference competition occurs in the field (for both species).
Temperature has species-specific kinetic effects on metabolism, and this can influence behavioural activity (e.g. walking speed, host handling time, activity versus quiescence; Abram et al., 2015;Moiroux et al., 2016;Boukal et al., 2019;Augustin et al., 2020). Moiroux et al. (2016) recorded a reduction in patch residence time and activity levels in Trichogramma euproctidis and Aphidius ervi with increasing temperature. The latter species attacks hosts with active behavioural defence mechanisms, which are also affected by temperature, partially explaining reduced residence time of the  . Mean parasitism success (± SE) of (a) Diadegma semiclausum and (b) Cotesia vestalis at different temperatures (22, 27 or 33 C), when foraging with a conspecific female (blue), together with one competitor (orange) or when both parasitoid densities were doubled (grey). Parasitoid females were released in cages with a single host-infested plant and were allowed to forage for 3 h. Parasitism success is calculated as the proportion of parasitoid cocoons out of 30, the initial number of caterpillars that were placed on the plants. The dotted lines depict significant linear relationships between parasitism success and temperature (see text for statistics). Number of replicates (at ascending temperatures) was as follows: D. semiclausum: 33, 18 and 18; C. vestalis: 15, 18 and 16; one female of each species: 31, 19 and 18; two females of each species: 14, 19 and 21.
parasitoid (Moiroux et al., 2016). Interestingly, under conditions of intraspecific competition, temperature did not significantly affect parasitism success in either D. semiclausum or C. vestalis in this study. The critical thermal maximum for development of the less thermophilic D. semiclausum is 30 C (Furlong & Zalucki, 2017). In general, less is known about critical thermal maxima for behavioural attributes (Abram et al., 2017;Reznik et al., 2009;Zamani et al., 2006). We only exposed the parasitoid females to 'warm' (27 C) or 'hot' (33 C) temperatures for about 3 h. Current and previously experienced temperature is an important parameter influencing insect activity levels (Berrigan & Partridge, 1997;Van Baaren et al., 2005;le Lann et al., 2011). It is conceivable that 3 h is simply not long enough to induce temperature-related changes in behaviour. However, under conditions of interspecific competition, effects of temperature were recorded (discussed below). Thus, even during a relatively short exposure period to warm or hot temperatures, behaviour can be affected but this depends on ecological context, here the presence of a heterospecific competitor.
When parasitism success under conditions of intra-and interspecific competition was compared, both species were less successful when they were foraging in the presence of the other species, irrespective of their density. However, with increasing temperature, this difference in parasitism success increased for D. semiclausum, whereas it did not change for C. vestalis. We only indirectly studied the effect of foraging behaviour on parasitism success, so we can only speculate on the underlying behavioural mechanism. Our results suggest that both species behave differently in the presence of conspecific and heterospecific female parasitoids. Cotesia vestalis is considered the more thermophilic species (Furlong et al., 2013) and, therefore, may be more active or more aggressive in the presence of an interspecific competitor at higher temperatures. Alternatively, the less thermophilic D. semiclausum may become less assertive in the presence of C. vestalis with increasing temperature.
Scaling up the effects of ETEs from individual to population to ecosystem level, as well as integrating them over longer timescales, is incredibly challenging (Van de Pol et al., 2017). Because each species has its specific thermal tolerance levels for various performance attributes, biologically relevant ETEs are highly species specific (Van de Pol et al., 2017). A thermal event experienced in the same habitat may be biologically extreme for one species but not for another (Chevin & Hoffman, 2017). Given that the critical thermal maximum for D. semiclausum is 30 C (Furlong & Zalucki, 2017), we predict that the relatively short exposure to elevated temperature in this experiment underestimates the effect of exposure to ETEs experienced by D. semiclausum during heatwaves with longer and repeated exposure to ETEs. Furlong and Zalucki (2017) modelled the effect of climate warming on the distribution of P. xylostella and D. semiclausum in Australia and predicted reduced control by D. semiclausum in most of its established range in 2070, exemplifying the impact of warmer and hot temperatures on this parasitoid.
An increase in the frequency of ETEs may accelerate shifts in community composition by altering competition strengths between species (Jentsch et al., 2007). The more thermotolerant C. vestalis may benefit from ETEs, in particular when they occur more frequently, by increasing its competitiveness and higher offspring survival which may ultimately result in a shift in species composition in favour of C. vestalis. This does not necessarily imply that D. semiclausum will be displaced as environmental heterogeneity will favour coexistence of both species (Bonsall et al., 2002;Gols et al., 2005;Hood et al., 2021;Outreman et al., 2018;Poelman et al., 2014;Price, 1972). Moreover, the impact of competition between C. vestalis and D. semiclausum in natural ecosystems is likely to be attenuated by the higher degree of host specialization of the latter (Hiroyoshi et al., 2017;Sarfraz et al., 2005). However, temperature may result in a shift in community structure. An observational study by Ngowi et al. (2019) reported a predominance of C. vestalis in the warmer lowlands and a predominance of D. semiclausum in the cooler highlands in East Africa. Although temperature is not the only parameter that can explain these differences in population dynamics and parasitism success, it undoubtedly contributed to this pattern (Talekar & Yang, 1991, Jeffs & Lewis, 2013Wang et al., 2022;this study). Other studies have also reported how asymmetric responses to high temperature and ETEs can affect population dynamics of interacting species. For instance, the effect of warming and thermal tolerance of competing ant species resulted in a decrease in the abundance of the thermosensitive species only when a competitor with higher thermal tolerance was present (Diamond et al., 2017). In an exemplary experiment, Davis et al. (1998) showed that the competitive outcome between three Drosophila species was driven by temperature, but the addition of a competing species altered the focal species' thermal optima. This result suggests that species-specific differences in thermal tolerance will yield more complex outcomes at the community than at the individual level (Boukal et al., 2019;Gvo zdík & Boukal, 2021;Outreman et al., 2018). The magnitude and direction of the effects of ETEs on parasitoid community will be mediated by many parameters such as the individual nutritional status, host abundance, interpatch distances and community composition (Felton & Smith, 2017;Jentsch et al., 2007;Thakur et al., 2022;Van de Pol et al., 2017) as well as the frequency of and time lapses between ETEs. A study focusing on the fitness impact of multiple ETEs showed that their effects were highly dependent on the temporal clustering of these events (Ma et al., 2018). Understanding the effects of ETFs on parasitoid community assembly requires a high level of integration across temporal scales (e.g. season), spatial scales (e.g. landscape and patch connectivity), occurrence and magnitude of extremes, and food web structure (e.g. strength of bottom-up and top-down forces) creating multiple possible scenarios (Han et al., 2019;Rosenblatt & Schmitz, 2016;Thierry et al., 2019;Tougeron et al., 2016).
Overall, this study showed a decrease in competitive superiority of D. semiclausum when foraging together with C. vestalis at 'warm' and 'hot' temperatures. Our results, combined with other studies, suggest a convergence in niche exploitation by the two competing parasitoids (le Lann, et al., 2014b;Sentis et al., 2017;Outreman et al., 2018). The effects on long-term population dynamics and parasitoid community structure and composition will depend on other parameters such as host species preferences and host densities, which for P. xylostella could also be favoured by climate warming (Furlong & Zalucki, 2017;Liu et al., 2002). To improve our mechanistic understanding of the effects of temperature variability, in particular at the higher end of the continuum, across multiple layers of biological organization, is extremely challenging (le Lann et al., 2021;Ma et al., 2021), but is imperative to predict the consequences of climate warming and concomitant ETEs. Importantly, species, species interactions and whole communities may differ in their response to more gradual climate warming and unpredictable ETEs, where the latter may cross species-critical thermal tolerance levels with severe repercussions (Harvey et al., 2023). This study contributes to this goal by demonstrating the effects of short-term exposure to high temperatures on nontrophic interactions. Future research should be aimed at investigating the impacts of ETEs over longer temporal scales (Koussoroplis et al., 2017;Harvey et al., 2020;Kankaanp€ a€ a et al., 2020;le Lann et al., 2021).

Author Contributions
T.P.M.C. and R.G.: designed and performed the experiments. T.P.M.C.: analysed the data and wrote the manuscript. R.G., P.W.J., J.A.H., J.J.A.L., M.D.: supervised and coordinated the experiments, discussed the results and critically reviewed the various drafts of the manuscript.

Declaration of Interest
None.