Complex responses of global insect pests to climate change

Insect pests strongly affect the productivity and profitability of agriculture and forestry. Despite the well-known sensitivity of insects to abiotic effects such as temperature, their potential responses to ongoing climate change remain unclear. Here we compile and review documented climate change responses of 31 of the globally most impactful phytophagous insect pests, focussing on species for which long-term, high-quality data are available. Most of the selected species show at least one response affecting their severity as pests, including changes in geographic range, population dynamics, life-history traits, and/or trophic interactions. Of the studied pests, 41% only show responses that are linked to increased pest severity, 4% only show responses of decreased severity, whereas importantly 55%, the majority of studied pests, show mixed responses including both increased and decreased severity under ongoing climate change. Variability in impact is further supported by a thermal sensitivity analysis showing little benefit of climate warming in relation to the optimal developmental temperatures for the majority of these pests under both current climate and future projections. Overall the results show that calculating the net effect of climate change on phytophagous insect pest impact is far from straightforward. The documented variation in responses, e.g. between agricultural and forest pests, indicates that efforts to mitigate undesirable climate change effects must target individual species, taking into account the complex ecological and evolutionary mechanisms underlying their responses.


45
Climate change and insect pest impact. Insect pests have major detrimental impacts 46 on agricultural and forestry production 1 that are likely to increase with anticipated rise in 47 demands for food 2 , bioenergy feedstocks and other agricultural products. For example, 48 animal pests (mainly insects) cause estimated losses of ca. 18% of total global annual 49 crop production 3 . Many forest pests, such as the gypsy moth (Lymantria dispar) and and likely responses to ongoing climate change is essential to counter changing risks. 66 Widespread ecological damage through range expansions and increasing frequencies of 67 All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/425488 doi: bioRxiv preprint 4 outbreaks are increasingly reported 14-17 , but there is a severe deficiency in 68 comprehensive information on insect pests' responses [18][19][20] .  To assess current empirically-based knowledge within these four categories of response 88 to climate change, we reviewed primary literature on 31 globally detrimental insect pest 89 species. Species were selected to cover both agricultural and forestry pests, representing 90 All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/425488 doi: bioRxiv preprint 5 various feeding guilds (Fig. S1), being present in various biomes and having large 91 geographic ranges (Fig. 1). Furthermore, we only selected species that have been well 92 studied over a long period. While this approach perhaps leads to biases in terms of 93 geographical range and taxonomy, we feel that it is compensated by having high-quality 94 comprehensive datasets available for the species. This is also critical for allowing an 95 integrated assessment of all the four major response categories outlined above in each 96 species and would not be possible otherwise. As there is a need for more information on 97 biological mechanisms relating to past and present climate change responses in several 98 key biological traits for single organisms 18 , we here provide an update on a number of 99 such mechanisms (range expansion, life-history, population dynamics and trophic 100 interactions) for the selected species in hopes that the data can be used for further 101 predictive modelling. This information is presented in the form of species-specific 102 descriptions and data tables in Supplement 1. We also identify critical knowledge gaps, 103 and highlight aspects that require further research to anticipate, mitigate and manage 104 climate-driven changes in pest impacts.

106
All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was not peer-reviewed) is the author/funder.  affect insect ecology, we assume that species in disparate habitats will have different 136 All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was not peer-reviewed) is the author/funder.   (Table   149   S1). We used a modified version of a generic impact score system to assess impact and   (Table S3). Latitude and longitude coordinates were either copied straight from the  The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/425488 doi: bioRxiv preprint Ambient temperatures at each location in our species database (Table S3)   The overall Tamb for each of the time periods were compared against the species Topt at 204 each location in two ways. First by visually comparing the differential between Topt and 205 All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/425488 doi: bioRxiv preprint 11 Tamb (Fig. 3), where a small value (close to 0) indicates high thermal suitability, and then 206 with a phylogenetically corrected generalized linear least square model (pgls) 207 investigating the relationship between thermal suitability (expressed as Tamb / Topt) and 208 absolute latitude. A high value (close to 1) indicates high thermal suitability. Models were 209 run using primarily the "pgls" function in the "caper" package for R 42 . Overall model results 210 are shown in Table S4 and the full R-code workflow can be found at GitHub:  (Table S1), and 28 (90%) present more than 217 one response (Fig. 2a). Of the 29 showing some response 26 (90%), 18 (62%), 16 (55%) 218 and 4 (14%) respectively show changes in: geographic range, population dynamics, life-219 history (traits related to phenology and voltinism), and trophic interactions (Fig. 2b). While 220 at least one reported response of almost all of these species is likely to increase pest 221 severity (e.g. range expansion or increases in population density), 59% (17/29) of them 222 also show responses likely to reduce pest severity (e.g. range contraction or decreased 223 physiological performance), and often this reduction occurs simultaneously with other 224 responses likely to increase severity (Fig. 2c). The most common severity-reducing 225 responses are reduction in pest population density (13/29), followed by range contraction 226 (6/29) (Fig. 2c). The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/425488 doi: bioRxiv preprint 12 228 All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was not peer-reviewed) is the author/funder.  (Table S1). The range of the winter moth (Operophtera brumata) has also 245 expanded, towards higher latitudes and more continental areas at the northern European  (Table S1). Several species also show both severity-249 increasing and severity-reducing responses in different parts of their ranges. Notably, 250 thermal tracking 43,44 has been observed in some species (4/17), e.g. the spruce budworm 251 All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/425488 doi: bioRxiv preprint 14 (Choristoneura fumiferana; Table S1) has expanded its geographic range towards higher 252 latitudes while it has retracted, or its abundance has declined, at lower latitudes. Similarly, 253 northward range expansion of the hemlock woolly adelgid (Adelges tsugae) has been 254 observed in the USA, while the economic damage it causes is decreasing in the southern 255 part of its range due to poor heat tolerance of young nymphs during summer (Table S1).  (Table S1). Further, the range of the western corn rootworm (Diabrotica virgifera virgifera) 274 All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/425488 doi: bioRxiv preprint in Europe has expanded, and it can cause large ecological damage by spreading maize 275 chlorotic mottle virus to several natural hosts (Table S1) (Table S1). However, pests in annual and perennial systems might differ in 297 All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/425488 doi: bioRxiv preprint general susceptibility to phenological mismatching, inter alia the former might be more 298 sensitive to phenological host limitation; especially relative to bark beetles and root 299 feeders. Taken together, while there are some differences that seem to associate with 300 whether the system is annual or perennial, pests in both systems show large variability in 301 how ongoing climate change is affecting both their ecological and socioeconomic impact. compared to their ambient habitat air temperatures (Tamb) (Fig. 3). Relating ambient 309 temperature during the growing season in past, present and future climates to Topt shows 310 large variability in how pests are expected to benefit from climate change owing to 311 regional complexity. In general, warming climates are expected to be beneficial for growth 312 and development, and indeed, in all but two cases Tamb closely approached Topt when 313 comparing past, current, near future and future climates (Fig. 3B). This conclusion was 314 also supported by a phylogenetically-informed regression analysis (Table S4). Further, 315 this analysis suggested that pests at higher latitudes have greater disparity between Tamb   316 and Topt, indicating greater capacity to benefit from climate warming, unlike more low 317 latitude pests that are already close to Topt. Low latitude species also potentially risk 318 increasing frequency and intensity of heat stress as climate warms 51 , a notion receiving 319 support in a recent analysis of the upper thermal tolerance of 15 dipteran pests 50 . 320 All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. represent a wide geographic distribution (Fig. 1A), the studies on Topt used here mostly 342 reflect populations sampled in the northern hemisphere (Fig. 3C). This is a general    The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. modelling studies, to identify the factors related to climate change that most strongly 404 influence pest population growth and performance, such as for example the increased negligible for many of the studied pests (Fig. 3C). Indeed, since low-latitude species 421 All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/425488 doi: bioRxiv preprint 22 already showed Tamb close to Topt, as climates warm Tamb for these species may 422 surpass Topt, thus decreasing pest severity, under future climates 50,51 . 423 6. Finally, and importantly, the patterns of regional variability and complexity described 424 here are likely to apply to non-pest insects as well as non-insect species in addition to 425 the 31 insect pest species assessed here. The extent of generality of responses 426 across various taxa will be important to assess in future studies 14,20,59,65 . The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/425488 doi: bioRxiv preprint