Impacts of climate change on tomato, a notorious pest and its natural enemy: small scale agriculture at higher risk

Climate change (CC) impacts global agricultural production (e.g. Rosenzweig et al 2014, Fleisher et al 2017, Moat et al 2019, Yoon et al 2019). Considerable effort focuses on exploring CC risks on production of stable crops, with studies on vegetables, pests and natural enemies underrepresented in the literature (Porter et al 2017). While some studies have included both crops and pests (e.g. Berzitis et al 2014, Ponti et al 2014, Ramirez-Cabral et al 2018, Ramos et al 2018, Santana et al 2018), none has looked at a crop-pest-natural enemy system. We provide for the first time an assessment of CC impacts on the climatic suitability of agricultural areas for a vegetable-pest-natural enemy combination of global importance: Tomato (Solanum lycopersicum L.), the two-spotted spider mite (Tetranychus urticae (Koch)) and its key natural enemy, the predatory mite Phytoseiulus persimilis Athias-Henriot.

Tomato is one of the most popular vegetables in the world, with an annual value exceeding 90 billion USD (FAOSTAT 2019). Tomato acreage increased by almost threefold in the last 50 years to around five million ha in 2015. In the EU, one of the most important tomato producers, more than 85% of tomatoes are produced outdoors, mainly in Mediterranean Member States (Eurostat 2019). Modelling of worst-case CC scenaria revealed substantial restrictions of suitable areas for cultivation of the crop (da Silva et al 2017b, Ramos et al 2018). The Paris agreement created substantial interest in assessing the impacts of a 1.5 °C warming in different productive sectors (Hoegh-Guldberg et al in press), but currently no information exists for tomato. Furthermore, prior assessments for the crop were not restricted to agriculturally suitable land, as they included all terrestrial areas of the planet.

A suite of pests attack tomato, including the two-spotted spider mite (Meck et al 2013, Gigon et al 2016), one of the world's most notorious pests (Vacante 2015), with a host range of more than 200 cultivated crops (Migeon and Dorkeld 2006–2017). Control costs exceed $400 million annually in pesticide sales alone (van Leeuwen et al 2015). The pest has developed resistance to close to 100 chemical active ingredients, more than any other plant-feeding arthropod (Michigan State University 2019). The sequencing of its genome illuminated a vast array of unique detoxification genes that contribute to its impressive ability to develop resistance (van Leeuwen et al 2010, Grbić et al 2011).

The unmatched ability of the two-spotted spider mite to evade control has catalysed early on the search for effective natural enemies. The predatory mite, P. persimilis, has been one of the key successes of biological control worldwide (Knapp et al 2018). The predator is both mass produced by companies and occurs in natural populations around the globe (Demite et al 2014). The mite feeds almost exclusively on the two-spotted spider mite, and unlike its prey, it is limited by both high and low temperatures, and lacks the ability to diapause (Khodayari et al 2012, Coombs and Bale 2013). Phytoseiulus persimilis is known to develop strains adapted to the harsh environment of tomato leaves (Ditillo et al 2016), that are defended by glandular hairs oozing sticky exudates.

In the current work we used CLIMEX, a species distribution model, to assess the impacts of CC on tomato, the two-spotted spider mite and P. persimilis. CLIMEX is a semi-mechanistic model that has been used successfully to project climatically suitable areas under CC for many species including insects, plants and pathogens (Berzitis et al 2014, Burgess et al 2017, Ireland et al 2018). We restrict our analyses to agricultural areas equipped with AEI (Siebert et al 2013), and rely on outdoor experiments and a farmer survey to validate model findings.

The specific aims of the study were: (a) develop a global niche model for tomato, the two-spotted spider mite, and P. persimilis; (b) evaluate model results using global datasets, outdoor experiments and expert/farmer input and (c) assess the effects of CC by 2050 on the three species on areas equipped with irrigation facilities.

CLIMEX models and spatial analysis

Model validation

CLIMEX models and spatial analysis

Approximately 90%, 98% and 99% of the presence data for tomato, the two-spotted spider mite and P. persimilis, respectively, fell in areas with EI values greater than 10. Detailed results of the baseline model for each species are shown in the supplementary material and table S1.

Tomato

Approximately 20% of AEI was classified as unsuitable or low suitability (EI ≤ 30) for commercial tomato production in 1975H, while the rest 26%, 34% and 20% fell in the medium (EI from 31 to 40), high (EI from 41 to 50) and optimal categories (EI ≥ 50), respectively (figures 1, 2, S1(b), table S3). Categorisation of EI values in different classes was based on a spatial land use dataset depicting outdoor tomato crops (Monfreda et al 2008—see section on Categorisation of EI values suitable for commercial tomato production in supplementary material). The historic range for optimal suitability includes extensive areas throughout the world, and especially in the Americas.

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In 2050 land available for tomato cultivation in the three upper classes is estimated at 69% of AEI (figures 1, 2 and S1(c)), because approximately 15% of AEI becomes unsuitable-low suitability, while 3% changes from unsuitable-low suitability to medium suitability or higher. Approximately 43% of AEI remains in the same category, while 13% of AEI becomes less and 9% more suitable. Most of the improvements in land suitability occur in North America, Europe and China. The model predicts that 12 nations in total (five EU members States) experience a positive impact of CC on conditions for tomato production (figure 3). Conditions become less suitable for commercial tomato cultivation on extensive areas in India and parts of South East Asia, as well as scattered areas in the Middle East and Africa (figures 2 and 3). Six out of the 10 worst affected by CC countries are in Africa, while the rest four nations are: Pakistan, Iran, India and Mexico (figure 3).

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Two-spotted spider mite

Approximately 95% of AEI is classified as suitable for the two-spotted spider mite, with slightly less than 1/3 of AEI in the low suitability category, and 25%, 19% and 20% in the medium, high and optimal classes (figures 2 and S2(b), table S3). The historic range for the two-spotted spider mite includes the largest part of AEI in all continents, except for northern areas of Scandinavia, the Russian Federation and China. (figure 2).

Land suitable for the two-spotted spider mite drops slightly to 92% of AEI in 2050, with both expansion and contraction areas covering less than 5% of AEI (figures 2 and S2(c), table S3). Suitability remains the same on 57% of AEI, while 17% becomes less and 16% more suitable. The pest follows a northward expansion trend.

The two-spotted spider mite continues to persist in all areas suitable for commercial tomato production (suitability of land for tomato production medium or higher) in 2050. However, suitability of climate for the pest changes to a higher category on 15% or more of AEI suitable for commercial tomato production in nine countries: India and Pakistan in South East Asia, Nigeria and Cameroon in Africa, Italy, Bulgaria, Ukraine, Romania in Europe and China in Asia (figure S2(d)). The climate worsens for the pest in only two countries: Sudan and Uzbekistan.

Phytoseiulus persimilis

Only 56% of AEI is classified as suitable for P. persimilis (figures 2 and S3(c), table S3). Slightly less than 20% of AEI falls in the low suitability category, while 14%, 10% and 14% in the medium, high and optimal classes. AEI suitable for P. persimilis drops to 50% of AEI in 2050 (figures 2 and S3(c)), with expansion areas covering 5% and contraction areas 10% (table S3). Suitability remains the same on 25% of AEI, while 14% becomes less and 7% more suitable.

Under historical data, climatic conditions are not favourable for biological control (BCI < 0) on 40% of AEI, while conditions favour pest suppression by the natural enemy (BCI ≥ 0) on 15% of AEI (figures 1 and S3(d) and table S4). The pest persists in the absence of the natural enemy on 39% of AEI. In 2050, the pest persists on 42% of AEI where the natural enemy is not present (figure S3(d) and table S4). The percentage of AEI where conditions favour biological control drops to 7%, while biological control is not favoured on 43% of AEI. Close to 8% of AEI switch from adequate to failing biological control, including an extensive area on the South east coast of the US, smaller areas mainly in West South America, and substantial areas in South Asia, and especially in South East China (figure S3(d).

In areas with conditions suitable for commercial tomato production (suitability of land medium or higher), biological control is effective on 15% of AEI in 1975H and drops to 7% in 2050 (table S4). Changes are not uniformly distributed among the top producing tomato nations (figure S3(e)). Brazil in South America, Algeria and Cameroon in Africa, and Indonesia and China in Asia experience a substantial reduction in the percentage of land under effective biological control.

Model validation

The current study predicts a net loss in suitable AEI of 11.3% for tomato. Loss and gain of suitable AEI is not distributed uniformly across the globe, resulting in dramatic impacts at the country level in some cases. Seven countries are projected to lose from 30% to almost all of their area suitable for tomato production (figures 2(a) and 3). Major losses of suitable AEI are expected to occur exclusively in parts of Africa (Sudan, Nigeria, Benin, Cameroon, Egypt, Ghana), South Asia (India and Pakistan) and Iraq and Mexico (figure 3). Most of the affected regions are characterised by small scale agriculture (Lesiv et al 2019), and are therefore more prone to CC risks.

The large variations in temperature on AEI is a major factor determining its suitability for tomato production, as was previously shown for wheat, rice, maize and soybean in a different modelling context (Zhao et al 2015). The CLIMEX model is very sensitive to minor changes in the value of irrigation (table S1), highlighting the importance of irrigation provision for tomato cultivation. The availability of irrigation water under CC seems to be a realistic scenario for most countries (Elliott et al 2014), and offers an adaptation strategy via the expansion of AEI into new suitable areas of agricultural land not equipped with irrigation facilities. For example, Sudan and countries in the sub-Saharan Africa are projected to have an abundance of water towards the end of the century even under RCP 8.5 (Elliott et al 2014), and can expand their AEI into agricultural land of high suitability (Portmann et al 2010). However, several countries are projected to have a deficiency of irrigation water—Morocco, West Egypt, Iraq, Uzbekistan, Pakistan, North West India, east China and Mexico (Elliott et al 2014)—and therefore our model may underestimate CC impacts as it assumes the provision of adequate volumes of irrigation water. Drought severity under CC is an ongoing area of research (Swann et al 2016). Engineering solutions, such as the cultivation of the crop under nethouses with cooling systems can enable its production in hot areas. Selection of heat/drought resistant varieties is another pathway towards CC adaptation. Development of models that incorporate the potential effects of new technologies/breeding efforts in the assessment of CC impacts (e.g. Asseng et al 2019) would enable the evaluation of the viability of different adaptation options.

Previous work on CC effects on tomato cultivation lacked a relevant spatial context as it included all terrestrial areas of the planet. Parameters of the baseline CLIMEX model (table S1) are generally similar/within reasonable range of that of da Silva et al (2017b). Variation in parameter values between the two studies probably reflects differences in the initial areas used for parameter estimation, and the literature sources for parameter identification. Saadi et al (2015) modelled CC impacts on tomato yield in the Mediterranean under the A1B scenario in 2050 and showed no major impacts, in accordance with the current work. Da Silva et al (2017b) and Ramos et al (2018) used projections for a warmer world than the GCM/SERS used in the current study and reported both restrictions and expansions in land suitable for tomato cultivation. The choice of the modelling platform, GCM and CC scenario/RCP can significantly influence predictions (Meynard et al 2013, Shabani et al 2016). An additional factor that needs to be incorporated in future modelling efforts is the potential positive effect of CO₂ fertilisation on tomato growth and yield. Wei et al (2018) have shown that elevated CO₂ mitigates the negative effects of drought and low nitrogen availability on the yield of tomato plants, and elevated CO₂ can also enhance tomato quality (Dong et al 2018).

Regional worsening of conditions for tomato cultivation is associated with an intensification of two-spotted spider mite infestations. Four countries with better conditions for the pest under CC (15% or more of area changing to a higher class) are in the top 10 countries worst affected by CC for tomato production: India and Pakistan in Asia, and Nigeria and Cameroon in Africa (figures 3 and S2(d)). The climate becomes less suitable for the pest in just two nations: Sudan and Uzbekistan. Drought can potentially intensify two-spotted spider mite pressure on tomato (Ximénez-Embún et al 2017), while a recent study on maize suggests that the increase in CO₂ can attenuate some of the positive effects of temperature increase on the species (Xie et al 2018).

Expected failures in biological control are highly concentrated in North and South America, China and South East Asia, as well as parts of the Mediterranean (figures 1 and S3(d)). Five countries (Brazil, Cameroon, Indonesia, China, and Algeria) experience a 20 to 40-unit reduction in area under effective biological control by 2050 (figures S3(d)–(e)). No meaningful increase in the area under effective biological control occurs for any country (figure S3(e)). Effects of CC on biological control as estimated in the current study represent the most optimistic scenario, as the underlying assumption is a temporal overlap between pest and natural enemy. Potential temporal differentiation in the periods of activity of pest and natural enemy will result in decreased effectiveness of biological control (da Silva et al 2017a). Both pests and natural enemies can adapt to CC through phenotypic plasticity and genetic adaptation, and future evaluations of CC impacts need to incorporate phenotypic and evolutionary processes (e.g. Bush et al 2016, Macfadyen et al 2018).

Model results showed good correspondence with the short-term outdoor experiments (figures S5 and 6), especially when irrigation in the model was adjusted to site-based evapotranspiration. Coefficient of determination values in regressions for the baseline model ranged from 26% for the two-spotted spider mite to 56% for tomato, and increased to 46% and 72%, respectively when irrigation was adjusted to field evapotranspiration (-see Results and figures S5–6). Future research based on long-term experiments would provide a more complete picture of the relationship between model predictions and field observations. EI values from the baseline CLIMEX model showed very good correspondence to farmer/expert opinion, highlighting the relevance of results to pest outbreaks in the field (figure S7). Further research needs to evaluate whether farmers are already experiencing a higher frequency of CC-related spider mite outbreaks as has been shown for other pests (e.g. Savary et al 2019). In North Carolina for example, Meck et al (2009) report an increase in spider mite outbreaks on tomatoes and other vegetables, with efforts focusing on improving biological control by P. persimilis (Meck et al 2013). While farmers in Cyprus generally agree that spider mite infestations are more problematic in recent years, it is very difficult to tease apart whether the increase is because of CC alone or because of the withdrawal of several pesticides from the EU market that were used against the multi-resistant pest.

Understanding and adapting to CC effects requires work on both detailed biophysical models (Antle et al 2017), as well as broader picture studies at different trophic levels, such as the current work. The present study predicts substantial impacts under a 1.5 °C warming, suggesting that impacts can be severe if the world overshoots this target. Future studies in the direction of developing detailed biophysical crop models for tomato and other vegetables, including CO₂ effects, as well as incorporating pest and natural enemy impacts under different CC futures (Donatelli et al 2017), including the difference between 1.5 °C and 2 °C of warming, will aid adaptation efforts.

We thank Ms Athanasia Mandoulaki for field work help, and N Tzortzakis for commenting on the manuscript. The work was funded by the FACCE ERA-NET Plus—FACCE JPI GENOMITE project through EC and national sources (EC contract 618105), including the Cyprus Research Promotion Foundation (FACCE/1013/10), the French Agence Nationale de la Recherche (Grant ANR-14-JFAC-0006-01 to MN, AM and MST), and the metaprogramme Adaptation of Agriculture and Forest to Climate Change launched by the French National Institute for Agricultural Research (INRA).

Any data that support the findings of this study are included within the article.