Brian M. Irish, USDA-ARS Plant Germplasm Introduction and Testing Research Unit, Prosser, Washington 99164 USA (Brian.Irish@usda.gov)

Gayle M. Volk, USDA-ARS National Laboratory for Genetic Resources Preservation, 1111 S. Mason St., Fort Collins, Colorado USA 80521 (Gayle.Volk@usda.gov)

outline

1. Introduction
2. Climate change effects on pollinators and beneficial arthropods
3. Climate change effects on pathogens and pests
4. Conclusions
5. References
6. Acknowledgments

1. introduction

Agricultural productivity depends on pollinators and other beneficial arthropods. Naturally occurring and managed insects provide pollination services for horticultural fruit and vegetable crops, and for seed production. Within genebanks, insect pollinators are often key to successfully being able to produce ample quality seed during regeneration activities. In addition, predatory arthropods are used to manage plant pests through integrated pest management. Critical plant-pollinator relationships, as well as the balance between plants, pests, and beneficial arthropods can easily become disrupted by altered climatic conditions (Volk et al., 2023).

Changing climatic conditions can make disease and pest management increasingly challenging, affecting both crop production and plant collection conservation activities. Although most published research has focused on the impact of these problems on agricultural production, the same problems will affect the management of plant germplasm collections. Plant pathogen and insect pest survival, infection timing, and virulence are influenced by environmental factors including temperature, precipitation/moisture, and concentration of atmospheric gasses (Volk et al., 2023).

2. climate change effects on pollinators and beneficial arthropods

Climate change impacts plant physiology and phenology, and sometimes growing practices must be shifted to optimize and improve or sustain productivity. The effects of climate change on pollinators and the services they provide can often be indirect. This occurs when predicted warming trends cause the synchrony between flowering and pollinator activity to shift and become mismatched, affecting the services provided by pollinators and integrated pest management approaches (Freimuth et al., 2022).

Research is beginning to better address the effects of global warming on pollinators. Declines in honeybee (Apis meliffera L.) populations are caused by the use of agricultural pesticides, increases in pathogens, and would likely be exacerbated by increasing temperatures (Zhao et al., 2021). While honeybees and bumblebees can dissipate heat in their colonies using thermoregulating mechanisms, these diverted activities often come at the expense of reproductive rates as well as foraging and pollination efficiency (Gérard et al., 2022; Zhao et al., 2021). Greenop et al. (2020) noted that fava beans (Vicia faba L.) tended to show reduced seed weight when flowers were pollinated by heat-stressed buff-tailed bumblebees (Bombus terrestris L.). In the same bumblebee species, foraging was reduced due to a decrease in the number of individuals produced in colonies that were exposed to higher temperatures (Gérard et al., 2022). A species that commonly serves as a managed pollinator for seed regeneration, the alfalfa leafcutting bee (Megachile rotundata Fabricius), appears to be quite vulnerable to climate change with predicted earlier emergence leading to asynchronicity with their food source as temperatures rise (CaraDonna et al., 2018). In addition, as Grassl et al. (2018) indicate, the synergistic effects of stressors such as elevated temperatures and pathogens need to be considered when assessing negative impacts on honeybee pollinator colony health.

Under increasing temperatures, biological control with beneficial insects is often complicated and less effective. Biological control of pests (e.g., aphids, scale, mites) is an important tool when insecticide use is not an option due to its impact on insect pollinators. The diamondback moth (Plutella xylostella L.), a global pest of crucifers, is one example of a pest that is becoming more difficult to manage under climate change. Traditionally, insecticides were heavily relied on, which lead to resistance in pest populations. As an alternative, parasitoid wasps (Diagdegma semiclausum Hellén) have been used to reduce infestation of moth pests. However, global warming trends show expanding/favorable conditions for the moth and contracting/unfavorable conditions for the wasp (Furlong et al., 2017). In a review of biological control of aphids by apdidophagous ladybird species, Sloggett (2021) shows that cold-adapted ladybird species might decline or go extinct due to warming. These threatened ladybird species are retreating to higher latitudes or altitudes, avoiding warming temperatures. Access to biological control options in managing plant collections might be limited if the beneficial populations are significantly affected by climate change.

The effect of predicted increased precipitation in some regions will likely also impact pollinators and their activities. Antiqueira et al. (2020) found that pollinator visitation was reduced as precipitation increased, thereby affecting seed production. Increased precipitation predicted for midwestern regions of the U.S. would likely influence managed insect pollinators for plant genetic resources regeneration by genebanks in those areas.

3. climate change effects on pathogens and pests

In their comprehensive reviews, Velásquez et al. (2018) and Kybartaite et al. (2020) suggest that rising temperatures are a leading factor contributing to a surge in incidence and severity of crop plant diseases. Other climate change factors (e.g., humidity) can negatively influence disease and plant collection management, often to a lesser extent. Climate change models suggest a global warming tendency will impact many of the genebank sites within the USDA National Plant Germplasm System (NPGS; Volk et al., 2023). It is understood that plants that are grown under less-than-ideal environmental conditions (i.e., too hot or too cold) are often weaker and more susceptible to diseases (Kybartaite et al., 2020). Rising global temperatures and milder winters might lead to increased plant pathogen inoculum survival rates that would have otherwise diminished during colder temperatures (Ma et al., 2016). Crop- and site-specific approaches must be developed to address relevant diseases. However, cultural approaches could also have unintended consequences. For instance, altering planting dates to earlier in the year to evade climatic extremes (e.g., increasing summer heat) might also expose plants to less favorable conditions occurring earlier in the year that would also favor disease development.

Precipitation patterns have become progressively more unpredictable in the United States and elsewhere in the world (EPA, 2022). Although many NPGS sites in more arid areas of the country increasingly depend on dedicated irrigation infrastructure, too much precipitation and/or moisture is difficult to avoid when managing plant germplasm collections. Increased atmospheric moisture/humidity often leads to surges in fungal and bacterial diseases that can be especially problematic for spring-established perennial field-grown plant collections. Soil-borne diseases, especially root-rot complexes, can be particularly severe and easily disseminated during floods or prolonged waterlogged conditions (Reeksting et al., 2014).

Not all climate change scenarios are predicted to be harmful, as warmer conditions and elevated CO₂ levels might allow for healthier and more productive plants due to increased photosynthetic rates and/or a progression of crop cultivation to higher latitudes towards the poles (Chaloner et al., 2021). Unfortunately, these conditions might favor plant pathogens that could comigrate with the crops and offset any gains (Váry et al., 2015). While crop production may be able to move latitudinally towards the poles, genebanks and their dedicated infrastructure and resources are more difficult to relocate.

Like plant diseases, many insect pests of crops are favored by warming trends, erratic precipitation, and increased levels of CO₂ brought on by climate change. A number of pest-related factors are predicted to make crop production and plant germplasm collection management more difficult: pests’ increased local, regional, and global distribution; earlier epidemics due to overwinter survival and warmer springs; expanded multiplication rates and generation numbers; and the possible intensification of incidence and severity of diseases vectored by insect pests (Skendzic et al., 2021).

The predicted rise in global temperatures will likely play an outsized role in influencing insect pest population dynamics. In forecast scenarios where only moderate warming occurs, earlier infestations coupled with migration and expanded distribution towards higher latitudes has been shown for several insect pest species including the European corn borer (Ostrinia nubilalis Hübner) and black cutworm (Agrostis ipsilon Hufnagel) (Porter et al., 1991; Zeng et al., 2020). These lepidopteran species are two of the most detrimental corn pests, but they also affect numerous other essential crops and corresponding plant species in plant genetic resource collections. Pham and Hwang (2020) demonstrate that damage by the polyphagous cotton leafworm (Spodopter litura Fabricius) can be more severe when nutrient and defense compounds are reduced in a plant during physiological responses to stressful high temperatures. Complicating these scenarios, the lack of nutrients obtained from the plant could also cause reduced development in larvae with insect pests migrating to other crops for sustenance.

In another example, spider mites (arachnids) are agricultural pests that are generally favored by warmer temperatures. Prediction models that incorporate increased global temperatures predict intensified spider mite distribution as a result of accelerated population growth rates and shorter generation times for the two-spotted spider mite (Tetranychus evansi C.L. Koch), a significant pest of solanaceous species and other agricultural crops (Knegt et al., 2020; Ghazy et al., 2019). Tscholl et al. (2021) showed that elevated temperatures played a role in developmental plasticity between the two-spotted spider mite and the predatory mite Phytoseiulus persimils Athias-Henriot, favoring the pest and limiting biological control efficiency.

As increasing temperatures lead to expanding insect pest populations, it is likely that plant pathogenic diseases vectored by insects and mites will also increase. Huanglongbing disease of citrus (spread by the Asian citrus psyllid; Ajene et al., 2020) and zebra chip of potato (spread by Bactericera cockerelli; Zeilinger et al., 2017) are both examples of psyllid-vectored bacterial diseases with expanded global ranges attributed to globalization, but also to larger insect pest populations favored by warming trends. Insect-vectored viral diseases of crops are also predicted to expand globally. With rising global temperatures, Wei et al. (2019) showed possible expanded ranges and risk maps for the invasive pineapple mealybugs (Dysmicoccus spp.), a vector of pineapple associated wilt viruses.

4. conclusions

Pollinators and beneficial arthropods will likely experience both direct and indirect effects of climate change. Pollination and biological control approaches using arthropods might also suffer from increased use of agrochemicals used to mitigate the rise in damaging insect pests and diseases. It is important to point out that not all climate change effects are a cause for alarm, as some research shows that many insect pollinators and biological control insects have the capacities for plasticity and resilience (Sloggett, 2021).

If diseases and insect pest pressures are intensified by climate change, long-term sustainable efforts to conserve plant collections will be further stressed. Possible genetic erosion, population shifts, and/or loss of diversity can occur during plant regeneration (Cieslarová et al., 2011); all these detrimental outcomes could be aggravated by disease and insect pest pressures. Other biotic factors that can complicate plant genetic resource management in an era of climate change include possible increased pressure from both native and introduced pervasive agricultural weed species, diminished beneficial soil microbes, and declining activities of essential pollinator species. Although the effects of climate change on diseases and insect pests cannot be predicted precisely, crop production and plant collection management approaches must develop solutions and adapt best practices in response to these threats.

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6. acknowledgments

Citation: Irish BM, Volk GM. 2023. Climate change affects plant interactions with pollinators, pathogens, and pests. In: Volk GM, Moreau TL, Byrne PF. Conserving and Using Climate-Ready Plant Collections. Fort Collins, Colorado: Colorado State University. Date accessed. Available from: https://colostate.pressbooks.pub/climatereadyplantcollections/chapter/pollinators-pathogens-and-pests/

This eBook chapter was developed through a collaboration among USDA-Agricultural Research Service, Colorado State University, and the University of British Columbia Botanic Garden, with additional funding from the USDA-NIFA-Higher Education Challenge Grant (2020-70003-303930).

Editor: Katheryn Chen