Climate Change: Resetting Plant-Insect Interactions

Elevated CO2 and temperature are altering the interactions between plants and insects with important implications for food security and natural ecosystems. Ecologically, the acceleration of plant phenology by warming is generating mismatches between plants and insect pollinators. Similarly, shifting the rate of plant development relative to insect development can amplify or minimize the consequences of herbivory. Warming also enables some insects to increase the number of generations per year, thus increasing damage to plant communities. The suitability of plant tissues as food for insects also is modulated by global change. Elevated CO2 typically increases the concentration of leaf carbohydrates and in combination with elevated temperature decreases nitrogen (N) content. Together, these changes lower nutritional value, causing certain herbivores to consume more foliage to meet their nutritional needs. Whereas the responses of primary metabolites in plants to global change are reasonably well understood, how elevated CO2 and temperature affect plant defensive compounds (allelochemicals) is considerably less predictable. Recent studies indicate that exposure to elevated CO2 suppresses the plant defense hormone jasmonic acid (JA) while stimulating production of salicylic acid (SA). By differentially affecting defense compounds, these changes in plant hormones potentially increase susceptibility to chewing insects and enhance resistance to pathogens. Exposure to elevated temperature, in contrast, stimulates JA, ethylene (ET), and SA, enhancing defenses. A deeper understanding of how elevated CO2 and temperature, singly and in combination, modulate plant hormones promises to increase our understanding of how these elements of global change will affect the positive and negative interactions between plants and insects. Chemoautotrophs notwithstanding, plants provide energy in the form of carbohydrates for all nonphotosynthetic organisms, including insects. Not long after the colonization of land by plants 510 million years ago, plants and insects have engaged in an evolutionary arms race that continues today—plants evolve mechanisms to minimize consumption by insects, and insects evolve mechanisms to circumvent these defenses. Rapid changes in Earth’s atmosphere initiated by the human use of fossil fuels is resetting this complex coevolutionary relationship, not only between plants and herbivores but also between plants and their mutualistic partners, including pollinators. Insects have the potential to cause enormous reductions in crop yields and the productivity of natural ecosystems, as well as to provide irreplaceable pollination services that underpin much of the world’s agriculture. The combustion of fossil fuels during the Industrial Revolution initiated a rapid rise in atmospheric CO2 concentration that is accelerating today; preindustrial levels were approximately 280 μL L−1 and below 300 μL L−1 for the previous 20 million years (Pearson and Palmer, 2000). Today’s atmosphere is approximately 397 μL L−1, and at current rates of fossil fuel combustion, the atmospheric CO2 concentration will double relative to the preindustrial level in the latter half of the 21st century (IPCC, 2007). In addition to directly affecting plant physiology, this increase in CO2, a potent greenhouse gas, is causing an unprecedented rate of planetary warming. Global average temperatures already have increased by 0.8°C, and the last two decades of the 20th century were the warmest in at least four centuries, and possibly in several millennia. At current rates of fossil fuel use, global mean temperatures will rise by 4°C by the end of the 21st century. Because of the complex relationships between plants and insects, both favorable and detrimental from the plant’s perspective, how this “one-two punch” of elevated CO2 and elevated temperature will affect plant-insect interactions is difficult to anticipate. Whereas most herbivorous insects do not respond directly to changes in CO2 in the atmosphere (Fig. 1; Guerenstein and Hildebrand, 2008), as exotherms they can be very sensitive to temperature, which affects their life cycle, population size, and geographic distribution (Bale et al., 2002). Populations of many insect herbivores are strongly regulated by invertebrate predators (top down), which also respond to temperature. In this update, we take the “plant’s perspective” and focus on our current understanding and major unresolved questions about how these two major elements of global change, elevated CO2 and temperature, affect insect populations and their relationship with plants. We will elaborate on the concept of ecological mismatches, where global change disrupts the synchrony between plants and insects. Then we will consider how global change affects plants as food for insects, including their chemical defenses, and how changes in leaf chemistry modulate herbivory. We conclude with a discussion of new findings that may reveal the mechanisms governing the interactions between plants, insects, and global change. Elevated atmospheric CO2 affects plant-insect interactions through its direct effects on plant metabolism and elevated temperature through its direct effect on plant and insect metabolism. Some insects respond directly to elevated CO2 during oviposition, when foraging for live or dead plant material belowground, or when foraging for nectar, for example (Goyret et al., 2008). At current and projected future levels of atmospheric CO2, the primary effect of elevated CO2 on the suitability of plant tissues as food is mediated largely through changes in plant chemistry and morphology. The activities of plants and insects often are coordinated in time—pollinators arrive just when flowers are ready, or feeding larvae enter a resting state (diapause) just as their host plant senesces. The synchrony between plants and insects is mutually constrained by their ecological and evolutionary relationships, yet rising atmospheric CO2 and global temperature challenge the status quo by altering leaf chemistry and advancing phenology. This perturbation increases the selection pressure for asynchrony and, as a result, an increasing number of plant and insect interactions have been characterized as ecologically “mismatched” (Wolkovich et al., 2012). The rapid advancement of plant phenology by global change brings into question how pollinators and herbivores will keep pace. From the plant’s perspective, rising CO2 increases carbohydrate levels in nectar (Erhardt et al., 2005) and drives greater reproductive investment in many plant species (Jablonski et al., 2002). Sweeter nectar favors some pollinators, such as certain bees and flies (Petanidou, 2005), but not all pollinators (Hoover et al., 2012). The interaction between elevated CO2 and temperature further complicates our understanding of plant interactions with pollinators. For example, elevated CO2 accelerates flowering time for entomophilic C3 species (Springer and Ward, 2007), yet rising temperatures may reduce nectar production by limiting water or by reducing flower longevity (Hoover et al., 2012; Wolkovich et al., 2012). It is important to note that the interactive effects of rising CO2 and temperature as manifested through pollinators remain largely unexplored (but see Hoover et al., 2012). It is likely that pollinator mismatches may be less common among generalists given the long history of adaptation to natural perturbations in climate (e.g. glaciation), but of greater importance for specialist plant-pollinator interactions. Comparisons of historical collections with observations of flight across the last decade indicate many generalist bees avoid mismatches by keeping pace with climate-induced advances in plant phenology (Bartomeus et al., 2011). For herbivorous insects, mismatches may be more prevalent as traditional host plant resources decrease in availability and nutritional suitability. For example, the comma butterfly (Polygonia c-album) altered its host preference from Humulus lupulus to Ulmus glabra and Urtica dioica, with a corresponding increase in insect performance (Braschler and Hill, 2007). Polyphagous species or those that undergo recent host switching or inclusion events (see also the brown argus butterfly [Aricia agestis]; Pateman et al., 2012) are not constrained by host range and thus are able to expand within their temperature optima faster than the plants on which they feed. This polyphagy may enable insects to track changing climate and move onto new plant resources. How plant resources and defense chemistries have changed, however, remains to be investigated and may resolve mechanisms underlying the host switch. Taken together, these patterns indicate natural selection may go a long way in resolving current mismatches. Global change not only modulates the beneficial relationship between plants and their pollinators, it also alters the magnitude of damage caused by herbivores. The largest ecosystem across the United States, the soybean (Glycine max)-corn (Zea mays) rotation, suffers substantial herbivory from the invasive Japanese beetle (Popillia japonica) on soybean. Because soybean is tolerant to herbivory during vegetative development when beetles emerge, damage has little effect on yield (Fig. 2). Earlier emergence of Japanese beetles caused by progressively warmer winters and spring should further reduce the potential for defoliation-induced yield losses by Japanese beetles (Fig. 2). The invasive soybean aphid (Aphis glycines) reduces soybean yield at moderate densities, in part because of its prevalence during reproductive stages when soybean is more vulnerable to herbivory (Fig. 2). As with beetles, if warming causes aphids to move from their alternate host, buckthorn (Rhamnus cathartica) trees, to soybeans earlier when beans are more tolerant of herbivore damage, then warming may reduce potential yield reductions and management costs. The consequences of insect damage depend on its timing relative to plant development. In soybean, the sensitivity of seed yield to leaf area removal by herbivory varies strongly among developmental stages (V, vegetative; R1, beginning bloom; R2, full bloom; R3, beginning pod; R4, full pod; R5, beginning seed; from National Crop Insurance Service publication 6302), where a 60% reduction in leaf area during R5 results in greater than 20% yield reduction, but no detectable yield reduction if the same leaf area removal occurs during vegetative growth. The dates (right) for different developmental stages are for soybean in the SoyFACE experiment (Castro et al., 2009). Vertical bars represent the time when Japanese beetles and soybean aphids are abundant (97% of the total annual population), and the black bars represent times of peak abundance (beetles in central Illinois: 26% of total population; Van Timmerman et al., 2000; aphids in southern Wisconsin: approximately 60% of total population; http://www.plantpath.wisc.edu/soyhealth/aglycine.htm). the timing of insect relative to plant development will its effect on seed insect species typically respond to increasing temperatures with an increase in development reproductive and number of generations within a (Fig. 1; and 2000). of these responses are likely to increase the magnitude of with on plant these global warming has effects on herbivore the number of life that can be in a In many insect life are than and In the of is by temperature, is and by human As temperatures insect development can be such that the sensitive the that is not to the development. were of insects an within a to increases in global however, have increased the of of in years of of patterns in central and that a substantial of the species in their an increased of and generations with species a increase in the number of generations after From the plant perspective, generations of on plants, can unprecedented levels of damage the of a damage may increase the of and and reproductive The of in the between and in the of of 2008). on a warmer temperatures are with increased species in for increase in temperature, the species of increases in a by species and plants are vulnerable to effects of have mechanisms for for of leaf from can be and to production of to can be and can be relative to et al., et al., 2012). however, can these mechanisms et al., et al., 2009). 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