Update on Climate Change 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 mL L and below 300 mL L for the previous 20 million years (Pearson and Palmer, 2000). Today’s atmosphere is approximately 397 mL L, 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 plantinsect 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 1 This work was supported by the National Science Foundation, the U.S. Department of Agriculture, and the U.S. Department of Energy. * Corresponding author; e-mail [email protected]. www.plantphysiol.org/cgi/doi/10.1104/pp.112.204750