Insects take a bigger bite out of plants in a warmer, higher carbon dioxide world
Carbon dioxide is a potent “greenhouse” gas. The dramatic increase in its concentration in the atmosphere as a result of human activities, beginning with accelerated fossil fuels combustion in the late 18th century, and perhaps even earlier, with modern agricultural expansion 8,000 years ago (1, 2), is driving a striking rise in global temperature (3). For the past 650,000 years, until relatively recently, the concentration of CO2 in the atmosphere was 280 ppm or less; however, the current concentration exceeds 380 ppm and, on its present trajectory, will surpass 550 ppm by 2050 (3). The accumulation of CO2 and other greenhouse gases in the atmosphere is forcing an elevation of global mean temperature; during the lifetime of child born today, the average temperature of the earth will increase by as much as ≈6°C (3). Working in concert, elevated temperature and CO2 are redistributing plant and animal communities on the surface of the earth (4). Because of the direct effect of CO2 and temperature on global food supplies, the influence of these changes on plant physiology and ecology is being actively studied (4–7). How these elements of global change may alter the interactions between plants and the insects that feed on them is relatively unknown. By bringing to light secrets contained in the fossil record, Currano et al. (8), published in this issue of PNAS, found that the amount and diversity of insect damage to plants increased in association with an abrupt rise in atmospheric CO2 and global temperature that occurred >55 million years ago. If the past is indeed a window to the future, their findings suggest that increased insect herbivory will be one more unpleasant surprise arising from anthropogenic climate change.
The intersection of the Paleocene and Eocene epochs 55.8 million years ago was marked by a sudden, transient elevation in atmospheric CO2 and a corresponding rise in global temperature. During this Paleocene–Eocene Thermal Maximum (PETM), the concentration of CO2 tripled, and surface temperatures rose by ≈5°C in 10,000 years. The speed with which temperature increased makes the PETM a powerful deep-time analog for contemporary anthropogenic climate change.
To examine how the rapidly increasing CO2 and temperature in the PETM affected insect damage to leaves, Currano et al. (8) unearthed >5,000 fossil leaves from the Bighorn Basin of Wyoming and measured the type, frequency, and extent of herbivory. The leaves revealed a dazzling array of damage types, from gaping holes inflicted by chewing insects with large, powerful mandibles and galls formed by wasp oviposition, to delicate mines created by larval moths and flies as they consumed nutritious leaf mesophyll, to the piercing damage caused by aphids and mites. As the elevation in CO2 forced mean annual temperature to rise from 10.5° to 20.1°C, the percentage of leaves damaged increased from ≈38% to ≈57%, and the diversity of damage increased as well. The expansion in types and magnitude of leaf damage during the PETM may, in part, reflect fundamental changes in the interaction between plants and insects.
Although the pattern of increasing herbivory approaching the PETM is clear, the mechanisms governing the escalation in herbivory are elusive and represent a complex interplay of the effects of temperature and CO2 on insects and plants. From the distribution and behavior of contemporary insects, it is reasonable to hypothesize that increased herbivory should follow rising temperatures. As with many taxa, the number of insects per unit area increases as one moves from cold, northern latitudes toward the warmth of the equatorial regions and from high peaks down to mountain bases (9, 10). Development time and growth rates accelerate, and the threshold temperatures for movement are exceeded earlier with warming temperatures for many, but not all, insects (11). The strength of these generalizations is, however, tempered by the close synchrony of insect life cycles with plant phenology and the great variation in the response to temperature among insects with widely divergent life history traits. Although the respiration rates and food consumption of insects may increase with temperature in the isolation of the laboratory, changes in the composition of the plant community (12, 13), or individualistic responses of plants and insects to temperature (14), may be the primary factors affecting herbivory in natural communities as the climate warms.
The mechanisms governing the amount of herbivore damage become even more complex when one considers the potential interactions with elevated CO2. Many insects respond directly to CO2 as a cue for identifying favorable oviposition sites or desirable food sources (15); however, the CO2 concentrations producing this response are typically much higher than those expected from global change. The indirect effect of elevated CO2 on leaf chemistry, and subsequently on the palatability of leaves to insects, likely will have the greatest influence on herbivory (16).
A rise in CO2 generally increases the carbon-to-nitrogen ratio of plant tissues (17, 18), reducing the nutritional quality for protein-limited insects (19). Insects may accelerate their food intake to compensate for reduced leaf nitrogen content (19–21), although this is not always the case (22, 23). By exposing a soybean crop to elevated CO2 under otherwise natural field conditions (Fig. 1), foliar damage inflicted by Japanese beetles (Popillia japonica; Fig. 2) more than doubled, and, when given a choice, both Japanese beetles and Mexican bean beetles (Epilachna varivestis) preferred to feed on high-CO2 leaves (24). Recent results indicate that growth under elevated CO2 compromises the ability of soybean plants to produce defensive proteinase inhibitors (C.L.C. and J. Zavala, unpublished data) and that consuming these poorly defended leaves increases the fecundity of Japanese beetles (25). Future elevated levels of atmospheric CO2 will fundamentally alter the relationship between plants and insects, and accelerated feeding by insects may offset some of the predicted increases in agricultural productivity associated with greater levels of CO2 in the atmosphere (5, 26).
The Soybean Free-Air Concentration Enrichment (SoyFACE) experiment at the University of Illinois (www.soyface.uiuc.edu), following a factorial design, exposes a soybean crop to the elevated levels of CO2 and O3 expected to occur in the Midwest by the middle of this century. The SoyFACE facility enables precise control of the atmosphere above the plant canopy under otherwise natural conditions, while permitting insects and pathogens unrestricted access. Equipment for sensing and controlling gas concentrations is located at the center of the plot. The tower at the upper left measures canopy temperature, and the caged subplots exclude canopy insects. Research at SoyFACE is supported by the Office of Science (BER), U.S. Department of Energy.
Japanese beetles (Popillia japonica) consuming soybean leaves. The Japanese beetle is a broadly polyphagous species introduced into the United States in 1916 that is now expanding its range throughout the Midwest (27). Japanese beetles are attracted to poorly defended, high-sugar soybean leaves that develop under elevated CO2. Future increases in CO2 and temperature may further the success of such destructive invasive species (28)
Understanding how these rapid anthropogenic changes in climate and atmospheric chemistry will affect the “goods and services” provided by native and agricultural ecosystems is one of the greatest scientific challenges of our time. By interpreting the “text” of the fossil record, Currano et al. (8) suggest that global change will result in greater insect damage to valuable crops and forests. Open-air experiments, such as SoyFACE (Fig. 1 and ref. 29), that combine precise experimental control with the opportunity for realistic ecological interactions will be instrumental in developing a mechanistic understanding of trophic interactions, as well as in devising the next-generation theory for predicting such interactions in the future.
Footnotes
- †To whom correspondence should be addressed. E-mail: delucia{at}life.uiuc.edu
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Author contributions: E.H.D., C.L.C., P.D.N., and B.F.O. wrote the paper.
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The authors declare no conflict of interest.
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See companion article on page 1960.
- © 2008 by The National Academy of Sciences of the USA
