Greenhouse gases, the gases involved in determining the I Earth’s average temperature and climate, are accumulating at a rapid rate within the atmosphere. Such gases include carbon dioxide, methane, nitrous oxide, ozone, and chlorofluoro-carbons. By far the most important of these is carbon dioxide, CO2,whose contribution to the total greenhouse gas warming effect is at least 73%. For this reason, most research pertaining to insects and greenhouse gases has focused on the response of insects to elevated levels of CO2. Global atmospheric carbon dioxide levels are increasing at an astonishing rate, mainly because of the burning of fossil fuels. The atmospheric concentration of CO2 has increased from a preindustrial level of about 270ppm to a current level of about 381 ppm, an increase of over 100 ppm or 41%. According to some reports, the atmospheric concentration of CO2 will likely stabilize at four times the preindustrial levels. Most studies indicate that CO2 levels will at least double from preindustrial levels over the next five to ten decades. This increase represents one of the most large-scale and wide-reaching perturbations to the environment.
Many of the changes in insect populations likely to result from elevated CO2 will be brought about by changes in plant chemistry. The chemical changes in plants result from increases in plant carbon, decreases in nitrogen, and increases in levels of defensive compounds such as phenolics. In addition, global warming, which will result from elevated levels of greenhouse gases, may increase the reproductive capabilities of some insects and change their distributional ranges. This could change the abundance of some pest species and disease vectors. Some of the myriad effects of elevated CO2 on insects are summarized in Fig. 1 .
STUDYING THE EFFECTS OF GREENHOUSE
GASES ON INSECTS
Most published studies on the effect of CO2 on insects tell of experiments in which plants and insects are confined to CO2 levels of 700-710 ppm, or about double the 2000 level. Such experiments are typically conducted in the laboratory, where well-watered potted plants are grown in nutrient-rich soil and maintained under elevated CO2 for several months. Insects are introduced onto these
FIGURE 1 Schematic representation of the effects of elevated CO2 on insects.
experimental plants, and their feeding rates and performance are measured.
Studying the effects of elevated CO2 on altered temperature and rainfall patterns, and the effects on insects of these modifications of the environment is much more problematic. It is not easy to warm whole communities in the field, except through the use of greenhouses—which tend to change many other features such as precipitation patterns. Thus, the effect of temperature is often studied on laboratory populations. In addition, mathematical models are used to determine the likely range alterations of plants and insects in the face of increased global temperatures and changes in precipitation patterns.
CHANGES IN PLANT CHEMISTRY
Plants cGreenhouse Gases, Global Warming, and Insectsommonly respond to elevated CO2 by increasing their rates of photosynthesis. Higher rates of photosynthesis usually result in higher accumulations of carbon-rich carbohydrates. Furthermore, the increased atmospheric CO2 levels mean that stomatal conductance is reduced because plants can get sufficient atmospheric CO2 into their leaves even when their stomates are closed more often. A reduction in stomatal conductance results in greater efficiency of water use by plants, because less water is lost through transpiration. Both these factors have important effects on plant chemistry.
First, increased carbon uptake by plants results in higher plant growth rates, with leaf area index, woody biomass, and below-ground biomass sometimes increased by as much as 25-50%. Despite the increase in plant growth, there is usually no increase in the availability of soil nutrients, particularly nitrogen, and these nutrients must be spread further among the available plant biomass. The usual result is a decrease in total plant nitrogen because nitrogen is diluted over the entire plant. Herbivore growth is most often limited by nitrogen rather than by carbon, so that plants grown in atmospheres of elevated CO2 become poorer quality forage. Plant water content usually affects digestibility, so that the poorer quality diet is partly offset by an increased ease of digestion.
The second major change in plants grown under conditions of elevated CO2, namely, is a change in the ratio of carbon to nitrogen (C:N), as described in the preceding section. This has major implications for the concentration of defensive compounds in the leaves, the so-called secondary chemicals. Carbon-based secondary chemicals often increase and deter insect feeding. The overall effect of increased CO2 on insect herbivores is to decrease plant palatability because of decreases in nitrogen levels and increases in secondary chemicals.
For secondary chemicals, the increases seem to be greatest for soluble phenolic compounds, especially condensed tannins, which are found in a variety of trees, especially oaks. These compounds are known to negatively affect many herbivorous insect species. Yet for other defensive compounds, such as linear furanocoumarins, found in celery, and monoterpenes and sesquiterpenes, found in peppermint, a slight decrease has been noted.
CHANGES TO INSECT HERBIVORE FEEDING
There have been over 75 studies of the performance of insect herbivores of various types under conditions of elevated CO2. The majority of these have been conducted with leaf-chewing insects, especially lepidopteran caterpillars. A commonly reported change is that food consumption increases, between 10 and 20% as the insects struggle to obtain sufficient nitrogen in their diet. The efficiency of food conversion to insect biomass (conversion efficiency) decreases, probably because of the increased concentration of secondary chemicals, such as tannins, which bind digestive enzymes and render them less effective. Thus, it takes insects much longer to develop, and their final weight is often reduced. Early instars seem to be more susceptible than late instars. Of course such changes in diet could, in theory, be partly offset by the increase in digestibility due to the increased water content. However, at least in the studies done so far, the net outcome of elevated CO2 on herbivorous insect digestibility has been negative.
The responses just outlined may vary somewhat according to the feeding guild of insects involved. Thus, chewing insects, which often digest the whole leaf and encounter both reduced nitrogen levels and increased defensive compounds, are particularly susceptible to changes in nitrogen and phenolics. Insects that feed in a different way may be less susceptible. Phloem and xylem feeders in particular may be less affected by CO2 because they feed on plant sap, which is low in defensive compounds. Seed feeders also may be less affected by increased CO2 because these plants try to maintain high levels of nitrogen in their reproductive parts. In cotton, for example, the C:N ratio of cotton balls is unaffected by elevated CO2 and lepidopterans feeding there are unaffected. The concern is that pest insects could be stimulated to feed on these reproductive parts when the quality of the remainder of the plant decreases, which in turn would increase the pest status of some insects.
Of course CO2 has also the direct effect of increasing temperature via the greenhouse effect, which may stimulate feeding activity because of increased metabolic rate in higher temperatures. Over a 20 year period, from 1985 to 2005, the peak date of caterpillar biomass in mixed oak woodland in Holland advanced by 15 days. Studies on the green peach aphid, Myzus persicae, a pest of many crops, suggest that elevated temperature increases aphid population growth rate and thus the likelihood that aphids will become more important pests in the future. In this case, both elevated CO2 and elevated temperature increased aphid densities in experiments. Since, however, very few experiments have examined both CO2 concentration and temperature in factorial experiments, the generality of the aphid results is unknown. It is also possible that the effects of elevated CO2 and elevated temperature could cancel each other out for other insect species, especially leaf chewers.
EFFECTS OF CHANGED PLANT CHEMISTRY ON INSECT DENSITIES AND MORTALITIES
There has been relatively little research into how CO2-mediated changes in plant chemistry affect insect densities and mortalities. This is because most plant-insect work has been done in laboratory conditions, where insects are fed foliage grown in elevated or ambient CO2 and insect weight gains, losses, and digestibility coefficients are measured. To predict the effects of elevated CO2 on insect densities, a population must be established on CO2-treated foliage. However, in the few cases where insects have been reared from first instars through to pupae and adults, a significant decrease has commonly been found in resultant population sizes. This is usually because nutritionally inadequate foliage kills the immature insects. In some species (e.g., leafminers), we can get a good estimate of host-plant-induced mortality. Here, larvae that die from nutritional inadequacy are entombed with the leaf and can be counted, permitting an accurate assessment of deaths induced by the host plant.
To study the effects of elevated CO2 on the interactions of insect herbivores with their natural enemies, such as predators and parasites, whole communities containing insect herbivores and their predators, parasites, and diseases are exposed to elevated CO2. Such community-wide exposure has proved to be very difficult to achieve in the laboratory. Only where whole communities of plants and insects are exposed to elevated CO2 in the field is it possible to fully address the effects of CO2 on natural enemies. Experiments like this are very costly to do because of the huge quantities of CO2 needed to arrive at a large enough increase in CO2 under field conditions. However, it is widely thought that the net result of increased plant consumption and slower growth by herbivorous insects in elevated CO2 is likely to result in increased exposure to natural enemies. For example, consumption of additional foliage increases the probability of ingestion of viruses or pathogenic bacteria, such as Bacillus thuringiensis, which can cause death. Once again, leaf-mining insects are a valuable study organism with which to examine the effects of elevated CO2 on attack rate by natural enemies. This is because the leafmines themselves leave a permanent record of the fate of the insect inside. Parasite larvae can often be found within a mine, or the emerging adult parasitoids leave characteristic small shotgunlike holes in the upper mine surface. A recent study by the author, at Kennedy Space Center, was able to examine attack rates of leafminers by parasitic Hymenoptera in field chambers under conditions of ambient and elevated CO2 . The open-topped chambers contained the full complement of herbivores and their natural enemies on naturally occurring oak vegetation (Fig. 2 ). Leafminer density was reduced inside the chambers, and leaf nitrogen content was reduced. The leafminers died more frequently inside the mines in elevated CO2 and the mine area was bigger, indicating that larval leafminers had to eat more. Attack rate by natural enemies, particularly parasitoids, was significantly increased inside the chambers in which CO2 was elevated. Perhaps the leafminers had created bigger, more obvious mines. Alternatively, their developmental time might have been slower in elevated CO2, exposing them to natural enemies for a longer time, or they might have been physiologically less well able to resist attack.
FIGURE 2 Open-topped chamber at Kennedy Space Center, Florida used to elevate atmosphere CO2.
In other systems, aphids known to produce alarm pheromones show a reduced capacity to do so under elevated CO2. Once again, the result is an increased susceptibility to natural enemy attack.
Finally, increased global temperatures are also likely to increase parasite and predator abundance as a result of increased population growth rates. This in turn could also lead to higher insect herbivore mortalities.
EFFECTS OF TEMPERATURE CHANGES ON INSECT DISTRIBUTION PATTERNS
Greenhouse gases are likely to change insect distribution patterns both directly, via increases in temperature and rainfall, and indirectly, via changes in the distribution of host plants. Research on a sample of 35 nonmigratory European butterflies showed that 63% had ranges that shifted to the north by 35-240 km during the 20th century, while only 3% shifted to the south. Thus for many insects, global warming has already changed range boundaries. The data appear to be robust because for most of these species, northward shifts have been shown in more than one country. Furthermore, the data appear to be robust across families, with many members of the Lycaenidae, Nymphalinae, Satyrinae, and Hesperiidae showing such range shifts. The northward shifts of the butterflies are of the same magnitude as the shift in climatic isotherms, which have moved about 120 km north as Europe has warmed by about 0.8°C. Since then, northerly range shifts have been shown for European grasshoppers, longhorn beetles, lacewings, carabid beetles, aquatic insects, millipedes, wood-lice, spiders, soldier beetles, and dragonflies.
Changes in rainfall, likely to have at least as big an impact as rising temperatures, have not been much studied. Global rainfall patterns clearly will change as a result of changes in global temperature, with many coastal areas becoming wetter and many interior continental areas becoming drier. This set of changes will affect the distribution of host plants and the insects that live on them. In addition, rainfall changes can directly affect the hatching of immatures from eggs laid in the soil, including eggs of many species of locust. Increased soil moisture increases the likelihood of locust outbreaks because it increases hatching and stimulates growth of host plants on which the locusts feed. The threat of locust plagues in new areas of the globe is therefore very real.
Margaret Davis, a paleobotanist from the University of Minnesota, showed that in the event of a CO2 doubling, beech trees, presently distributed throughout the eastern United States and southeastern Canada, would die back in all areas except northern Maine, northern New Brunswick, and southern Quebec. Of course favorable new locations would develop in central Quebec, but the trees would take a long time to colonize such areas. Presumably the animals that feed on beech trees, including insect herbivores, would suffer a severe range contraction too, though this has not yet been studied.
EFFECT OF GREENHOUSE GASES ON SOIL INSECTS
It is doubtful that soil-inhabiting insects will respond directly to increased levels of CO2 because of existing high concentrations in the soil. However, there are many likely indirect effects of CO2 on soil insects. Light interception by a larger canopy may lower soil temperature and moisture. The most important change, though, is likely to be increased litterfall. Soil organic matter is likely to accumulate, rendering grasslands and forests net sinks of carbon under conditions of elevated CO2 . However, before senescence, most leaf nitrogen is reabsorbed by the plant, so that whereas living leaves in elevated CO2 generally have a lower nitrogen content than leaves in ambient CO2 conditions, litter quality remains unchanged. However, the increased volume of litter is likely to increase the number of litter-decomposing insects there.
In addition, increased root production may benefit root-feeding insects. Total numbers of Collembola per kilogram of soil have been shown to be significantly higher in experimental laboratory-based mesocosms where CO2 levels were 60% above ambient. Species composition of Collembola also changed. Part of these increases in Collembola may be due to changes in abundance of mycorrhizal and nonmycorrhizal fungi on which they feed.
AQUATIC COMMUNITIES
Aquatic insect communities are unlikely to be directly influenced by increased CO2 as much as terrestrial systems are. However, the increased litterfall associated with forest productivity is likely to increase allochthonous (i.e., leaf fall from riparian zones) litter input into forest streams and lakes. Such increased litter input is likely to increase stream insect populations. Litter quality itself, because it does not generally differ between ambient and elevated CO2 treatments, is unlikely to affect aquatic decomposer communities. This has been verified by adding litter from ambient and elevated CO2 to laboratory microcosms (simulated treeholes) and examining effects on eastern treehole mosquitoes, Aedes triseriatus. No differences in mosquito development time or survival were found. However, the elevated water temperatures and precipitation may increase the abundance of disease vectors such as mosquitoes. On the other hand, some cold water species may be reduced in abundance.
ELEVATED CO2 AND DISEASE VECTORS
One of the main concerns voiced about global warming is that the delicate balance between diseases, their vectors, and humans might be upset as tropical climates that are so hospitable to spawning and spreading diseases move poleward. The spread of infectious diseases is controlled by the range of their vectors—mosquitoes and other insects. Increases in temperatures mean increases in the activity and ranges of these vectors.
Data on recent trends support this observation. An increase of 1°C in the average temperature in Rwanda in 1987 was accompanied by a 337% rise in the incidence of malaria that year as mosquitoes moved into mountainous areas they had not previously inhabited. Also, Aedes aegypti, a mosquito that carries dengue and yellow fever, has extended its range high into the mountain areas of such diverse areas as Colombia, India, and Kenya. Although global warming is expected to deliver its most deadly punch in the tropical areas of the world, where over 500-million people are affected (and 2.7 million die), the United States is not immune. A computer model by a Dutch public health team proposed that an average global temperature increase of 3°C in the next century could result in 50-80 million new cases of malaria each year. In the United States, public health facilities are likely to keep new incidences of disease in humans to a minimum, because of vaccinations. But disease outbreak in wildlife, which is not vaccinated, could be more severe.
