Effects of elevated atmospheric carbon dioxide on insect–plant interactions

The rarefied atmosphere of US politics has been heating up recently. During March, President George W. Bush contributed significantly to the accumulation of hot air over Washington and elsewhere by announcing two major policy shifts related to the emission of CO2 into the atmosphere. First, President Bush reneged on a campaign pledge to regulate carbon dioxide emissions from U.S. power plants. Soon afterwards, his administration explicitly opposed the Kyoto Protocol, the international agreement setting country-by-country limits on emissions of greenhouse gases. These two policy positions ensure that little will change in the near future to reduce the amounts of CO2 entering the atmosphere from US sources. In short, it is a great time to be in the CO2 business. Entomologists have recognized for some time that elevated concentrations of atmospheric CO2 may influence the distribution, abundance and performance of insects that feed on plants (Lincoln et al., 1984, 1986; Fajer et al., 1989). Major questions remain, however, on the relative importance of changes in weather, changes in plant quality and changes in predation pressure on the dynamics of insect herbivore populations under conditions of elevated CO2. If you grow crops or trees for a living, these questions boil down to one simple concern; will yields increase or decrease as CO2 levels continue to rise? The problem is that we do not really know yet, and it is going to cost significant sums of money to find out. There are too many interacting variables to make simple predictions about changes in pest damage to forestry and agricultural commodities. CO2–mediated changes in temperature or precipitation may affect insects directly and may influence the geographical ranges of agricultural and natural plant communities (Cannon, 1998). The predators, parasites and pathogens that maintain some level of control over insect populations may also be affected by global climate change or changes in plant phenotype (Stiling et al., 1999). Changes in the nutritional and defensive characteristics of host plants may drive changes in levels of insect damage to plants (Bezemer & Jones, 1998) and all of these ecological effects may interact with other sources of environmental variation including drought, nutrient availability and light (Arnone et al., 1995; Roth et al., 1997; Haettenschwiler & Schafellner, 1999; McDonald et al., 1999). In the longer term, elevated CO2 may influence the fundamental ecosystem properties upon which all plant productivity depends (Ball & Drake, 1997; Jones et al., 1998; Kampichler et al., 1998; Kandeler et al., 1998; Hungate et al., 1999; Strand et al., 1999). While presidents and policy makers play Russian roulette with the climate, ecologists and entomologists are exploring with ever-increasing accuracy and complexity the potential ramifications of elevated CO2 for plant–herbivore interactions. Without long-term studies of the crucial variables, we will simply be unprepared for the enriched CO2 atmosphere that is developing (Coviella & Trumble, 1999). Atmospheric CO2 concentrations have already risen by about 25% since the industrial revolution and are expected to increase from current ambient levels of 350–360 p.p.m. (or µL/L) to around 600 p.p.m. by the end of the century (Houghton et al., 1995). All of the potential consequences of elevated CO2 concentrations are too great to cover in detail here. In this paper, I focus upon what we know about changes in plant quality under elevated CO2 and how changing food quality might interact with other ecological variables to alter the performance and abundance of insects on plants. As the principle source of carbon for photosynthesis, it should be no surprise that changes in concentrations of CO2 have marked effects upon the phenotype of plants (Lincoln, 1993; Ceulemans & Mousseau, 1994; Curtis & Wang, 1998). For example, elevated CO2 generally results in increased rates of photosynthesis (Drake et al., 1997; Norby et al., 1999), increased rates of growth (Saxe et al., 1998) and increased biomass (Leadley et al., 1999; Owensby et al., 1999). Assuming no concurrent changes in nutrient availability, the accumulation of biomass under elevated CO2 dilutes concentrations of nitrogen in tissues by 15–25% (Lincoln et al., 1993; Lindroth et al., 1995), thereby increasing C : N ratios (Ceulemans & Mousseau, 1994; Wilsey, 1996; Hughes & Bazzaz, 1997) and the allocation of carbon to some carbon-rich secondary metabolites (Lindroth et al., 1995; Agrell et al., 2000). Elevated concentrations of CO2 may sometimes (Agrell et al., 2000) but not always (Thompson & Drake, 1994; Bezemer & Jones, 1998) decrease the water content of foliage and increase rates of leaf abscission and plant senescence (Paez et al., 1983; Houpis et al., 1988; Baxter et al., 1994; Sicher & Bunce, 1997). Of course, not all plant species respond identically to elevated concentrations of CO2 (Lindroth et al., 1993). For example, elevated CO2 results in reduced foliar nitrogen levels and increased condensed tannin levels in paper birch but not in white pine (Roth & Lindroth, 1994). In further studies with paper birch, quaking aspen and sugar maple (Roth et al., 1998; Agrell et al., 2000), all species show increases in foliar concentrations of condensed tannins under elevated CO2. However, the foliage of quaking aspen also expresses higher concentrations of phenolic glycosides, and sugar maple is the only species to show elevated foliar concentrations of hydrolysable tannins. In a study contrasting a C3 sedge with a C4 grass in marsh habitat, Thompson & Drake (1994) reported CO2-mediated declines in foliar nitrogen only in the sedge. The grass, in contrast, exhibited increases in foliar water concentrations and concomitant increases in fungal infection. Despite the predictions of the carbon-nutrient balance hypothesis (Chapin, 1980; Bryant et al., 1983) that all carbon-rich secondary metabolites should increase under elevated CO2, this appears not to be the case. For example, foliar concentrations of the iridoid glycosides in Plantago lanceolata are unaffected under CO2 enrichment (Fajer et al., 1989, 1991). Likewise, the volatile terpenoids of peppermint (Lincoln & Couvet, 1989), big sagebrush (Johnson & Lincoln, 1990) and loblolly pine (Williams et al., 1997a) do not vary with experimental increases in CO2. Because nitrogen concentrations in foliage are diluted by the increased C : N ratio of plant tissues under elevated CO2, there is the potential for reduced efficacy of nitrogen-based plant defences. In an interesting twist to this hypothesis, Coviella et al. (2000) reported that transgenic cotton grown under elevated CO2 expressed reduced concentrations of Bt protein. In bioassays with Spodoptera, larval performance increased under elevated CO2 because increased larval consumption in response to low nitrogen levels did not compensate for reductions in Bt protein. Before you dash out and sell your biotech stocks, it is obviously far too early to say that the use of Bt transgenes will be compromised under elevated CO2, but it certainly merits further study. The Bt-lovers amongst us may be gratified to learn that the efficacy of conventional topical applications of Bt may be enhanced under elevated CO2. Experiments suggest that increased consumption by insects to compensate for high C : N ratios results in greater exposure to Bt and higher levels of mortality (Coviella & Trumble, 2000). We are dealing with complex organisms and there will be no perfect generalities for the way that plant phenotype changes under elevated CO2. Nonetheless, in nearly every case examined to date, foliar nitrogen concentrations decline under elevated CO2 and, when present, foliar concentrations of condensed tannins increase (Fajer et al., 1989, 1991; Johnson & Lincoln, 1991; Lincoln et al., 1993; Lindroth et al., 1995). This level of generality is somewhat heartening and allows us to predict that overall decreases in foliar quality should induce at least some insect herbivores to eat more. And that prediction usually holds true. Lower levels of nitrogen and higher C : N ratios in plants under elevated CO2 have generally been associated with compensatory feeding and subsequent increases in levels of damage or defoliation (Lincoln et al., 1984, 1986; Fajer et al., 1989; Lincoln et al., 1993; Lindroth et al., 1993, 1995; Salt et al., 1995; Docherty et al., 1996; Kinney et al., 1997; Williams et al., 1997a). Leaf-chewing insects such as grasshoppers (Johnson & Lincoln, 1990, 1991) and caterpillar larvae (Lindroth et al., 1993, 1995) generally consume more leaf area when they are fed plants that have been grown under elevated CO2. Likewise, the area damaged by leaf-mining insects may also increase (Salt et al., 1995). For example, the area of leaf mines on Quercus myrtifolia increased by over 25% under elevated CO2, apparently because nitrogen concentrations fell by over 11% (Stiling et al., unpublished data). However, this is where the first complicating factor arises: simply because per capita consumption of foliage by insects increases under elevated CO2, it does not mean that plants suffer more damage overall. Two additional effects that mediate the ultimate level of damage that plants receive are CO2-induced increases in plant biomass and changes in insect density. It is well established that many plants accumulate more biomass under elevated CO2 (Leadley et al., 1999; Owensby et al., 1999) and that such direct effects of CO2 on plant growth can more than compensate for increases in defoliation (Caulfield & Bunce, 1994). For example, even though per capita rates of consumption by insects on Q. myrtifolia increase with CO2 enrichment, the proportion of leaves damaged by mining and chewing insects actually declines (Stiling et al., unpublished data). The leaf area index on Q. myrtifolia increases by 26% under elevated CO2 but this ignores the impact of reductions in damaged leaf area. Calculations suggest that undamaged leaf area actually increases by 38% when effects on insects are considered. Similarly, leaf area increases of 1.6-fold on milkweed under elevated CO2 jump to 3.6-fold increases in undamaged leaf area when the effects on herbivorous thrips are accounted for (Hughes & Bazzaz, 1997). Ultimately, the effects of increases in atmospheric CO2 on damage by insect pests will depend upon changes in insect performance at the individual and population levels. The ability of insects to compensate for CO2-mediated reductions in foliage quality is key to understanding long-term effects on herbivore population dynamics and the injury that will be inflicted upon hosts of economic importance. If eating more allows insects to compensate fully, then defoliation levels will rise while insect fitness remains constant. The question then becomes whether CO2-mediated increases in plant productivity are sufficient to offset increases in defoliation levels and which effect is more important to the part of the crop that is harvested for human use. Some insects can certainly compensate well when foliage quality declines. For example, red-headed pine sawfly larvae increase nitrogen utilization efficiency in response to CO2-mediated declines in foliar nitrogen in loblolly pine (Williams et al., 1994). The result is that their rates of nitrogen accumulation remain unchanged. Potential mechanisms by which insect herbivores may compensate for CO2-mediated changes in plant quality are diverse. For example, the activity of detoxification enzymes may be stimulated by increased concentrations of secondary metabolites in foliage (Lindroth et al., 1993). The good news, if you grow plants for a living, is that most insects appear to be unable to compensate fully for CO2-mediated reductions in plant quality. For example, buckeye butterflies on Plantago lanceolata exhibit both higher rates of mortality and increased development time when fed on plants grown under elevated CO2 (Fager et al., 1989; Fajer et al., 1991). Higher rates of insect mortality have been associated with nutritional deficiency that results from reduced foliar nitrogen concentrations under elevated CO2 (Brooks & Whittaker, 1999; Stiling et al., 1999). However, direct effects of changes in plant quality on insect performance are not always dramatic. For example, Lindroth et al. (1995) explored the performance of three species of saturniid moths feeding on paper birch under elevated CO2. Birch leaves were lower in nitrogen (23%), higher in condensed tannin (two-fold increase) and foliar C : N ratios increased from 12.7 to 28.1. Despite these significant reductions in foliage quality, survival of first-instar larvae declined only marginally, while fourth-instar larvae exhibited moderate increases in rates of consumption and decreases in rates of growth, development and food processing efficiency. Brooks & Whittaker (1998, 1999) have studied multiple generations of insects reared on plants under elevated CO2. In their first experiment (Brooks & Whittaker, 1998), Gastrophysa leaf beetles grown on Rumex plants for three consecutive generations exhibited relatively minor effects of elevated CO2 on performance, despite measurable declines in indices of foliage quality. Fecundity and egg size were reduced by the end of the second generation, which led to fewer, smaller larvae in the third generation. In the second study (Brooks & Whittaker, 1999), they reported reductions in the survival of nymphal spittlebugs in two sequential generations under elevated CO2. There were also declines in the rate of development in consecutive years. Such multigenerational studies are crucial if we are to develop any kind of realistic predictions of long-term population dynamics (Williams et al., 1997a). Perhaps more dramatic effects upon insect performance will be mediated by the third trophic level. Given that rates of insect growth also seem to decline under elevated CO2 (Fajer et al., 1989; Lindroth et al., 1995; Smith & Jones, 1998), we might expect that the risk of mortality from natural enemies will However, two studies have to for greater mortality by natural enemies under elevated CO2 (Roth & Lindroth, 1995; Bezemer et al., 1998). For example, effects of by on the performance of larvae do not ambient and elevated CO2 (Roth & Lindroth, 1995). Nonetheless, studies have that rates of increase under elevated CO2 (Stiling et al., 1999; Stiling et al., concentrations in the foliage of two Quercus myrtifolia and Q. decline under elevated CO2 and of leaf-mining insects are lower because of the effects of reduced foliage quality and increased rates of by from plant effects increases by and from by over under elevated CO2. We have to study the effects of elevated CO2 on the efficacy of natural enemies and to be of CO2 enrichment on have been foliar phenolic and of are well established & & 1993). However, in at least one study (Lindroth et al., of larvae to unaffected by CO2-mediated changes in foliar upon and pathogens under conditions appear to be a for future If declines in foliar nitrogen and increases in foliar C : N ratios are generally of plants to elevated concentrations of CO2, there to be in the of levels of consumption by insects usually rise under elevated CO2, additional effects upon performance appear to be somewhat For example, reductions in performance on aspen are associated with CO2-induced increases in phenolic glycosides et al., 1999). nutrient and secondary of birch and maple are also affected by CO2, there are no changes in In other CO2-mediated effects on insect herbivores will depend both on the species of plant and the species of insect under study (Lindroth et al., 1995; et al., 1996; Coviella & Trumble, 1999). In with white marked Agrell et al. (2000) have that it is to host plants upon their effects on insects under elevated CO2. on larvae were most when fed upon quaking by paper birch, and least on sugar effects of elevated CO2 may vary as both leaves and herbivores increases in foliar C : N ratios more as leaves effects on are more in early on larvae appear to be to compensate for reductions in foliar quality than are larvae (Williams et al., 1998). species such as loblolly elevated concentrations of CO2 can interact with natural in foliage quality to influence the of leaf for insect larvae (Williams et al., not all insects respond to the changes in plant phenotype that are mediated by elevated concentrations of CO2. least some insects exhibit increases in performance when with plants grown under elevated CO2 et al., 1997; Bezemer & Jones, 1998). As however, there appears to be variation in the of insects to changes in plant quality. For example, the of the to elevated CO2 on two plant species et al., 1997). the rate of increases by rates of development are In contrast, on exhibit rates of development and no change in are under elevated CO2 on both host but the mechanisms this to is that we are a way from to predict changes that may in the population dynamics of important crop pests under elevated concentrations of atmospheric CO2. studies under conditions were to the of plant phenotype to elevated CO2 and their potential effects on insect However, most studies in which plants are not by nutrient availability or where communities are to two or three interacting where of herbivores are and where in the are (Lincoln et al., 1993; et al., 1995). In other they are of any ecological In the effects of elevated CO2 on plant and subsequent insect will be mediated by the availability of to plants such as water (Roth et al., light et al., 1999) and (Arnone et al., 1995; Haettenschwiler & Schafellner, 1999) and by and effects of light and CO2 on growth and secondary have been studied by McDonald et al. in insect performance on aspen grown under high light and elevated CO2 were dramatic. were reared on foliage for the larval survival fell by with concomitant decreases in growth rate and in performance on aspen were associated with both and increases in phenolic The key of these studies is the to which changes in plants under elevated CO2, and the subsequent effects on insect depend upon the availability of light et al., 1999; Agrell et al., 2000). This that and will influence the response of and their insect to elevated CO2. availability is also to affect plant and insect to atmospheric change (Arnone et al., 1995). the nutrient is to limits on the in plant biomass that generally result from elevated CO2 (Johnson & Lincoln, 1991; et al., 1998). Given natural variation in nutrient availability and by and increasing levels of nitrogen from we should be of potential elevated CO2 and nutrient nitrogen may the effects of elevated CO2 on insect In one experimental Haettenschwiler & larvae of the to trees grown under three levels of nitrogen and three levels of CO2. The effects of the on plant phenotype were generally reductions in condensed tannins and and increases in sugar and nitrogen concentrations in the direct of to elevated CO2. As a nitrogen to in the effects of elevated CO2 on In contrast, Kinney et al. relatively nutrient availability and CO2 in their studies of performance on and of the were than In some the consequences of nitrogen may of elevated CO2. For example, et al. have that the defensive and nutritional phenotype of does not change of growth under elevated CO2. In contrast, nitrogen results in decreases in foliar C : N ratio and increases in other studies (Lindroth et al., 1995; Haettenschwiler & Schafellner, 1999; Agrell et al., 2000), elevated CO2 nitrogen the foliar of with changes in the the performance of larvae increased by nitrogen and unaffected by elevated CO2. of elevated levels of atmospheric CO2 is the increase in global studies that effects of plants and elevated on insect performance are In one such study et al., 1998), a increase in temperature reduced the nutritional quality of leaves by foliar nitrogen concentrations and increasing foliar concentrations of condensed In other elevated temperature in changes in plants that were to mediated by elevated CO2. In with CO2-mediated reductions in the quality of and secondary leaf the elevated associated with global may significantly reduce the quality of plant food for insect However, complex plant quality, insect performance and make predictions of pest in future global (Cannon, 1998). For example, the reduced rates of insect growth that have been under elevated CO2 may as temperature increases in response to levels of atmospheric CO2 (Fajer et al., 1991). The We under conditions to have any of the effects of CO2 and other ecological variables on the insect pests of crops and Given this can we make any about the effects of elevated CO2 on insects that feed on While there are always going to be effects that are and et al., 1996; Kinney et al., 1997; Roth et al., 1998; Coviella & Trumble, 1999; Agrell et al., 2000), we should not from when (Fajer & 1993). For example, Bezemer & Jones from plant–herbivore and some First, they the decreases in foliar nitrogen and increases in and secondary metabolites reported in many individual consumption by herbivores related to changes in nitrogen and levels. no were CO2-mediated herbivore on and plant insects generally increased their consumption of foliage under elevated CO2 to compensate for reduced nutritional quality and no effects upon leaf-mining insects only compensate by increased consumption and their did and insects to elevated CO2, with increases in population size and decreases in development Of course, there will be to these but they a from which to develop for future we more studies of a of in under conditions (Saxe et al., 1998). There remain fundamental in understanding of plant and insect to elevated concentrations of atmospheric CO2. For example, we know little about the of herbivores to increases in atmospheric CO2. the of studies CO2-mediated changes in the dynamics of communities is increasing (Ball & Drake, 1997; Jones et al., 1998; Kampichler et al., 1998; Kandeler et al., 1998), effects on insects that feed on plant are In at least some elevated CO2 results in increases in growth et al., and increases in of plants et al., 1999). However, the quality of these for insects that feed are generally Likewise, we know about the effects of CO2-mediated changes in plant quality on of water temperature many insects in depend upon as sources of carbon to drive food Changes in quality as the result of elevated CO2 have the potential to influence and availability in However, in the one study I find to date, from and birch grown under elevated CO2 effects on growth and as did from ambient atmospheric conditions et al., 1999). We more on CO2-mediated changes in quality and subsequent effects on food In to we do not really know whether the studies of and that have the the that we should expect from The increasing availability of and carbon enrichment should us with the ability to long-term on plants and the insects that they studies that insects with communities of and under environmental conditions may be more to future effects of elevated CO2 on insect and abundance (Fajer & 1993; Stiling et al., 1999). I have already how little we know about the of natural enemies to CO2 and studies have potential to the of complex that are in both natural and of natural enemies (Stiling et al., 1999), & Lincoln, and complex plant communities (Arnone et al., 1995) on insect and performance be in the ecological of the Perhaps most important of we long-term studies that multiple generations of both insects and plants. Such studies are for such as effects on quality and by herbivore species to a atmosphere. studies under conditions of course, they a of the cost that big is to to the will their to levels of CO2 I to the of and the of for on the ecological consequences of elevated concentrations of atmospheric CO2.