Docherty et al. (1997) grew beech and sycamore saplings in glasshouses maintained at atmospheric CO2 concentrations of 350 and 600 ppm, while groups of three sap-feeding aphid species were allowed to feed on the saplings.  Overall, the elevated CO2 had few significant effects on aphid feeding and performance.  There was, however, a non-significant tendency for elevated CO2 to reduce the individual weights and population sizes of the aphids, suggesting that future increases in the air's CO2 content might reduce aphid feeding pressures on beech and sycamore saplings, and possibly other plants as well.

Whittaker (1999) reviewed the scientific literature dealing with population responses of herbivorous insects to atmospheric CO2 enrichment, concentrating on papers resulting from relatively long-term studies.  Based on all pertinent research reports available at that time, the only herbivorous insects that exhibited population increases in response to elevated CO2 exposure were those classified as phloem feeders, specifically, aphids.  Although this finding appeared to tip the scales in favor of aphids over plants, additional studies would complicate the issue and swing the pendulum back the other way.

Newman et al. (1999) grew tall fescue plants for two weeks in open-top chambers maintained at atmospheric CO2 concentrations of 350 and 700 ppm before inoculating them with aphids (Rhopalosiphum padi).  After nine additional weeks of differential CO2 exposure, the plants were harvested and their associated aphids counted.  Although elevated CO2 increased plant dry matter production by 37%, this phenomenon did not result in similar increases in aphid colonization.  In fact, the plants grown in air of elevated CO2 concentration contained far fewer aphids than the plants grown in ambient air.

Percy et al. (2002) grew the most widely distributed tree species in all of North America - trembling aspen - in twelve 30-m-diameter FACE rings in air maintained at (1) ambient CO2 and O3 concentrations, (2) ambient O3 and elevated CO2 (560 ppm during daylight hours), (3) ambient CO2 and elevated O3 (46.4-55.5 ppb during daylight hours), and (4) elevated CO2 and O3 over each growing season from 1998 through 2001.  Throughout their experiment they assessed a number of the young trees' growth characteristics, as well as the responses of the sap-feeding aphid Chaitophorus stevensis, which they say "infests aspen throughout its range."  This experiment revealed that, by itself, elevated CO2 did not affect aphid abundance; but it increased the densities of natural enemies of the aphids, which over the long term would tend to reduce aphid numbers.  Also, by itself, elevated O3 did not affect aphid abundance, but it had a strong negative effect on natural enemies of aphids, which over the long term would tend to increase aphid numbers.  When both trace gases were applied together, however, elevated CO2 completely counteracted the reduction in the abundance of natural enemies of aphids caused by elevated O3.  Hence, elevated CO2 tended to reduce the negative impact of aphids on trembling aspen in this comprehensive study.

At about the same time, Holopainen (2002) reviewed the scientific literature dealing with this phenomenon, i.e., the joint effects of elevated concentrations of atmospheric O3 and CO2 on aphid-plant interactions.  After compiling the results of 26 pertinent studies, it was found that atmospheric CO2 enrichment increased aphid performance in six studies, decreased it in six studies, and had no significant impact on it in the remaining 14 studies, while similar results were found for aphid-plant interactions in the presence of elevated O3 concentrations.

Newman (2003) reviewed what was known, and not known, about aphid responses to concurrent increases in atmospheric CO2 and air temperature, while also investigating the subject via the aphid population model of Newman et al. (2003).  This literature review and model analysis lead him to conclude that when the air's CO2 concentration and temperature are both elevated, "aphid population dynamics will be more similar to current ambient conditions than expected from the results of experiments studying either factor alone."  And if that sounds ambiguous, it is.  We can only draw the general conclusion, according to Newman, that "insect responses to CO2 are unlikely to all be in the same direction."  Nevertheless, he says that "the lack of a simple common phenomenon does not deny that there is some overriding generality in the responses by the system."  It's just that we did not at that time know what that overriding generality was, which is why experimental work on the subject has continued apace.

Concentrating on thermal effects alone, Ma et al. (2004) conducted detailed experiments on the impacts of high temperature, period of exposure, and developmental stage on the survival of the aphid Metopolophium dirhodum, which they say "is the most abundant of the three cereal aphid species in Germany and central European countries."  This protocol revealed, in their words, that "temperatures over 29°C for 8 hours significantly reduced survival, which decreased generally as the temperature increased."  They also determined that "exposing aphids to 32.5°C for 4 hours or longer significantly reduced survival," and that "mature aphids had a lower tolerance of high temperatures than nymphs."  In light of what they observed, therefore, as well as what a number of other scientists had observed, Ma et al. concluded that "global warming may play a role in the long-term changes in the population abundance of M. dirhodum."  Specifically, they say that "an increase in TX [daily average temperature] of 1°C and MaxT [maximum daily temperature] of 1.3°C during the main period of the aphid population increase would result in a 33% reduction in peak population size," while "an increase in TX of 2°C and MaxT of 2.6°C would result in an early population collapse (74% reduction of population size)."  Consequently, it would appear that a little global warming could greatly decrease aphid infestations of cereal crops grown throughout Germany and Central Europe.

Returning to the subject of joint CO2 and O3 effects on aphids, Awmack et al. (2004) conducted a two-year study at the Aspen FACE site near Rhinelander, Wisconsin, USA, of the individual and combined effects of elevated CO2 (+200 ppm) and O3 (1.5 x ambient) on the performance of Cepegillettea betulaefoliae aphids feeding on paper birch trees in what they call "the first investigation of the long-term effects of elevated CO2 and O3 atmospheres on natural insect herbivore populations."  At the individual scale, they report that "elevated CO2 and O3 did not significantly affect [aphid] growth rates, potential fecundity (embryo number) or offspring quality."  At the population scale, on the other hand, they found that "elevated O3 had a strong positive effect," but that "elevated CO2 did not significantly affect aphid populations."

In comparing their results with those of prior related studies, the three scientists report that "the responses of other aphid species to elevated CO2 or O3 are also complex."  In particular, they note that "tree-feeding aphids show few significant responses to elevated CO2 (Docherty et al., 1997), while crop-feeding species may respond positively (Awmack et al., 1997; Bezemer et al., 1998; Hughes and Bazzaz, 2001; Zhang et al., 2001; Stacey and Fellowes, 2002), negatively (Newman et al., 1999) or not at all (Hughes and Bazzaz, 2001), and the same species may show different responses on different host plant species (Awmack et al., 1997; Bezemer et al., 1999)."  In summarizing their observations, they thus stated that "aphid individual performance did not predict population responses to CO2 and O3," and they concluded that "elevated CO2 and O3 atmospheres are unlikely to affect C. betulaefoliae populations in the presence of natural enemy communities."

In a study of a different aphid (Chaitophorus stevensis) conducted at the same FACE site, Mondor et al. (2004) focused on the subject of pheromones, which they say "are utilized by insects for several purposes, including alarm signaling," and which in the case of phloem-feeding aphids induces high-density groups of them on exposed leaves of trembling aspen trees to disperse and move to areas of lower predation risk.  In this experiment the four treatments were: control (367 ppm CO2, 38 ppb O3), elevated CO2 (537 ppm), elevated O3 (51 ppb), and elevated CO2 and O3 (537 ppm CO2, 51 ppb O3).  Within each treatment, several aspen leaves containing a single aphid colony of 25 ± 2 individuals were treated in one of two different ways: (1) an aphid was prodded lightly on the thorax so as to not produce a visible pheromone droplet, or (2) an aphid was prodded more heavily on the thorax and induced to emit a visible pheromone droplet, after which, in the words of the scientists, "aphids exhibiting any dispersal reactions in response to pheromone emission as well as those exhibiting the most extreme dispersal response, walking down the petiole and off the leaf, were recorded over 5 min."

Mondor et al.'s observations were striking.  They found that the aphids they studied "have diminished escape responses in enriched carbon dioxide environments, while those in enriched ozone have augmented escape responses, to alarm pheromone."  In fact, they report that "0% of adults dispersed from the leaf under elevated CO2, while 100% dispersed under elevated O3," indicating that the effects of elevated CO2 and elevated O3 on aphid response to pheromone alarm signaling are diametrically opposed to each other, with elevated O3 (which is detrimental to vegetation) helping aphids to escape predation and therefore live to do further harm to the leaves they infest, but with elevated CO2 (which is beneficial to vegetation) making it more difficult for aphids to escape predation and thereby providing yet an additional benefit to plant foliage.  Within this context, therefore, ozone may be seen to be doubly bad for plants, while carbon dioxide may be seen to be doubly good.  In addition, Mondor et al. state that this phenomenon may be of broader scope than what is revealed by their specific study, noting that other reports suggest that "parasitoids and predators are more abundant and/or efficacious under elevated CO2 levels (Stiling et al., 1999; Percy et al., 2002), but are negatively affected by elevated O3 (Gate et al., 1995; Percy et al., 2002)."

In another intriguing study, Chen et al. (2004) grew spring wheat from seed to maturity in high-fertility well-watered pots out-of-doors in open-top chambers (OTCs) maintained at atmospheric CO2 concentrations of 370, 550 and 750 ppm.  Approximately two months after seeding, 20 apterous adult aphids (Sitobion avenae) from an adjacent field were placed upon the wheat plants of each of 25 pots in each OTC, while 15 pots were left as controls; and at subsequent 5-day intervals, both apterous and alate aphids were counted.  Then, about one month later, 10 alate morph fourth instar nymphs were introduced onto the plants of each of nine control pots; and for the next two weeks the number of offspring laid on those plants were recorded and removed daily to measure reproductive activity.  Last of all, at the end of the study, the wheat plants were harvested and their various growth responses determined.

Adherence to these protocols revealed that the introduced aphid populations increased after infestation, peaked during the grain-filling stage, and declined a bit as the wheat matured.  On the final day of measurement, aphids in the 550-ppm CO2 treatment were 32% more numerous than those in ambient air, while aphids in the 750-ppm treatment were 50% more numerous.  Alate aphids also produced more offspring on host plants grown in elevated CO2: 13% more in the 550-ppm treatment and 19% more in the 750-ppm treatment.  As for the wheat plants, Chen et al. report that "elevated CO2 generally enhanced plant height, aboveground biomass, ear length, and number of and dry weight of grains per ear, consistent with most other studies."  With respect to aboveground biomass, for example, the 550-ppm treatment displayed an increase of 36%, while the 750-ppm treatment displayed an increase of 50%, in the case of both aphid-infested and non-infested plants.

In commenting on their findings, Chen et al. report that "aphid infestation caused negative effects on all the plant traits measured ... but the negative effects were smaller than the positive effects of elevated CO2 on the plant traits."  Hence, they concluded that "the increased productivity occurring in plants exposed to higher levels of CO2 more than compensate for the increased capacity of the aphids to cause damage."  In this experiment, therefore, we have a situation where both the plant and the insect that feeds on it were simultaneously benefited by the applied increases in atmospheric CO2 concentration.  In other words, the CO2-induced responses resulted in a win-win situation with no loser, as both plant and insect profited.

Last of all, in a study that investigated a number of plant-aphid-predator relationships, Chen et al. (2005) grew transgenic cotton plants for 30 days in well watered and fertilized sand/vermiculite mixtures in pots set in controlled-environment chambers maintained at atmospheric CO2 concentrations of 370, 700 and 1050 ppm.  A subset of aphid-infected plants was additionally supplied with predatory ladybugs, while three generations of cotton aphids (Aphis gossypii) were subsequently allowed to feed on some of the plants.  Based on measurements made throughout this complex set of operations, Chen et al. found that (1) "plant height, biomass, leaf area, and carbon:nitrogen ratios were significantly higher in plants exposed to elevated CO2 levels," (2) "more dry matter and fat content and less soluble protein were found in A. gossypii in elevated CO2," (3) "cotton aphid fecundity significantly increased ... through successive generations reared on plants grown under elevated CO2," (4) "significantly higher mean relative growth rates were observed in lady beetle larvae under elevated CO2," and (5) "the larval and pupal durations of the lady beetle were significantly shorter and [their] consumption rates increased when fed A. gossypii from elevated CO2 treatments."  In commenting on the significance of their findings, Chen et al. say their study "provides the first empirical evidence that changes in prey quality mediated by elevated CO2 can alter the prey preference of their natural enemies," and in this particular case, they found that this phenomenon could "enhance the biological control of aphids by lady beetle."

In considering the totality of these many experimental findings, it would appear that the ongoing rise in the air's CO2 content will likely not have a major impact, one way or the other, on aphid-plant interactions, although the scales do appear to be slightly tipped in favor of plants over aphids.  Yet a third possibility is that both plants and aphids will be benefited by atmospheric CO2 enrichment, but with plants benefiting more.

References
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