Review
How do aphids respond to elevated CO2?

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Abstract

The performance of herbivore insects is determined directly by the quality of host plants. Elevated CO2 induced a decline in foliar nitrogen, which reduced the growth of chewing insects. Phloem-sucking insects (i.e. aphid), however, had species-specific responses to elevated CO2 and were the only feeding guild to respond positively to elevated CO2. Although many studies attempt to illuminate the interaction between aphids and plants under elevated CO2, few studies can explain why some aphids are more successful than other chewing insects in elevated CO2. Elevated CO2 leads to a re-allocation of the carbon and nitrogen resources in plant tissue, which increases the thickness of the microscopic structures of leaves, reduces amino acids content of leaf phloem sap and increases the secondary metabolites. Considering the complexity of aphid–plant interactions, it is difficult and unreasonable to predict the general response of aphids to elevated CO2 using a single plant component. Instead, it is more likely that aphids are able to overcome the disadvantages of the indirect effects of elevated CO2 by reducing developmental times and increasing fecundity under elevated CO2 conditions. Our results provide several clues to why some aphids are successful in elevated CO2 conditions. We review recent studies of the effects of elevated CO2 on aphids and discuss the effects of elevated CO2 on aphid performance on crops using cotton and cereal aphids as examples.

Introduction

Owing to human activity and to the increased use of fossil fuels, global atmospheric CO2 concentration has increased from 280 ppm in pre-industrial times to 379 ppm in 2010, and is predicted to at least double by the end of this century (IPCC, 2007). Increases in atmospheric CO2 accelerates photosynthetic rate, stimulates plant growth, and increases the carbon:nitrogen ratio of most plant species (Barbehenn et al., 2004, Reich et al., 2006). In addition, elevated CO2 can affect plant quality by inducing changes in allocation of carbon and nitrogen to primary and secondary metabolites, which affects tritrophic interactions (Hartley et al., 2000, Sun et al., 2010b). There is widespread evidence that elevated CO2 can promote plant growth, with consequent reallocation of resources and dilution of foliar nitrogen, which modify both consumption rates and fitness of herbivores (Yin et al., 2009, Sun et al., 2010a).

Generally, the elevated CO2 treatment used in global change biology experiments was one and a half or two times the ambient CO2 concentration (~ 600–750 ppm). Compared with weak direct effects, the impact of elevated CO2 on herbivores acts mainly through altering host plant composition, and are called “indirect effects” (Coviella and Trumble, 1999, Hunter, 2001). Typically, chewing insects develop more slowly, suffer greater mortality and have higher consumption rates when fed foliage grown under elevated CO2 conditions (Chen et al., 2005b, Wu et al., 2006). In contrast, phloem sap-suckers (e.g., aphids) have a more complex response to elevated CO2 (Newman, 2003). Like many homopteran insects, aphids feed exclusively on the phloem sap and are very sensitive to changes in quantity/quality of plants resulting from elevated CO2 (Pritchard et al., 2007). Thus, comprehensive understanding of aphid from ecological and physiological view may explain how elevated CO2 modifies the interaction between plant and aphid.

Section snippets

Growth and development

Aphid responses to elevated CO2 are frequently “species-specific” and can be negative, positive or neutral (Bezemer and Jones, 1998, Hughes et al., 2001). Bezemer et al. (1999) proposed several reasons for variability in aphid species responses to elevated CO2 and suggested that differential feeding behavior between generalist and specialist aphid species may result in variation in responses. Additionally, the same aphid species exhibits various responses to elevated CO2 on different host

Phenotype and reproduction

Aphids can switch between apterous and alate morphs with environmental change to increase fitness. Alate morphs developed slower and produced significantly fewer nymphs than apterous morphs (Liu and Yue, 2001). Alate aphids (Aphis fabae) may also reduce their weight by fasting before take-off, which results in aerodynamic benefits (Powell and Hardie, 2002). Zou et al. (1997) indicated that the apterous:alate ratios of aphids are related to the content of some amino acids, foliar nitrogen, and

Feeding behavior

Once aphids arrive at a new plant, they probe the plant to determine if it is acceptable. Sucrose is an attractant and an important cue in sieve element location. Elevated CO2 increases sucrose in plant tissues, which may explain why cereal aphids prefer wheat plants grown in elevated CO2 (Awmack et al., 1996).

Aphids face many structural barriers before they can feed successfully from a sieve element elevated CO2 may affect these structures and modify the feeding behavior of aphids. Elevated CO2

Nutrient effects

The nutritional quality of phloem sap may be an important limiting resource for the growth, development and performance of aphid populations (Bezemer and Jones, 1998). Aphids, however, feed on different plants and appear to have species-specific requirements for amino acids (Wilkinson and Douglas, 2003). Generally, only around 20% (mol%) relative concentration of the essential amino acids compared to concentration of all amino acids were found in phloem sap, with a range from 15% to 48%, while

Interspecific interaction

Because changes in plant quantity/quality can alter the interspecific interactions among insect herbivores, elevated CO2 is likely to change these interactions (Inbar et al., 1995, Gonzáles et al., 2002). Aphid species often respond differently to the same host plants grown under elevated vs. ambient CO2, and this may change the outcome of interspecific competition (Harrington et al., 1999). For example, Stacey and Fellowes (2002) found a significantly lower ratio of Myzus persicae :

Response to plant defenses

As predicted by the Carbon Nutrient Balance (CNB) hypothesis, excess carbon accumulating in plant tissues due to elevated CO2 is probably allocated to more carbon-based secondary metabolites, such as phenolics, condensed tannins, and terpenoids (Sun et al., 2009a). Although these responses are species-specific in plants, aphids may enhance the activities of superoxide dismutase and catalase in elevated CO2 environments. Microarrays were used to examine Arabidopsis responding to elevated CO2. It

Chemical signals

The aphid alarm pheromones warn aphids of attack by natural enemies (Nault et al., 1973). Aphids perceiving the alarm pheromone increase production of alate offspring and reduce their foraging rate, which increase their ability to disperse into enemy-free space thereby reducing exposure to predators (Montgomery and Nault, 1977, Kunert et al., 2005). Previous studies suggest that, under elevated CO2, parasitoids and predators are more abundant or effective (Percy et al., 2002, Chen et al., 2005a

Conclusions

A general prediction of the response of aphids to elevated CO2 is currently impossible. Contrary to other insect guilds, some aphid species exhibit higher fitness under elevated CO2 conditions. Understanding the unique pattern of how aphids interact with their host plant can elucidate the species-specific responses of aphids to elevated CO2. Newman (2003) constructed a mathematic model and concluded that aphid populations tend to be larger under elevated CO2 if soil N levels are high, that the

Acknowledgments

This project was supported by the “National Basic Research Program of China” (973 Program) (No. 2006CB102006), the National Nature Science Fund of China (No. 30770382, 31000854 and 30621003) and National Key Technology R&D Program (2008BADA5B01-04).

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