Elevated carbon dioxide concentrations indirectly affect plant fitness by altering plant tolerance to herbivory

Abstract

Global environmental changes, such as rising atmospheric CO(2) concentrations, have a wide range of direct effects on plant physiology, growth, and fecundity. These environmental changes also can affect plants indirectly by altering interactions with other species. Therefore, the effects of global changes on a particular species may depend on the presence and abundance of other community members. We experimentally manipulated atmospheric CO(2) concentration and amounts of herbivore damage (natural insect folivory and clipping to simulate browsing) to examine: (1) how herbivores mediate the effects of elevated CO(2) (eCO(2)) on the growth and fitness of Arabidopsis thaliana; and (2) how predicted changes in CO(2) concentration affect plant resistance to herbivores, which influences the amount of damage plants receive, and plant tolerance of herbivory, or the fitness consequences of damage. We found no evidence that CO(2) altered resistance, but plants grown in eCO(2) were less tolerant of herbivory-clipping reduced aboveground biomass and fruit production by 13 and 22%, respectively, when plants were reared under eCO(2), but plants fully compensated for clipping in ambient CO(2) (aCO(2)) environments. Costs of tolerance in the form of reduced fitness of undamaged plants were detected in eCO(2) but not aCO(2) environments. Increased costs could reduce selection on tolerance in eCO(2) environments, potentially resulting in even larger fitness effects of clipping in predicted future eCO(2) conditions. Thus, environmental perturbations can indirectly affect both the ecology and evolution of plant populations by altering both the intensity of species interactions as well as the fitness consequences of those interactions.

Ontogenetic changes in tolerance to herbivory in Arabidopsis

“…At first glance, increased leaf biomass should contribute to tolerance through increased assimilation. However, Arabidopsis plants grown under elevated CO 2 (purportedly having an increased C assimilation) were recently shown to be less tolerant than those grown at ambient CO 2 (Lau and Tiffin 2009), thus indicating that the timing of increased assimilation with respect to ontogeny is crucial for tolerance. Similarly, stems may contribute to tolerance by providing additional photosynthetic area directly or through the cauline leaves they support, which, in turn, provide continuous assimilation during the reproductive stage of plants (Mooney et al 1995;Stevens et al 2008;Tiffin 2000).…”

“…Longer pre-reproductive periods contribute to tolerance through increased accumulation resource-garnering and storage tissue (Lau and Tiffin 2009;Marshall et al 2008), while longer reproductive periods allow plants to recover from losses in seed production caused by herbivoryinduced decreases in resource intake. Extending the reproductive period towards the end of the growing season should allow greater compensation than extending it towards the beginning, which shortens the time available for accumulation of resource-garnering and storage tissue (Lau and Tiffin 2009;Marshall et al 2008). Contrary to this expectation, plants in our study achieved greater compensatory ability by extending their reproductive period at the expense of the pre-reproductive period.…”

Testing for the Effects and Consequences of Mid Paleogene Climate Change on Insect Herbivory

“…This period was characterized by greenhouse conditions with atmospheric carbon dioxide levels ( p CO 2 ) ranging from two to three (i.e., p CO 2 >800 ppm) times those of Holocene values [24], [55]. In general, the effects of this increase in p CO 2 is the decrease of foliar nitrogen (N) concentration, thus elevating the carbon to nitrogen (C:N) ratio and thereby stimulating increased insect feeding which is necessary to maintain metabolic homeostasis [56]–[59]. Significantly, the herbivory pattern for Messel and Eckfeld demonstrates that overall diversity [60] and intensity [61]of insect herbivore damage parallels that of p CO 2 levels.…”

Elevated CO2 Influences Nematode-Induced Defense Responses of Tomato Genotypes Differing in the JA Pathway

“…Moreover, Zavala et al (2009) showed that elevated CO 2 down-regulated the gene expression and activity of cysteine proteinase inhibitors, which are the principal defenses of soybean against insect herbivores [7]. An interaction between CO 2 level and herbivory, however, has seldom been detected in host plants [20]. Our results show that in the jasmonate-deficient mutant spr2 , elevated CO 2 up-regulated the induced defense at 14-dpi based on the SA pathway, including PR1 and BGL2 genes, but did not up-regulate the induced defense based on the JA pathway.…”