Trophic cascade alters ecosystem carbon exchange

Global Change Biology, 2009

The effects of elevated CO 2 on plant growth and insect herbivory have been frequently investigated over the past 20 years. Most studies have shown an increase in plant growth, a decrease in plant nitrogen concentration, an increase in plant secondary metabolites and a decrease in herbivory. However, such studies have generally overlooked the fact that increases in plant production could cause increases of herbivores per unit area of habitat. Our study investigated leaf production, herbivory levels and herbivore abundance per unit area of leaf litter in a scrub-oak system at Kennedy Space Center, Florida, under conditions of ambient and elevated CO 2 , over an 11-year period, from 1996 to 2007. In every year, herbivory, that is leafminer and leaftier abundance per 200 leaves, was lower under elevated CO 2 than ambient CO 2 for each of three species of oaks, Quercus myrtifolia, Quercus chapmanii and Quercus geminata. However, leaf litter production per 0.1143 m 2 was greater under elevated CO 2 than ambient CO 2 for Q. myrtifolia and Q. chapmanii, and this difference increased over the 11 years of the study. Leaf production of Q. geminata under elevated CO 2 did not increase. Leafminer densities per 0.1143 m 2 of litterfall for Q. myrtifolia and Q. chapmanii were initially lower under elevated CO 2. However, shortly after canopy closure in 2001, leafminer densities per 0.1143 m 2 of litter fall became higher under elevated CO 2 and remained higher for the remainder of the experiment. Leaftier densities per 0.1143 m 2 were also higher under elevated CO 2 for Q. myrtifolia and Q. chapmanii over the last 6 years of the experiment. There were no differences in leafminer or leaftier densities per 0.1143 m 2 of litter for Q. geminata. These results show three phenomena. First, they show that elevated CO 2 decreases herbivory on all oak species in the Florida scrub-oak system. Second, despite lower numbers of herbivores per 200 leaves in elevated CO 2 , increased leaf production resulted in higher herbivore densities per unit area of leaf litter for two oak species. Third, they corroborate other studies which suggest that the effects of elevated CO 2 on herbivores are species specific, meaning they depend on the particular plant species involved. Two oak species showed increases in leaf production and herbivore densities per 0.1143 m 2 in elevated CO 2 over time while another oak species did not. Our results point to a future world of elevated CO 2 where, despite lower plant herbivory, some insect herbivores may become more common.

Oecologia, 2003

The unabated increase in global atmospheric CO 2 is expected to induce physiological changes in plants, including reduced foliar nitrogen, which are likely to affect herbivore densities. This study employs a fieldbased CO 2 enrichment experiment at Kennedy Space Center, Florida, to examine plant-herbivore (insect) interactions inside eight open-topped chambers with elevated CO 2 (710 ppm) and eight control chambers with ambient CO 2. In elevated CO 2 we found decreased herbivore densities per 100 leaves, especially of leaf miners, across all five plant species we examined: the oak trees Quercus myrtifolia, Q. geminata, and Q. chapmanii, the nitrogen-fixing vine Galactia elliottii and the shrub Vaccinium myrsinites. Both direct and indirect effects of lowered plant nitrogen may influence this decrease in herbivore densities. Direct effects of lowered nitrogen resulted in increased host-plant related death and an increase in compensatory feeding: per capita herbivore leaf consumption in elevated CO 2 was higher than in ambient CO 2. Indirectly, compensatory feeding may have prolonged herbivore development and increased exposure to natural enemies. For all leaf miners we examined, mortality from natural enemies increased in elevated CO 2. These increases in host-plant induced mortality and in attack rates by natural enemies decreased leaf miner survivorship, causing a reduction in leaf miner density per 100 leaves. Despite increased leaf production in elevated CO 2 from the carbon fertilization effect, absolute herbivore abundance per chamber was also reduced in elevated CO 2. Because insects cause premature leaf abscission, we also thought that leaf abscission would be decreased in elevated CO 2. However, for all plant species, leaf abscission was increased in elevated CO 2 , suggesting a direct effect of CO 2 on leaf abscission that outweighs the indirect effects of reduced insect densities on leaf abscission.

Acta Oecologica-international Journal of Ecology, 2018

Herbivory can trigger physiological processes resulting in leaf and whole plant functional changes. The effects of chronic infestation by an insect on leaf traits related to carbon and nitrogen economy in three Prunus avium cultivars were assessed. Leaves from non-infested trees (control) and damaged leaves from infested trees were selected. The insect larvae produce skeletonization of the leaves leaving relatively intact the vein network of the eaten leaves and the abaxial epidermal tissue. At the leaf level, nitrogen content per mass (N mass) and per area (N area), net photosynthesis per mass (A mass) and per area (A area), photosynthetic nitrogen-use efficiency (PNUE), leaf mass per area (LMA) and total leaf phenols content were measured in the three cultivars. All cultivars responded to herbivory in a similar fashion. The N mass , A mass , and PNUE decreased, while LMA and total content of phenols increased in partially damaged leaves. Increases in herbivore pressure resulted in lower leaf size and total leaf area per plant across cultivars. Despite this, stem cumulative growth tended to increase in infected plants suggesting a change in the patterns of biomass allocation and in resources sequestration elicited by herbivory. A larger N investment in defenses instead of photosynthetic structures may explain the lower PNUE and A mass observed in damaged leaves. Some physiological changes due to herbivory partially compensate for the cost of leaf removal buffering the carbon economy at the whole plant level.

Basic and Applied Ecology, 2011

The lack of data on the combined effects of livestock species and grazing intensity makes it difficult to propose recommendations for the management of biodiversity and production in grassland ecosystems. We therefore divided a fertile grassland into 12 plots that were grazed by either cattle at a high or a low stocking density or by sheep at the same low stocking density. Grazing management had an immediate and direct impact on sward structure. We infer that dominant forbs (Taraxacum officinale) and legumes (Trifolium repens) were strongly disadvantaged by biomass accumulation in lightly grazed plots. Consequently, stocking density affected plant community composition right from the start of the second year of the survey. There was direct and indirect evidence that the selection made by sheep on forbs and legumes could be stronger than the selection made by cattle. The impact of this difference in selectivity took six years to manifest, when legume abundance became lowest and grass abundance peaked in sheep-grazed pastures. Conversely, neither species richness nor evenness of the plant community was modified over the first six years of the survey; it should therefore be continued in order to determine the equilibrium states that can be reached under the three management strategies.

Ecological Studies, 2005

Oikos, 1983

The evolutionary response of plants to herbivory is constrained by the availability of resources in the environment. Woody plants adapted to low-resource environments have intrinsically slow growth rates that limit their capacity to grow rapidly beyond the reach of most browsing mammals. Their low capacity to acquire resources limits their potential for compensatory growth which would otherwise enable them to replace tissue destroyed by browsing. Plants adapted to low-resource environments have responded to browsing by evolving strong constitutive defenses with relatively low ontogenetic plasticity. Because nutrients are often more limiting than light in boreal forests, slowly growing boreal forest trees utilize carbon-based rather than nitrogen-based defenses. More rapidly growing shade-intolerant trees that are adapted to growth in high-resource environments are selected for competitive ability and can grow rapidly beyond the range of most browsing mammals. Moreover, these plants have the carbon and nutrient reserves necessary to replace tissue lost to browsing through compensatory growth. However, because browsing of juvenile plants reduces vertical growth and thus competitive ability, these plants are selected for resistance to browsing during the juvenile growth phase. Consequently, early successional boreal forest trees have responded to browsing by evolving strong defenses during juvenility only. Because severe pruning causes woody plants to revert to a juvenile form, resistance of woody plants to hares increases after severe hare browsing as occurs during hare population outbreaks. This increase in browsing resistance may play a significant role in boreal forest plant-hare interactions. Unlike woody plants, graminoids retain large reserves of carbon and nutrients below ground in both low-resource and high-resource environments and can respond to severe grazing through compensatory growth. These fundamental differences between the response of woody plants and graminoids to vertebrate herbivory suggest that the dynamics of browsing systems and grazing systems are qualitatively different.

PloS one, 2014

Predicted increases in atmospheric carbon dioxide (CO2) concentrations often reduce nutritional quality for herbivores by increasing the C:N ratio of plant tissue. This frequently triggers compensatory feeding by aboveground herbivores, whereby they consume more shoot material in an attempt to meet their nutritional needs. Little, however, is known about how root herbivores respond to such changes. Grasslands are particularly vulnerable to root herbivores, which can collectively exceed the mass of mammals grazing aboveground. Here we provide novel evidence for compensatory feeding by a grass root herbivore, Sericesthis nigrolineata, under elevated atmospheric CO2 (600 µmol mol(-1)) on a C3 (Microlaena stipoides) but not a C4 (Cymbopogon refractus) grass species. At ambient CO2 (400 µmol mol(-1)) M. stipoides roots were 44% higher in nitrogen (N) and 7% lower in carbon (C) concentrations than C. refractus, with insects performing better on M. stipoides. Elevated CO2 decreased N and i...

Biological Control, 2015

By altering foliage quality, exposure to elevated levels of atmospheric CO 2 potentially affects the amount of herbivore damage experienced by plants.

Biogeochemistry, 2011

The carbon (C) sink strength of arctic tundra is under pressure from increasing populations of arctic breeding geese. In this study we examined how CO 2 and CH 4 fluxes, plant biomass and soil C responded to the removal of vertebrate herbivores in a high arctic wet moss meadow that has been intensively used by barnacle geese (Branta leucopsis) for ca. 20 years. We used 4 and 9 years old grazing exclosures to investigate the potential for recovery of ecosystem function during the growing season (July 2007). The results show greater above-and belowground vascular plant biomass within the grazing exclosures with graminoid biomass being most responsive to the removal of herbivory whilst moss biomass remained unchanged. The changes in biomass switched the system from net emission to net uptake of CO 2 (0.47 and -0.77 lmol m -2 s -1 in grazed and exclosure plots, respectively) during the growing season and doubled the C storage in live biomass. In contrast, the treatment had no impact on the CH 4 fluxes, the total litter C pool or the soil C concentration. The rapid recovery of the above ground biomass and CO 2 fluxes demonstrates the plasticity of this high arctic ecosystem in terms of response to changing herbivore pressure.

Ecology letters, 2010

Grazing occurs over a third of the earth’s land surface and may potentially influence the storage of 109 Mg year^−1 of greenhouse gases as soil C. Displacement of native herbivores by high densities of livestock has often led to overgrazing and soil C loss. However, it remains unknown whether matching livestock densities to those of native herbivores can yield equivalent soil C sequestration. In the Trans-Himalayas we found that, despite comparable grazing intensities, watersheds converted to pastoralism had 49% lower soil C than watersheds which retain native herbivores. Experimental grazer-exclusion within each watershed type, show that this difference appears to be driven by indirect effects of livestock diet selection, leading to vegetation shifts that lower plant production and reduce likely soil C inputs from vegetation by c. 25 gC m^−2 year^−1. Our results suggest that while accounting for direct impacts (stocking density) is a major step, managing indirect impacts on vegetation composition are equally important in influencing soil C sequestration in grazing ecosystems.

Arthropod-Plant Interactions, 2010

Global environmental changes are hypothesized to affect herbivores indirectly via changes in plant defenses, and many studies have been conducted to explore effects of environmental change on plant chemistry and herbivory. We quantitatively synthesized data from these studies to produce generalities about the effects of a broad array of environmental changes on herbivores. Since conversion of natural habitat to agriculture has been one of the most profound environmental changes over the past century, the effects of global change variables on plant defense were also compared between natural and agricultural systems. We found evidence that increasing CO 2 , light availability, and nutrients all consistently increase herbivory, particularly by generalists. No significant differences in chemistry and herbivory response variables were found between natural and managed systems. Overall, these results are consistent with recent predictions of a disruption of natural trophic interactions with global change.

Ecology, 2020

Relatively little is known about how plant–soil feedbacks (PSFs) may affect plant growth in field conditions where factors such as herbivory may be important. Using a potted experiment in a grassland, we measured PSFs with and without aboveground insect herbivory for 20 plant species. We then compared PSF values to plant landscape abundance. Aboveground herbivory had a large negative effect on PSF values. For 15 of 20 species, PSFs were more negative with herbivory than without. This occurred because plant biomass on “home” soils was smaller with herbivory than without. PSF values with herbivory were correlated with plant landscape abundance, whereas PSF values without herbivory were not. Shoot nitrogen concentrations suggested that plants create soils that increase nitrogen uptake, but that greater shoot nitrogen values increase herbivory and that the net effect of positive PSF and greater aboveground herbivory is less aboveground biomass. Results provided clear evidence that PSFs ...

Functional Ecology, 2007

Impacts of environmental changes on carbon cycling in terrestrial ecosystems are typically correlated with shifts in the composition, biomass and activity of soil faunal communities. Given the role of soil fauna in decomposition, shifts in soil faunal communities may further modify the carbon dynamics of a perturbed system.