Trophic cascade alters ecosystem carbon exchange

Abstract

Trophic cascades-the indirect effects of carnivores on plants mediated by herbivores-are common across ecosystems, but their influence on biogeochemical cycles, particularly the terrestrial carbon cycle, are largely unexplored. Here, using a 13 C pulse-chase experiment, we demonstrate how trophic structure influences ecosystem carbon dynamics in a meadow system. By manipulating the presence of herbivores and predators, we show that even without an initial change in total plant or herbivore biomass, the cascading effects of predators in this system begin to affect carbon cycling through enhanced carbon fixation by plants. Prolonged cascading effects on plant biomass lead to slowing of carbon loss via ecosystem respiration and reallocation of carbon among plant aboveground and belowground tissues. Consequently, up to 1.4-fold more carbon is retained in plant biomass when carnivores are present compared with when they are absent, owing primarily to greater carbon storage in grass and belowground plant biomass driven largely by predator nonconsumptive (fear) effects on herbivores. Our data highlight the influence that the mere presence of predators, as opposed to direct consumption of herbivores, can have on carbon uptake, allocation, and retention in terrestrial ecosystems.experimental ecosystem ecology | animal-mediated carbon cycling | carbon tracer experiment | carbon retention T rophic downgrading-the disproportionate loss of species occupying top trophic levels of ecosystems-is a symptom of global biodiversity decline (1). Cutting short trophic chains in ecosystems causes significant changes in plant community biomass, composition, and diversity (2). These changes come about because loss of carnivores leads to increased impacts of herbivores on plant biomass through changes in herbivore density and foraging strategies (3).It is becoming increasingly recognized that the cascading effects of carnivores may affect ecosystem carbon dynamics as well. By altering the impact of herbivores on plants, carnivores may indirectly regulate the amount and type of plant biomass available for photosynthetic carbon fixation and storage (3-5). Moreover, herbivory can trigger physiological adjustments in the remaining damaged plants, including reduction in photosynthetic rates and increased respiration (6-8). Accordingly, we hypothesized that carnivores should increase plant community carbon fixation and reduce respiration, thereby increasing carbon retention, by causing herbivores to reduce their foraging impacts on plants. We tested this hypothesis with a 13 CO 2 pulse-chase field experiment in a grassland ecosystem in northeastern Connecticut.Using established methods to discern indirect effects of carnivores on plants in ecosystems (9), we applied three experimental treatments in replicated 0.25-m 2 fine-mesh enclosures (Fig. S1): (i) plants only (control), (ii) plants and herbivores (+ herbivore), and (iii) plants, herbivores, and carnivores (+ carnivore). The first treatment served as a control for animal effects, the + he...

The Importance and Benefits of Species

“…For example, fear of the spider Pisaurina mira alters feeding habits of grasshoppers, thus reducing herbivory [23]. Reduced herbivory translates into increased carbon storage because the plants have an increased area for photosynthesis and they no longer need to allocate resources to defend against grasshopper attacks ( Figure 1).…”

The Body Size Dependence of Trophic Cascades

“…By linking diversity and abundance across trophic levels, trophic cascades play an important role in mediating changes in the structure and function of ecological communities. For example, trophic cascades can determine the ecosystem-scale consequences of predator extinction (Estes et al 2011), influence biogeochemical cycles and greenhouse gas dynamics (Wilmers et al 2012;Atwood et al 2013;Strickland et al 2013), and naturally reduce pest abundance and increase agricultural yields (Costamagna et al 2007).…”

The effect of temperature on herbivory by the omnivorous ectotherm snail Lymnaea stagnalis

“…Whereas the temperature rise may generally enhance the growth rates of macrophytes and stimulate plant abundance (Rooney & Kalff, 2000;Feuchtmayr et al, 2009), increased consumption on plants may offset this benefit for the plants (O'Connor, 2009). Trophic downgrading, i.e., the shift toward more macrophyte consumption in food webs, can have a very strong impact on the vegetation, the organisms depending on it, and ultimately on ecosystem functions when temperatures increase (Estes et al, 2011;Strickland et al, 2013).…”