Do trophic cascades affect the storage and flux of atmospheric carbon? An analysis of sea otters and kelp forests

Wilmers, Christopher C.; Estes, James A.; Edwards, Matthew S.; Laidre, Kristin L.; Konar, Brenda

doi:10.1890/110176

Cited by 158 publications

(149 citation statements)

References 30 publications

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“…The cascading effects of carnivores are known to be important to carbon dynamics through carnivore-induced changes in autotroph community abundance and species composition (5,19,20). Our research shows that carnivores also can influence carbon dynamics by causing differential herbivory on different plant species coupled with plant physiological responses.…”

Section: Discussionmentioning

confidence: 69%

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Trophic cascade alters ecosystem carbon exchange

Hawlena

Reese

Bradford

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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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...

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Section: Discussionmentioning

confidence: 69%

“…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)(4)(5). Moreover, herbivory can trigger physiological adjustments in the remaining damaged plants, including reduction in photosynthetic rates and increased respiration (6)(7)(8).…”

mentioning

confidence: 99%

Trophic cascade alters ecosystem carbon exchange

Hawlena

Reese

Bradford

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…A trophic cascade in which predation by sea otters limits herbivorous sea urchins is essential for the maintenance of kelp forests across much of the North Pacific Ocean's rocky reefs at higher latitudes (20,21,38,39). Kelp density and standing biomass (a reasonable surrogate for sea cow carrying capacity) is >10-fold lower at islands where sea otter populations have been reduced or lost compared with otherwise similar islands where sea otters abound (21,40). Moreover, transitions between kelp-dominated and deforested ecosystem states with varying sea otter densities occur rapidly, as sharply punctuated phase shifts (41,42).…”

Section: Resultsmentioning

confidence: 99%

Sea otters, kelp forests, and the extinction of Steller’s sea cow

Estes

Burdin

Doak

2015

Proc. Natl. Acad. Sci. U.S.A.

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The late Pleistocene extinction of so many large-bodied vertebrates has been variously attributed to two general causes: rapid climate change and the effects of humans as they spread from the Old World to previously uninhabited continents and islands. Many large-bodied vertebrates, especially large apex predators, maintain their associated ecosystems through top-down forcing processes, especially trophic cascades, and megaherbivores also exert an array of strong indirect effects on their communities. Thus, a third possibility for at least some of the Pleistocene extinctions is that they occurred through habitat changes resulting from the loss of these other keystone species. Here we explore the plausibility of this mechanism, using information on sea otters, kelp forests, and the recent extinction of Steller's sea cows from the Commander Islands. Large numbers of sea cows occurred in the Commander Islands at the time of their discovery by Europeans in 1741. Although extinction of these last remaining sea cows during early years of the Pacific maritime fur trade is widely thought to be a consequence of direct human overkill, we show that it is also a probable consequence of the loss of sea otters and the co-occurring loss of kelp, even if not a single sea cow had been killed directly by humans. This example supports the hypothesis that the directly caused extinctions of a few large vertebrates in the late Pleistocene may have resulted in the coextinction of numerous other species.Steller's sea cow | extinction | sea otter | Commander Islands | kelp

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“…Starting with direct observations of a specific type of mammal within a particular region and timeframe, researchers typically calculate a local effect on carbon. They then extrapolate that effect throughout a mammal's larger range (1,3,5).…”

Section: Pricing Predatorsmentioning

confidence: 99%

Can predators have a big impact on carbon emissions calculations?

Willoughby¹

2018

Proc. Natl. Acad. Sci. U.S.A.

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Do trophic cascades affect the storage and flux of atmospheric carbon? An analysis of sea otters and kelp forests

Cited by 158 publications

References 30 publications

Trophic cascade alters ecosystem carbon exchange

Trophic cascade alters ecosystem carbon exchange

Sea otters, kelp forests, and the extinction of Steller’s sea cow

Can predators have a big impact on carbon emissions calculations?

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