全球变化知识资源中心(globalchange): Predators help protect carbon stocks in blue carbon ecosystems

Predators continue to be harvested unsustainably throughout most of the Earth's ecosystems. Recent research demonstrates that the functional loss of predators could have far-reaching consequences on carbon cycling and, by implication, our ability to ameliorate climate change impacts. Yet the influence of predators on carbon accumulation and preservation in vegetated coastal habitats (that is, salt marshes, seagrass meadows and mangroves) is poorly understood, despite these being some of the Earth's most vulnerable and carbon-rich ecosystems. Here we discuss potential pathways by which trophic downgrading affects carbon capture, accumulation and preservation in vegetated coastal habitats. We identify an urgent need for further research on the influence of predators on carbon cycling in vegetated coastal habitats, and ultimately the role that these systems play in climate change mitigation. There is, however, sufficient evidence to suggest that intact predator populations are critical to maintaining or growing reserves of 'blue carbon' (carbon stored in coastal or marine ecosystems), and policy and management need to be improved to reflect these realities.

Climate change is an urgent societal issue that can be addressed by a combination of reduced emissions and climate mitigation strategies, including those based on natural carbon (C) stores (that is, biosequestration). The need to reduce atmospheric CO₂ concentrations combined with global interest in C trading and pricing has intensified research on the C storage capacity of natural ecosystems. To date, most C conservation programs have focused on managing and/or restoring terrestrial ecosystems, such as tropical forests, to maintain/boost their role in climate change mitigation. Recent studies^{1, 2, 3} suggest, however, that despite their small global extent, vegetated coastal habitats (seagrass meadows, mangroves and salt marshes) play a disproportionately large role in the global capture and storage of C.

Biosequestration in vegetated coastal habitats, a process that takes up atmospheric CO₂ and stores it for millennia in plant biomass and sediments (that is, blue C), is emerging as one of the most effective methods for long-term C storage^{4, 5}. Vegetated coastal habitats bury C 40 times faster than tropical forests and contribute 50% of the total C buried in ocean sediments⁶. The quantity of C (up to 25 billion tonnes) estimated to be stored in vegetated coastal habitats makes them the most C-rich ecosystems in the world (Table 1)^{2, 4}. Because of the remarkable capacity of vegetated coastal habitats to sequester and store C for millennia, they should be prominent in our strategies to combat climate change⁷. Yet our ability to conserve these natural C sinks is hampered by our limited understanding of the mechanisms that are conducive to high C accumulation and preservation rates.

Table 1: Global organic carbon (OC) burial and stock within the top 1 m of sediment in vegetated coastal ecosystems.

Full table

Trophic cascades in vegetated coastal ecosystems have been identified in a number of ecosystems, but most studies have involved small-scale experiments and/or focused on small-bodied animals. In seagrass ecosystems, such studies have demonstrated that predators indirectly and positively affect plant growth through predation on small-bodied invertebrates that cause seagrass fouling²⁵. Multiple empirical studies have revealed that top predators can also initiate trophic cascades in seagrass ecosystems and that, in general, trophic cascades appear to be important in these systems²⁶. In a subtropical seagrass ecosystem in Western Australia, large tiger sharks induce shifts in foraging habitat use of the dominant grazers — dugongs (Dugong dugon) and green turtles (Chelonia mydas) — as well as changes in foraging tactics (see Heithaus et al.²⁷ for a review). These foraging shifts aid the development of high-biomass seagrass beds dominated by slow-growing species and higher C stocks in habitats dangerous to grazers (Fig. 2). In habitats that are safer for grazers, low-biomass beds dominated by fast-growing species²⁸ support lower C stocks. These findings suggest that herbivore and predator conservation need to be considered in concert to avoid degradation of seagrass beds and cascading effects on blue C¹³.

As in seagrass ecosystems, trophic cascades are increasingly being identified in salt marshes, and top-down control of community structure seems to be a feature of these ecosystems. For example, control of grazing snails by predatory crabs is critical to the persistence of some salt marshes²⁹. Indeed, loss of predatory crabs can result in the complete loss of salt marshes^{29, 30}. In other marshes, overfishing of predators has led to increases in populations of herbivorous crabs that can lead to marsh overgrazing, collapse and reduced C sequestration^{31, 32} (Fig. 2). It is, however, important to acknowledge that in salt marshes as well as other blue C ecosystems, the magnitude and direction of predator effects is context-dependent^{33, 34}. For example, in some marsh systems, predatory crabs can actually have negative indirect impacts on marsh grasses by inducing snails to climb higher where their grazing has a stronger negative impact on plant production³⁵.

Evidence for trophic cascades in mangrove ecosystems is scarce, especially involving top predators. For example, fisheries closures in an Australian mangrove ecosystem increased the abundance of large-bodied predators three-fold, but no effect was detected on the abundance of planktivores, scavengers or detritivores in broad-scale monitoring³⁶. Indirect evidence, however, suggests that reductions to predator populations in mangroves could have cascading effects on C capture and storage in some cases. Small-bodied predators (for example predatory ants and birds) can directly and indirectly protect mangroves from insect herbivory^{37, 38}, which would otherwise negatively affect the photosynthetic capacity of mangroves. Shore crabs also seem to be a major driver of recruitment, tree density and distribution, and size structure in mangrove and other coastal tropical forests^{39, 40}, and are a major dietary constituent for many declining species of predators (sting rays, shore birds and fish)^{41, 42}. Furthermore, bioturbating crabs appear to have major influences on C sequestration, as mangrove ecosystems with large crab populations have lower C sequestration rates than those with no or few crabs (Fig. 2). Although further research on the occurrence of trophic cascades in mangroves is needed, there is indirect evidence suggesting that C capture, accumulation and preservation in mangroves is likely to be influenced by top-down processes.

As mentioned above, the specific direction of predator impacts on their ecosystems is context-dependent, and can be influenced by several factors including food web structure, the number of trophic levels present, and the diversity of species^{43, 44, 45}. Trophic cascade theory predicts that the removal of predators from odd-numbered food chains will have negative effects on primary producers and aspects of C storage, while removal of predators from even-numbered food chains will have the opposite effect^{11, 12, 45}. For example, recent findings that American alligators (Alligator mississipiensis) can consume a considerable biomass of predatory blue crabs in coastal marshes and mangroves⁴⁶ indicate that it is possible that historical declines in alligator populations may trigger trophic cascades that benefit blue carbon processes in marshes of the southeastern United States. Omnivory and highly reticulate species networks can also reduce the magnitude of, alter the direction of, or eliminate cascading predator effects on lower trophic levels and ecosystem processes^{44, 45}. For example, time-series analyses from a temperate seagrass ecosystem suggest that recolonizing sea otters promoted the expansion of seagrass beds by reducing crab populations that in turn led to increases in micrograzer prey, which reduced the biomass of epiphytic algae, increasing seagrass productivity⁴⁷. This four-trophic-level cascade initiated by otters is in contrast to that observed by the loss of large predatory fish in temperate seagrasses of Sweden, which led to increases in mesopredators, declines in small herbivores and increases in epiphytic algae that triggered seagrass decline⁴⁸. As a result, predicting the effects of predator loss on blue C a priori may be challenging in ecosystems for which we lack sufficient knowledge of food web structure. Food web theory and behavioural ecological theory, however, provides a basis for making robust predictions that seem to apply across ecosystem types³³.

Most of the C stored in vegetated coastal ecosystems is in the form of organic material trapped in the anoxic sediments underlying vegetation^{1, 3, 49}. This organic matter may originate outside the ecosystem and can be trapped within the ecosystem in tidal currents; for example terrestrial plant material in seagrass beds¹⁵ or seagrass material in mangrove sediments⁵⁰. Deposited detritus is trapped within vegetated coastal ecosystems because of the enhanced friction offered by the vegetation structure^{50, 51, 52}. Here, the height and density of canopies, aerial roots and tree trunks are key factors that promote sediment deposition as they dampen waves and currents and increase benthic surface area^{53, 54}, allowing organic C to be buried under low- or no-oxygen conditions that slow decomposition^{55, 56}. Disturbances, such as herbivory, can alter the friction offered by vegetation by directly altering canopy height and shoot/root density, or indirectly via changes in the community composition of the vegetation.

Predation can alter the capacity of vegetated coastal ecosystems to trap particles by indirectly influencing canopy height, or shoot/root density via effects on herbivores. In some cases herbivores can alter canopy height or density through direct consumption of plant material^{28, 57, 58}. For example, the sudden appearance of a grazing limpet in seagrass meadows of Monterey Bay, US, resulted in the reduction of shoot densities by 68% and the conversion of over 50% of the meadow to bare sand⁵⁸. Under more extreme settings, such as those seen in the salt marshes of Cape Cod, US, and seagrass meadows of Bermuda and Indonesia, relaxed predation on herbivores can result in the removal of 90–100% of the aboveground vegetation in a patch, reducing the canopy height to zero^{13, 59, 60, 61}. Removal of the canopy can result in far lower sedimentation rates compared with vegetated areas^{62, 63}, and overall negative impacts on sediment accretion rates^{64, 65}. Risk of predation, however, can alter the feeding behaviour of some herbivores to less destructive modes⁶⁶. In the seagrass meadows of Shark Bay, Western Australia, dugongs trade-off food quality for vigilance in habitats with high predation risk by only cropping seagrass blades rather than excavating^{66, 67}. Although the effects of cropping on canopy height are context-dependent²⁸, cropping is less destructive than excavation because it leaves both rhizomes and leaf blades more intact. Intense cropping in the absence of predators, however, can have substantial impacts on the complexity of the meadow. Indeed, reductions to canopy height by more than 50%, as seen in the case of green sea turtles⁶⁰, can lead to as much as a 10-fold reduction in sediment accumulation rates and sediment re-suspension⁶⁸.

Herbivory may also indirectly alter canopy height and shoot/root density via indirect changes in plant species composition. For example, under low predation risk, dugongs and sea turtles forage by excavating the nutrient-rich rhizomes of seagrasses^{59, 66, 69}. This foraging mode creates conditions that favour fast-growing seagrass species that are associated with lower sedimentary C stocks^{14, 70}. Similarly, herbivory of the dominant marsh plant Spartina densiflora by crabs and wild guinea pigs affects secondary succession of salt marsh in Argentina by allowing structurally different subordinate species (Sarcocornia perennis and Cress truxillensis) to establish⁷¹. Alterations to the community composition of primary producers will affect sediment accumulation rates in vegetated coastal ecosystems because differences in canopy/root height, blade flexibility and shoot/root density influence sediment dynamics^{14, 15}. In general, large reductions in annual sedimentation rates mediated through top-down changes in plant community composition pose a serious threat to sediment C accretion rates of vegetated coastal habitats, as this is one of the major processes by which these systems accumulate C.

The proportion of outside material that is trapped in a vegetated coastal ecosystem can be high, for example 70% of the total organic carbon in seagrass⁷², but in many instances in situ production of roots and wood contributes the majority of the organic C within vegetated coastal ecosystems sediment^URL:


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