Salt marsh die-off is a term that has been used in the US and UK to describe the death of salt marsh cordgrass leading to subsequent degradation of habitat, specifically in the low marsh zones of salt marshes on the coasts of the Western Atlantic. Cordgrass normally anchors sediment in salt marshes; its loss leads to decreased substrate hardness, increased erosion, and collapse of creek banks into the water, ultimately resulting in decreased marsh health and productivity.
Die-off can affect several species of cordgrass (genus Spartina), including S. alterniflora, S. densiflora, and S. townsendii. There are several competing hypotheses predicting the causes and mechanisms of salt marsh die-off throughout the western Atlantic. These hypotheses place different emphasis on the effects of top-down or bottom-up processes for salt marsh die-off. Combined with salt marsh dieback of the high marsh, salt marsh die-off is a serious threat to the ecosystem services that marshes provide to local coastal communities.
History of top-down vs. bottom-up
In light of their effect on community processes, behaviors, and ecological interactions, consumptive interactions are some of the most widely studied concepts in ecology. Because of this, scientists use food webs to depict all of the food chains and trophic relationships in an ecological community.
Food webs can be controlled by bottom-up or top-down forces, which dictate whether a food web's structure and population dynamics are regulated by nutrients (a supply of fixed carbon) and primary production or by top predators, respectively.
Much energy is lost from one trophic level to the next (about 90%); therefore, the success of higher levels is linked to lower ones and their supply of resources (Lindeman 1942).Lindeman, R.L. 1942. The trophic dynamic aspect of ecology. Ecology 23: 399–418. However, the abundance and distribution of organisms in an ecosystem is also affected by densities of consumers, which limit the success of organisms at lower trophic levels and thereby influence the abundance of these organisms (Hairston et al. 1960).Hairston, N.G., E.D. Frederick, and B.S. Lawrence. 1960. Community structure, population control, and competition. The American Naturalist, 94(879): 421–425.
Many ecologists argue that bottom-up and top-down control do not play equally critical roles in the structure and dynamics of populations in an ecosystem; however, data suggests that both bottom-up and top-down forces impact the structure of food webs and the spatial and temporal abundance and distribution of organisms (Bertness 2007),Bertness, M.D. 2007. Atlantic Shorelines: Natural History and Ecology. Princeton, New Jersey: Princeton University Press. although to what extent each plays a role is not fully understood.
Historically, an emphasis on bottom-up control in many ecosystems has prevailed in ecological thought, often to the exclusion of consumer control (Strong 1992).Strong D.R. 1992. Are trophic cascades all wet-differentiation and donor control in speciose ecosystems. Ecology 73(3): 747–754. Many ecosystems in which consumer control has classically been considered trivial are dominated by plants (e.g., forests, grasslands, and salt marshes) and are usually green in appearance. Hairston and colleagues proposed an opposing view in 1960 that emphasized consumer control. They argued that the “world is green” because higher trophic levels regulate herbivore abundance (Hairston et al. 1960).
Critics pointed out that the world is not always green, and that when it is, herbivores do not necessarily play an important role in structuring plant communities (Ehrlich and Birch 1967).Ehrlich, P.R. and L.C. Birch. 1967. The “balance of nature” and “population control.” The American Naturalist, 101: 97–107. Others argued that what is green is not always edible or of sufficiently high quality to allow increases in herbivore populations (Dixon 1966, Murdoch 1966).Dixon, A.F.F. 1966. The effect of population density and nutritive status of the host on the summer reproductive activity of the sycamore aphid, Drepanosiphum platanoides. J. Anim. Ecol. 35 105–112.Murdoch, W.W. 1966. Community structure, population control, and competition: a critique. The American Naturalist, 100: 219–226. The debate is ongoing, but the dominant view of ecologists remains that although consumers affect many aspects of plant productivity and ecology, top-down control does not drive the productivity of entire plant ecosystems.
More recently, however, examples of conspicuous consumer control of entire ecosystems have emerged in a variety of habitats including lakes (Carpenter et al. 1985),Carpenter, S. R., J. F. Kitchell, and J. R. Hodgson. Cascading trophic interactions and lake productivity. BioScience 35, 634–639 (1985). rivers (Power 1992),Power, M.E. 1992. Habitat heterogeneity and the functional significance of fish in river food webs. Ecology, 73: 1675–1688. and marine (Estes and Duggins 1995)Estes, J. A. and D.O. Duggins. 1995. Sea otters and kelp forests in Alaska: Generality and variation in a community ecological paradigm. Ecological Monographs 65, 75–100. habitats. Foundation plant species can be replaced with other species or substratum completely lacking vegetation and insects can defoliate whole mangroves (Feller 2002).Feller, I. C. 2002. The role of herbivory by wood-boring insects in mangrove ecosystems in Belize. Oikos 97, 167–176.
A classic example of top-down interactions dictating community structure and function comes from Bob Paine's work in Washington, which established that removal of the starfish Pisaster triggered a trophic cascade in which the blue mussel (Mytilus) populations exploded due to release from predation pressure (Paine 1966)Paine, R.T. 1966. Web complexity and species diversity. The American Naturalist, 100(910): 65–75.
Another influential example of top-down control emerged from Jane Lubchenco's experiments on New England rocky shores, which demonstrated that the herbivorous snail L. littorea exerts control on the diversity and succession of tide pool algal communities (Lubchenco and Menge 1978).Lubchenco, J. and B.A. Menge. 1978. Community development and persistence in a low rocky intertidal zone. Ecological Monographs 48: 67–94. One hypothesis that arose from Lubchenco's work (Little and Kitching 1996)Little, C. and J.A. Kitching. 1996. The Biology of Rocky Shores. Oxford, UK: Oxford University Press. was that predation by the green crab (Carcinus maenas) influences rocky shore algal communities by regulating L. littorea abundances.
Ecologists cite these examples as evidence that consumer regulation is more potent and predominant than previously recognized.
Historical paradigms of salt marsh theory
In salt marshes, early ecologists like Eugene Odum and John Teal sparked the current bottom-up paradigm in ecology through work on Sapelo Island, GA (U.S.A) that stressed the dominant role of physical factors like temperature, salinity, and nutrients in regulating plant primary productivity and ecosystem structure (Teal 1962, Odum 1971).Teal, J.M. 1962. Energy flow in the salt marsh ecosystem of Georgia. Ecology 43: 614–624.Odum, E.P. 1971. Fundamentals of Ecology. Philadelphia: Saunders. Ecologists noted that marsh plants were not heavily grazed and appeared to be relatively unpalatable, and thus argued that most plants entered salt marsh food chains as detritus (Teal 1962). A corollary of this dogma is that consumers play an unimportant or subtle role in controlling salt marsh primary production (Smalley 1960, Teal 1962).Smalley A.E. 1960. Energy flow of a salt marsh grasshopper population. Ecology 41:672–77. This paradigm was widely accepted for decades and applied to other ecosystems like mangroves and seagrass beds (Bertness 2007), and has thus “become entrenched in the conceptual understanding of coastal ecosystems” (quote from Bertness and Silliman 2008; Smalley 1960, Nixon 1982).Bertness, M.D. and B.R. Silliman. 2008. Consumer control of salt marshes driven by human disturbance. Conservation Biology 22:618–623.Nixon, S.W. 1982. The ecology of New England high salt marshes: a community profile. Washington, DC: U.S. Dep. Int. Fish Wildl. Serv. FWS/OBS-81/55. 70 pp.
Recent work, however, has demonstrated strong top-down control of plant communities in salt marshes by a wide variety of consumers, including snails, crabs, and geese (Jefferies 1997, Bortolus and Iribarne 1999, Silliman and Bertness 2002, Holdredge et al. 2009).Jefferies, R.L. 1997. Long term damage of sub-arctic ecosystems by geese: ecological indicators and measures of ecosystem dysfunction. In Crawford, R.M.M (ed.). Disturbance and recovery in arctic lands: an ecological perspective. NATO, ASI Series Vol. 25: 151–165. Kluwer: 1997.Bortolus A, Iribarne O. 1999. Effects of the SW Atlantic burrowing crab Chasmagnathus granulata on a Spartina salt marsh. Mar. Ecol. Prog. Ser. 178: 79–88.Silliman, B.R. and M.D. Bertness. 2002. A trophic cascade regulates salt marsh primary production. Proceedings of the National Academy of Sciences USA 99: 10500-10505.Holdredge, C., A. Altieri, and M.D. Bertness. 2009. Role of crab herbivory in die-off of New England salt marshes. Conservation Biology 23: 672–679. Marsh grazers also include feral horses (Furbish and Albano 1994),Furbish, C.E. and M. Albano. 1994. Selective herbivory and plant community structure in a mid-Atlantic salt marsh. Ecology 75: 1015–1022. cattle, hares, insects, and rodents, some of which are able to strongly suppress plant growth.
Strong top-down control on marshes has been demonstrated in various marsh systems. Consumer control is driven by the grapsid crab (Chasmagnathus granulata) in the salt marshes of Argentina and Brazil on the Atlantic coast of South America (Bortolus and Iribarne 1999). Other experiments in Argentina have contributed to the growing body of work evidencing consumer control in salt marshes (Alberti et al. 2007),Alberti J, M. Escapa, P. Daleo, O. Iribarne, B.R. Silliman, M.D. Bertness. 2007. Local and geographic variation in grazing intensity by herbivorous crabs in SW Atlantic salt marshes. Mar. Ecol. Prog. Ser. 349: 235–43. and herbivory has also been suggested to play an important role in southwestern Atlantic marshes (Bortolus and Iribarne 1999, Alberti et al. 2007). Not only are consumers important on a small scale as demonstrated by cage experiments in various locations (Silliman and Zieman 2001, Silliman and Bertness 2002, Silliman et al. 2005),Silliman B.R., Zieman JC. 2001. Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia salt marsh. Ecology 82:2830–45.Silliman B.R., van de Koppel J, Bertness MD, Stanton LE, Mendelssohn IA. 2005. Drought, snails, and largescale die-off of southern U.S. salt marshes. Science 310:1803–6. but they also affect primary productivity across large geographic areas (Silliman and Zieman 2001).
Bertness and Silliman have also suggested that while salt marshes may have historically been nutrient limited and bottom up controlled, human disturbances such as eutrophication and predator depletion has shifted these systems to top down control in recent decades (Bertness and Silliman 2008).
Regional causes of salt marsh die-off
Both top-down and bottom-up forces have been proposed as primary drivers of salt marsh die-off throughout the western Atlantic. The relative importance of these factors depends on the abiotic and biotic conditions of each local or regional marsh system and its environment.
Top-down interactions