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Substrate Mediates Consumer Control of Salt Marsh Cordgrass on Cape Cod, New England

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Substrate Mediates Consumer Control of Salt Marsh Cordgrass on Cape Cod, New England Ecology, 90(8), 2009, pp. 2108–2117 Ó 2009 by the Ecological Society of America Substrate mediates consumer control of salt marsh cordgrass on Cape Cod, New England 1 MARK D. BERTNESS, CHRISTINE HOLDREDGE, AND ANDREW H. ALTIERI Department of Ecology and Evolutionary Biology, 80 Waterman Street, Brown University, Providence, Rhode Island 02912 USA Abstract. Cordgrass die-offs in Cape Cod, Massachusetts, USA, salt marshes have challenged the view that the primary production of New England salt marshes is controlled by physical factors. These die-offs have increased dramatically over the last decade and are caused by the common herbivorous marsh crab Sesarma reticulatum, but other factors that control crab impacts remain unclear. We examined the influence of plant nutrient supply and disturbances on Sesarma herbivory by fertilizing plots and creating experimental disturbances, since previous studies have revealed that they mediate the intensity of herbivory in other Western Atlantic marshes. Neither nutrient enrichment nor experimental disturbances affected crab grazing intensity despite their strong effects in other marsh systems. Within and among Cape Cod salt marshes, however, Sesarma burrows are concentrated on peat substrate. Surveys of 10 Cape Cod marshes revealed that burrow density, depth, and complexity are all much higher on peat than on sand or mud substrate, and paralleling these patterns, crab abundance, herbivore pressure, and the expansion of die-off areas are markedly higher on peat than on other substrates. Complementing work hypothesizing that predator release is triggering increased crab herbivory in Cape Cod marshes, these results suggest that cordgrass die-offs are constrained to the peat substrate commonly found on the leading edge of marshes and that the vulnerability of New England salt marshes to crab herbivory and future die-offs may be predictable. Key words: Cape Cod, New England, USA; consumer pressure; crab herbivory; marsh die-off; peat substrate; salt marsh productivity; Sesarma reticulatum; Spartina alterniflora; top-down control. INTRODUCTION overfishing, and climate change have precipitated extensive cordgrass die-offs (Silliman and Bertness Historically, salt marsh primary production has been 2002, Silliman et al. 2005). On the Atlantic coast of considered to be regulated by bottom-up forces (sensu South America, high densities of the herbivorous crab, Power 1992, Strong 1992). Physical factors like temper- Chasmagnathus granulata, likely a consequence of ature, salinity, and nutrients are thought to regulate the overfishing, maintain large, unvegetated areas in salt primary production of salt marsh plants (Teal 1962, marshes (Costa et al. 2003, Alberti et al. 2007). These Odum 1971, Mendelssohn and Morris 2000). A corol- examples suggest that human disturbances are triggering lary to this paradigm is that consumers play little role in consumer control in salt marsh systems that have controlling salt marsh primary production (Smalley historically been under strong bottom-up control (Bert- 1960, Teal 1962). ness and Silliman 2008). Recent research, however, has suggested that human Most recently, salt marsh die-off, characterized by the disturbances are triggering consumer control of salt extensive loss of Spartina alterniflora (cordgrass) in the marsh primary production across the western Atlantic low marsh and along creek banks (Fig. 1) has been (Bertness and Silliman 2008). Rising snow geese reported on Cape Cod in New England (Massachusetts, populations, fueled by North American nitrogen fertil- USA). These events were initially attributed to drought, izer subsides, have denuded Canadian sub-Arctic fungal disease and direct human disturbances (see Smith marshes, leading to their catastrophic collapse (Jefferies [2006] for an overview), but simple field experiments 1997). In New England, localized eutrophication, driven have revealed that grazing by a native, burrowing crab, by shoreline development, is increasing insect herbivory Sesarma reticulatum (hereafter referred to as Sesarma), and suppressing salt marsh primary production (Bert- is responsible (Holdredge et al. 2009). Sesarma is one of ness et al. 2008). On the Southeastern and Gulf coasts of the most common macroinvertebrates in western Atlan- North America, runaway consumption by native snails, tic salt marshes, from Cape Cod to the Gulf Coast (Gosner 1979, Subrahmanyam and Coultas 1980). They are known herbivores, but our understanding of their Manuscript received 25 July 2008; revised 8 October 2008; accepted 14 October 2008; final version received 8 December impact on marsh systems is entirely anecdotal. The most 2008. Corresponding Editor: P. M. Groffman. widely cited paper on Sesarma ecology is an observa- 1 E-mail: [email protected] tional study noting that Sesarma burrows are often 2108 August 2009 SUBSTRATE MEDIATION OF CONSUMER CONTROL 2109 surrounded by bare, unvegetated substrate that may be maintained by crab grazing (Crichton 1960). They can live communally in large burrow complexes (Seiple 1979, Seiple and Salmon 1982), but their general ecology is largely unstudied. We recently reported the results of field experiments and surveys demonstrating that Sesarma herbivory is responsible for the low-marsh cordgrass die-offs that are epidemic in Cape Cod salt marshes (Holdredge et al. 2009). Nearly 70% of outer and middle Cape Cod marshes are currently experiencing cordgrass die-offs, and Sesarma have denuded 10–90% of creek bank habitats within these marshes. Historic photographs reveal that the rate of die-off expansion has more than doubled over the past decade and currently die-off areas are expanding by .8% per year. In contrast, Sesarma is common in nearby Narragansett Bay, but its densities are limited there by predators (e.g., blue crabs and tautog) and die-offs are not occurring. On Cape Cod, predation pressure on Sesarma is weak, suggesting that the elevated Sesarma densities and herbivory are a consequence of predator release (Holdredge et al. 2009). While elevated herbivore densities appear to be the leading cause of these Cape Cod cordgrass die-offs, factors influencing Sesarma distribution and grazing patterns within and among marshes have yet to be investigated. In other marsh systems, natural distur- bance, nitrogen enrichment, and substrate preferences FIG. 1. Burrow-riddled creek bank at the Cape Cod have all been shown to mediate the herbivore intensity National Seashore, Wellfleet, Massachusetts, USA in June 2007, illustrating Sesarma burrowing activity. Photo credit: and may be modulating the occurrence and expansion M. D. Bertness. rate of die-offs on Cape Cod as well. Natural disturbances often escalate herbivore pressure in ecosystems. Disturbances can kill dominant space 2006), and by releasing plants from nutrient limitation holders and generate free space for weedy species that and increasing plant palatability (Pennings et al. 1998), are poorly defended from grazers (Connell and Slayter can trigger herbivore pressure and consumer control of 1977). This can lead to increased grazer densities and plant productivity. Studies in marsh systems have impacts in disturbed habitats (Sousa 1984). In salt strongly supported the idea that nutrient enrichment marshes, insect (Rand 1999) and small-mammal (Brom- can trigger increased consumer control of primary berg Gedan et al. 2009) herbivory are higher in productivity (Stiling et al. 1991, Gough and Grace disturbance-generated bare space than in undisturbed 1998, Silliman and Zieman 2001, Bertness et al. 2008). vegetation. Cape Cod cordgrass die-offs are most Whether nutrient supplies influence crab grazing in New frequent on the terrestrial border of the low marsh, a England salt marsh systems or contribute to marsh die- habitat dominated by cordgrass (Spartina alterniflora) off, however, has not been addressed. monocultures in undisturbed marshes, but also where Substrate characteristics can also influence consumer floating plant debris or wrack commonly accumulates, patterns by affecting the distribution and abundance of smothering underlying vegetation and generating bare benthic consumers (Raffaelli and Hawkins 1996, Bert- space (Bertness and Ellison 1987). Disturbance-gener- ness 2006). In soft-sediment habitats, substrate compo- ated bare space in New England salt marshes is usually sition can affect the burrowing and feeding efficiency of colonized vegetatively by cordgrass, and since marsh benthic invertebrates (Peterson 1982, Lipcius and Hines herbivores often prefer young over older shoots 1986). In salt marshes, Uca pugilator (sand fiddler crab) (Bortolus and Iribarne 1999), crab grazing could and Uca pugnax (mud fiddler crab), which deposit feed maintain and possibly expand bare patches created by by sieving surface substrate particles with their mouth- wrack disturbance. The role of disturbance in Cape Cod parts (Crane 1975), have substrate-specific field distri- die-offs, however, has not been explored. butions (Teal 1958). Marsh substrate types also affect Nutrient enrichment can also stimulate consumer the distribution and morphological traits of crab control of plants in natural systems (Auerbach and burrows. In soft, muddy substrate, crabs readily form Strong 1981, Menge 1992). Eutrophication is pervasive burrows, but due to poor structural support, longer- in coastal systems (Howarth et al. 2002, Lotze et al. term burrow-maintenance costs are high (Bertness and 2110 MARK D. BERTNESS ET AL. Ecology, Vol. 90, No. 8 Miller 1984). Marsh peat, the
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