CHAPTER 4

South Atlantic Tidal

STEVEN C. PENNINGS, MERRYL ALBER, CLARK R. ALEXANDER, MELISSA BOOTH, ADRIAN BURD, WEI-JUN CAI, CHRISTOPHER CRAFT, CHESTER B. DEPRATTER, DANIELA DI IORIO, CHARLES S. HOPKINSON, SAMANTHA B. JOYE, CHRISTOF D. MEILE, WILLARD S. MOORE, BRIAN R. SILLIMAN, VICTOR THOMPSON, and JOHN P. WARES

This chapter reviews tidal wetlands that occur along the (Sullivan 2001). Ballast stone offloaded into coastal wetlands Atlantic of the United States from the northern border by ships receiving timber formed novel back-barrier . of North Carolina to the northern distribution limit of man- of channels began in the late 1800s to accommo- groves in central Florida. The South Atlantic coast has a warm date shipping and continues today. Dredge spoil was depos- climate, a wide , and fewer anthropogenic impacts ited onto adjacent , forming another type of novel than the North and Central Atlantic . It is a gently slop- (Sullivan 2001). Finally, commercial and recreational ing coast that supports extensive tidal salt marshes. Tidal harvesting of oyster, crab, shrimp, and expanded in the brackish marshes are common where rivers provide a source of 20th century. How these various impacts affect the freshwater. Rivers upstream of are bordered by tidal functioning of tidal wetlands in the South Atlantic is largely freshwater marshes and . Below, we discuss the histor- unknown. ical human use of the area. Then, building on Pomeroy and Wiegert (1981), Wiegert and Freeman (1990), and Dame, Alber, et al. (2000), we review the ecology of South Atlantic tidal wet- The Physical Setting lands and discuss regional conservation concerns. Geology

Historic Human Use of the Landscape The South Atlantic coastline receives sediment from erosion of the Appalachian Mountains, the deeply weathered and Around 2200 b.c., coastal populations of Native Ameri- bedrock hills of the Piedmont, and the thick, sandy soils of the cans in the South Atlantic began intensively harvesting oys- (Fig. 4.1) (Kennedy 1964). Rivers draining the ters, Crassostrea virginica, and other shellfish (DePratter 1979; Piedmont typically transport more water and an order of mag- Thomas 2008), leaving thick shell deposits, including shell nitude more sediment than those draining the Coastal Plain rings up to 150 m across, on barrier and back-barrier islands (Meade 1982). Early farming practices increased sediment (Crusoe and DePratter 1976; Thompson 2007). When Europe- loads, but this effect has decreased since the 1940s (Trimble ans arrived, Native American populations were at their peak 1974). Most transported sediment is trapped behind or (DePratter 1978; Thomas 2008; Thompson and Turck 2009). in estuarine wetlands, and little reaches the By the late 1600s, however, Native American populations were (Milliman, Pilkey, et al. 1972; Meade 1982). severely reduced by Old World diseases and forced relocation Coastal marshes (Fig. 4.2) formed several thousand years by Europeans (Worth 1995). The shell deposits that they left ago behind developing barrier islands that moderated wave behind, however, were so extensive that European inhabitants action (Alexander and Henry 2007; Mallinson, Burdette, et al. mined them for road fill and construction material (Sullivan 2008). Barrier islands in North Carolina, northern South Caro- 2001). lina, and Florida are composed of unconsolidated (Hayes After 1600, human use of coastal wetlands shifted in focus. 1994). In contrast, barrier islands in southern South Carolina Rice was farmed in diked tidal marshes in Georgia and South and Georgia are compound, with younger, sandy components Carolina from the mid-1700s to circa 1900 (Coclanis 1989, on their eastern sides and older, stratigraphically variable 1993). Some former rice fields are currently maintained as deposits on their western sides. Back-barrier islands (= ham- habitat for waterfowl. Cypress and other trees were mocks) occur between barrier islands and the mainland, and harvested in coastal wetlands, and pine and hardwoods on were created either by erosion of uplands, progradation of the coastal highlands, and they were floated downstream to shoreline, or anthropogenic deposition of dredge-spoil, ballast coastal docks during the late 19th and early 20th centuries stone, or oyster shell.

45

49756txt.indd 45 2012.02.29 06:13 mixing) (McKay and Di Iorio 2010). inputs are mediated by seasonal wind patterns that cause sea level to fall or rise by up to 0.4 m in the summer versus fall and winter, respectively (Di Iorio unpublished).

Land Use and Freshwater Inputs

Rivers are a major source of nutrients and freshwater to coastal wetlands, and estuarine is well predicted by river dis- charge (Sheldon and Alber 2002; Di Iorio unpublished). Nutri- ent delivery varies with flow within a river: nitrate+nitrite dominates dissolved nitrogen (N) loading of the Altamaha River during periods of low flow, whereas dissolved organic nitrogen increases in importance during high flow (Weston, Hollibaugh, et al. 2003). The 12 largest watersheds are domi- nated by forest (33 to 70%) and agriculture (18 to 43.5%). The most important watershed N inputs are fertilizer (33%), net import of food and livestock feed (31%), and agricultural N fix- ation (26%) (Schaefer and Alber 2007a). Riverine N export is correlated with watershed N input (Schaefer and Alber 2007a), but the proportion of N exported to the is only 9% FIG. 4.1. Physiographic regions of the southeastern U.S., and major (Table 4.1), less than half of global estimates of ~25% (Boyer, southeastern rivers, from north to south: RO, Roanoke; PA, Pamlico; Goodale, et al. 2002; Galloway, Dentener, et al. 2004), possi- NE, Neuse; CF, Fear; PD, Pee Dee; BL, Black; SE, Santee; ED, bly due to temperature-driven differences in denitrification Edisto; SA, Savannah; OG, Ogeechee; AL, Altamaha; SL, Satilla; SM, (Schaefer and Alber 2007a). St. Marys; SJ, St. Johns. Another source of freshwater and nutrients to coastal wet- lands is submarine groundwater discharge (Moore 1999). Groundwater fluxes of nutrients, metals, and dissolved inor- Climate and Oceanographic Context ganic and organic carbon (C) can rival or exceed riverine fluxes (Krest, Moore, et al. 2000; Moore, Krest, et al. 2002; Crotwell The southeastern United States has a generally warm and wet and Moore 2003). The nature of groundwater discharge has climate, driven by the interaction between marine tropical been altered by dredging, which can breach underlying con- and continental polar air masses. Tropical air is unstable and fining layers (Duncan 1972), and by groundwater use, which is driven into the region by clockwise circulation around the can lower potentiometric surfaces in aquifers, causing subtropical Atlantic high-pressure cell (the Bermuda High), infiltration (Landmeyer and Stone 1995). giving rise to thunderstorm activity during the summer. The continental polar air mass interacts with the marine tropical air mass during winter, forming baroclinic instabilities that Soils and Biogeochemistry promote cyclogenesis, leading to the bulk of the winter pre- cipitation. South Florida, however, has drier winters than the Tidal salt and brackish marshes of the Southeast generally have rest of the region because the Atlantic high-pressure cell tends sandy, mineral soils, with higher bulk density and less organic to move toward the equator during winter, leading to sinking C and N than marshes of the North Atlantic and coasts air and inhibiting convective storm activity (Soulé 1998). The (Coultas and Calhoun 1976; Daniels, Kleiss, et al. 1984; Gard- strength and location of the Bermuda High are major factors ner, Smith, et al. 1992; Craft 2007). Soils are typically high in determining the supply of freshwater to Georgia coastal sys- sulfides and have poorly developed horizons or layers. Poros- tems (Sheldon and Burd unpublished) and historic patterns of ity is high, ranging from > 50% in mineral soils to 90% in rainfall in the Southeast (Stahle and Cleaveland 1992). organic soils (Craft, Seneca, et al. 1991). The pH of moist salt Tidal patterns in the South Atlantic are primarily driven by and brackish soils is neutral to slightly basic, but some the semidiurnal lunar (M2) and the solar tide (S2). The soils become acidic upon drying as sulfide is oxidized to sul- tidal range varies from 1 to 3 m depending on location and fate (Daniels, Kleiss, et al. 1984). Cation exchange capacity

M2 – S2 interactions. When the dominant M2 tidal wave enters varies depending on and organic content, but exchange bays and estuaries, nonlinear interactions with irregular creek sites are dominated by base cations, Na, K, Ca, and Mg. Brack- geometries and bottom topography produce overtides (har- ish and fresh marshes and swamps tend to have organic or monics) and more complicated tidal cycles (Huang, Chen, et organic-rich mineral soils (Daniels, Kleiss, et al. 1984; Loomis al. 2008). These overtides generally produce asymmetric tidal and Craft 2010). Tidal freshwater marshes and swamps contain currents, with the ebb current stronger and shorter than the little sulfide and are slightly more acidic than brackish and salt current. Water stored in intertidal marshes also contrib- marshes (Loomis and Craft 2010). utes to ebb dominance in the . Within the Southeast, tidal-marsh properties vary River flow, precipitation, and groundwater discharge create depending on salinity, geomorphic position, tide range, veg- an along-channel salinity gradient as high as 1 PSU km–1 (Blan- etation type, and other factors (Table 4.2). Barrier-island salt ton, Alber, et al. 2001). Because the estuaries are shallow, ver- marshes have very sandy soils, with high bulk density and tical stratification is easily destroyed by tidal stirring (vertical low nitrogen compared with lagoonal salt marshes (Table 4.2).

46 Coastal Wetlands

49756txt.indd 46 2012.02.29 06:13 A B

C

E

D

FIG. 4.2. A. Aerial view of creek network permeating Spartina alterniflora , Georgia. B. Aerial view of part of the Georgia coast, with light-green barrier islands to right, mainland to left, and dark green tidal wetlands between. C. Creekbank of S. alterniflora salt marsh at high tide. D. Wrack disturbance in upper levels of salt marsh, with S. alterniflora in foreground and Juncus roemerianus behind. E. Creekbank of S. alterniflora salt marsh at low tide, with oyster atwater’s edge. (Photo credits: A: Clark Alexander; B: 2000 Landsat ETM+ produced by the U.S. Geological Survey; C: K. Więski; D: C. Hladik; E: S. Pennings. Used by permission.)

49756txt.indd 47 2012.02.29 06:13 49756txt.indd 48

table 4.1 Watershed area, land use, N budgets, and N export for major watersheds of the southeastern U.S.

Watershed Riverine Percent Watershed Forest Agriculture Urban Wetlands Water Other N input Specific runoff N export N export Watershed Area (km2) (%) (%) (%) (%) (%) (%) (kg N km-2 yr-1) (mm yr-1) (kg N km-2 yr-1) (%)

Roanoke (NC) 21,984 69.6 22.2 2.8 1.7 2.5 1.4 2,889 352 197 7

Pamlico (NC) 5,748 58.8 26.5 2.7 10.3 0.6 1.0 4,118 334 446 11

Neuse (NC) 7,033 51.0 29.3 7.6 9.8 1.5 0.7 4,884 341 446 9

Cape Fear (NC) 13,599 62.8 20.8 7.0 6.0 1.5 1.8 3,604 355 248 7

Pee Dee (NC) 21,448 61.2 27.0 5.5 3.8 1.1 1.4 4,039 467 390 10

Santee (SC) 32,017 69.7 18.1 7.0 0.8 2.2 2.1 2,676 433 312 12

Black (SC) 3,274 33.3 43.5 3.0 18.1 0.2 1.9 3,282 286 158 5

Edisto (SC) 6,944 45.0 32.3 1.6 15.2 0.7 5.3 2,913 337 228 8

Savannah (GA) 25,488 65.9 18.0 2.8 4.7 3.6 4.9 2,762 418 272 10

Ogeechee (GA) 8,415 44.9 33.6 0.7 14.2 0.6 5.9 3,098 330 283 9

Altamaha (GA) 35,112 57.9 24.5 3.5 7.3 1.2 5.7 3,099 339 273 9

Satilla (GA) 7,348 45.9 30.4 1.0 14.4 0.6 7.7 3,203 275 365 11

Area-weighted average 59.7 24.5 3.9 6.6 1.7 3.5 3,199 379 294 9

note: Watershed N input was obtained by summing all inputs (net atmospheric deposition, fertilizer, N fixation, and net food and feed import) and subtracting non–food crop export. Adapted from Schaefer and Alber (2007a). Specific runoff is calculated as annual river flow divided by watershed area, thus allowing comparisons among watersheds of different sizes. 2012.02.29 06:13 table 4.2 Selected properties of soils (0–30 cm) of the southeast Atlantic coast (North Carolina, South Carolina, Georgia, and Florida) as a function of geomorphic position and location on the salinity gradient

Organic Clay Bulk density matter Total N Total P (%) (%) (%) (g cm-3) (%) (%) (ug g-1)

barrier/sea island Salt marsha,b,c,d 65 ± 8 16 ± 2 13 ± 2 0.94 ± 0.14 4 ± 1 0.19 ± 0.04 690 ± 240

riverine Salt marshb,c,e–l 57 ± 10 20 ± 7 11 ± 4 0.56 ± 0.09 12 ± 2 0.36 ± 0.05 530 ± 100 Brackish marshe,f,g,k,m 16 ± 16 29 ± 16 27 ± 27 0.33 ± 0.07 28 ± 7 0.81 ± 0.26 620 ± 10 Tidal freshwater marshe,k 32 41 2 0.23 ± 0.02 25 ± 4 0.73 ± 0.05 740 ± 190 Tidal forestn 66 7 1 0.45 26 0.64 490

lagoonal Brackish marsha,b,o,p 13 30 6 0.17 ± 0.02 51 ± 3 1.58 ± 0.12 860 ± 60

a Craft, Seneca, and Broome 1993. b Craft, Broome, and Seneca 1988. c Four barrier-island salt marshes and one riverine salt marsh (Craft unpublished data). d Two marshes (Sapelo River estuary) (Craft 2007). Sand, silt, and clay content (Craft unpublished data). e Two salt marshes, one , and one tidal (Paludan and Morris 1999). f Three salt marshes and one brackish marsh (Bradley and Morris 1990). g One salt marsh (Goni and Thomas 2000). h Two salt marshes. Silt content is silt plus clay (Gardner, Smith, Michener 1992). i Two salt marshes (Sharma, Gardner, et al. 1987). j One salt marsh (Vogel, Kjerfve, and Gardner 1996). k Three rivers (Ogeechee, Altamaha, Satilla) (Loomis and Craft 2010). Sand, silt, and clay content (Craft unpublished data). l N from Haines, Chalmers, et al. (1977), P from Nixon (1980). m Coultas and Calhoun 1976. n Craft unpublished data. o Craft, Broome, and Seneca 1986. p Craft, Seneca, and Broome 1991.

Some tidal freshwater and brackish marshes (i.e., those in the by variation in temperature (Weston and Joye 2005; Weston, Albemarle-Pamlico estuaries) are underlain by several meters Porubsky, et al. 2006). of peat, due to the microtidal tide regime, low sediment inputs, and low salinity relative to marshes elsewhere (Craft, Seneca, et al. 1993). Phosphorus content does not vary strongly among Microbial, Plant, and Communities barrier-island, riverine, and lagoonal marshes (Table 4.2). As in all wetlands, biogeochemical conditions in sedi- Microbial Communities ments vary as a function of plant production, microbial pro- cesses, macrofauna, and hydrology. The relative importance Microbes drive the detritus-based food webs of South Atlan- of these factors varies spatially, driving variation in biogeo- tic wetlands and surrounding waters through their activities chemical zonation in both horizontal (across the marsh) and in mineralizing plant and processing carbon. Four or vertical (over depth) directions. Bioturbation and plant roots five of ascomycetous fungi are the primary decompos- affect vertical structure, creating fine-scale spatial variation in ers of Spartina alterniflora along the entire U.S. Atlantic coast, redox conditions (Bull and Taillefert 2001; Kostka, Gribsholt, complemented by seven major bacterial taxa (Newell, Blum, et al. 2002; Gribsholt, Kostka, et al. 2003). Large-scale hori- et al. 2000; Newell 2001; Buchan, Newell, et al. 2003). Spar- zontal zonation occurs along the salinity gradient in estuar- tina patens hosts a higher diversity of ascomycete species than ies. In salt marshes, inundation with seawater rich in sulfate S. alterniflora (Lyons, Alber, et al. 2009). A different suite of favors organic matter decomposition and mineralization via ascomycetous fungi are the major decomposers of black need- microbially mediated sulfate reduction, whereas in tidal fresh lerush, Juncus roemerianus (Newell 2003). Less work has been marshes, decomposition of organic matter is limited by the done on the microbial decomposers of tidal brackish and fresh availability of terminal electron acceptors, and methanogen- marshes. esis is of more pronounced importance (Weston and Joye 2005; Recent studies using molecular techniques have shown that Weston, Dixon, et al. 2006). Soil biogeochemical conditions the sediment bacterial communities of Spartina-dominated vary seasonally (Bull and Taillefert 2001), driven by variation salt marshes in the South Atlantic are quite diverse, with in availability of labile dissolved organic carbon more than estimates of “species” richness comparable to those in terres-

South Atlantic Tidal WetlandS 49

49756txt.indd 49 2012.02.29 06:13 trial soil (Caffrey, Bano, et al. 2007; Lasher, Dyzszynski, et al. nings and Bertness 1999). This hypothesis, however, is false. 2009). A variety of protist species consume bacteria but may Instead, competitive interactions predominate among salt- not control their densities (First and Hollibaugh 2008). marsh plants in the South Atlantic, in part because the more salt-sensitive plant species are rare at low latitudes and in part because low-latitude species are stronger competitors due to Benthic Algae their larger size (Pennings, Selig, et al. 2003). Brackish marshes are dominated by Spartina cynosuroi- Benthic microalgae (diatoms and cyanobacteria) are abun- des and Juncus roemerianus (Higinbotham, Alber, et al. 2004). dant in South Atlantic salt marshes compared with Central The distribution of S. cynosuroides and S. alterniflora on creek- and North Atlantic sites, but are less abundant than in some banks shifts depending on river discharge and estuarine salin- Gulf coast marshes (Joye unpublished data). Macroalgae are ity (White and Alber 2009). The dominant plant in tidal fresh rare in South Atlantic marshes due to the combination of tur- marshes is the grass Zizaniopsis milacea (Higinbotham, Alber, bid water, which limits photosynthesis when algae are sub- et al. 2004), and tidal swamps are dominated by the trees Taxo- merged, and hot temperatures, which cause desiccation when dium distichum (bald cypress) and Nyssa aquatica (tupelo gum) algae are exposed. Microalgal biomass is often greatest on (Conner, Doyle, et al. 2007). Several aspects of the marsh-plant , because these areas are fully exposed to sunlight and community vary systematically along the estuarine salinity constantly moist. Water stress at higher elevations favors cya- gradient. Species richness increases fivefold from saline to fresh nobacteria at the expense of diatoms. Microalgae are also com- sites (Więski, Guo, et al. 2010). Plants are tallest, and nitrogen mon in lower-salinity marshes, though data are limited (Neu- stocks in plants greatest, at fresh sites, but standing biomass bauer, Miller, et al. 2000; Neubauer, Givler, et al. 2005). and carbon stocks in vegetation are greatest at brackish sites. Microalgae production can rival that of angiosperms in coastal marshes (Tyler, Mastronicola, et al. 2003; Porubsky, Velasquez, et al. 2008), and enters the more directly Marine and Terrestrial Invertebrates (Currin, Newell, et al. 1995). Benthic microalgae account for 10 to 60% of gross primary production (Pinckney and Zing- Southeastern salt marshes support dense populations of mol-

mark 1993a,b; Sullivan and Currin 2000) and 20 to 25% of net lusks and (Fig. 4.3a – g). The mud snail Illyanassa vascular plant production (Tobias and Neubauer 2009). Cya- obsoleta occurs in the and feeds on carrion and algae nobacteria are an important source of fixed nitrogen during (Currin, Newell, et al. 1995). The periwinkle Littoraria irrorata periods of nitrogen limitation (Tyler, McGlathery, et al. 2003), occurs in the mid-marsh and feeds on fungal decomposers whereas benthic microalgae can release copious dissolved of Spartina alterniflora (Silliman and Newell 2003). The pul- organic carbon to the water under nutrient-replete conditions monate Melampus bidentatus occurs at high elevations, espe- (Porubsky, Velasquez, et al. 2008). cially in areas not frequented by Littoraria (Lee and Silliman 2006), and feeds on biofilms and fungi. The oyster Crassostrea virginica is the dominant bivalve, forming low-lying reefs. The Angiosperms ribbed , demissa, forms mounds in the mid- marsh (Smith and Frey 1985; Stiven and Gardner 1992). The The dominant salt-marsh plant in the South Atlantic is the Carolina marsh clam Polymesoda caroliniana occurs at low den-

grass Spartina alterniflora (Fig. 4.2a – e), which occurs in mono- sities in the . specific stands at low to intermediate elevations, sometimes Eight crab and several shrimp species are common. Pred- mixed with Salicornia virginica or other species at intermedi- atory mud crabs, Panopeus herbstii and Euritium limosum, ate elevations (Wiegert and Freeman 1990). High marsh eleva- occur throughout all Spartina zones (Silliman, Layman, et tions are dominated by Juncus roemerianus (Pennings, Grant, et al. 2004). Predatory blue crabs, Callinectus sapidus, enter and al. 2005) and Borrichia frutescens (Pennings and Moore 2001). leave marshes with the . The deposit-feeding sand fiddler, This zonation pattern is driven by competition and varying Uca pugilator, and mud fiddler, U. pugnax, occur in sandy and sensitivities of the different plants to flooding and salinity muddy salt habitats, respectively, while the larger U. minax stress. In some marshes, the border between S. alterniflora and occurs in brackish habitats. Finally, the omnivorous wharf high-marsh vegetation is interrupted by an unvegetated salt crab, Armases cinereum, and the herbivorous purple marsh pan with porewater several times those of seawater crab, Sesarma reticulatum, occur, respectively, at the terrestrial (Pennings and Bertness 1999) that is surrounded by a group of border and lower edge of the marsh. The commercial brown, highly salt-tolerant plant species (Wiegert and Freeman 1990). white, and pink shrimp and the smaller grass shrimp use salt Latitudinal variation in climate drives variation in plant marshes for feeding and nursery habitats. Finally, a variety ecology. North of Virginia, aboveground parts of grasses and of meso- and microinvertebrates occupy marshes, living in rushes senesce in the fall, but plants south of Virginia grow association with plants or in marsh soils. These taxa repre- year-round (Gallagher, Reimold, et al. 1980). Due to this dif- sent an important trophic link between detritus or microalgae ference in phenology and warmer temperatures, primary pro- and larger consumers, but only a few have been well studied duction is greater at low than at high latitudes (Turner 1976). (Haines and Montague 1979; Kneib 1986; Kneib, Newell, et al. A number of low-latitude plants, such as J. roemerianus and 1997; Graça, Newell, et al. 2000; Griffin and Silliman 2011). B. frutescens, do not occur north of Virginia (Pennings and The marshes are also populated by “terrestrial” invertebrates

Bertness 1999), likely because they cannot tolerate harsh win- (Fig. 4.4a – e), most notably insects and spiders (Davis and Gray ters. Because salt-marsh plants can benefit each other by shad- 1966; Pfeiffer and Wiegert 1981). More is known about arthro- ing the soil and ameliorating high soil salinities, and because pod food webs in salt marshes than about those in low-salinity low-latitude marshes are hotter than high-latitude marshes, it marshes. Spartina alterniflora supports several herbivores includ- is reasonable to hypothesize that low-latitude plant communi- ing the planthoppers Prokelisia marginata and P. dolus, the bug ties would be strongly structured by positive interactions (Pen- Trigonotylus uhleri, several stem borers, and the tettigoniid Orche-

50 Coastal Wetlands

49756txt.indd 50 2012.02.29 06:13 A B

C D

E F

FIG. 4.3. A. Mud snail, Illyanassa obsoleta. B. Mussel, Geukensia demissa. G C. Littorine snail, Littoraria irrorata, at high densities on Spartina alterniflora. D. Alligator mississippiensis at marsh edge. E. Mud fiddler crab, Uca pugnax. F. Herbivorous crab, Sesarma reticulatum.

G. Predatory crab, Eurytium limosum. (Photo credits: A – C, E, G: S. Pennings; D: J Nifong; F: K. Więski. Used by permission.)

49756txt.indd 51 2012.02.29 06:13 A B

C

D E

FIG. 4.4. A. Tettigoniid grasshopper, Orchelimum fidicinium. B. Prokelisia spp. planthopper on Spartina alterniflora. C. Aphids, Uroleucon ambrosiae,

on Iva frutescens. D. Succulent plant, Batis maritima. E. Forb, Solidago sempervirens. (Photo credits: A, D, E: S. Pennings; B – C: C.-K. Ho. Used by permission.)

limum fidicinium (Smalley 1960; Stiling and Strong 1984). These Ophraella notulata and Paria aterrima, and the grasshoppers Par- are fed on by a variety of parasitoids and predatory insects and oxya clavuliger and Hesperotettix floridensis (Ho and Pennings spiders (Pfeiffer and Wiegert 1981; Stiling and Bowdish 2000). 2008; Pennings, Ho, et al. 2009). Predators include ladybugs, The shrub Borrichia frutescens supports several herbivores, spiders, and the crab Armases cinereum. including the planthopper Pissonotus quadripustulatus, the gall fly Asphondylia borrichiae, and the lepidopteran Argyres- thia sp. (Moon and Stiling 2004), all of which are attacked Vertebrates by hymenopteran parasitoids (Moon, Rossi, et al. 2000). The shrub Iva frutescens supports several herbivores, including Vertebrate utilization of marsh habitat for feeding, foraging, leaf-galling mites, the aphid Uroleucon ambrosiae, the beetles and reproduction is one of the most understudied aspects of

52 Coastal Wetlands

49756txt.indd 52 2012.02.29 06:13 tidal-marsh ecology. The list of vertebrates that utilize tidal marshes is extensive, including feral hogs and horses, deer, rac- coons, otters, bobcats, dolphins, sharks, teleost fish, birds, liz- ards, snakes, turtles, and alligators (Fig. 4.3d). Most of these are not full-time residents of marshes, but instead visit from ter- restrial or to forage on wetland plants, inverte- brates, and fish. For example, although large alligators on bar- rier islands may spend up to 80% of their time in the marine waters of salt marshes, and consume a diet composed of up to 88% marine organisms by weight, they periodically return to freshwater wetlands to reduce osmotic stress and reproduce (J. Nifong and B. Silliman unpublished data). The degree to which vertebrates depend on marshes is in general poorly documented, but it certainly varies among taxa. The fish mullet and mummichog inhabit marsh creeks in huge numbers and feed on marsh detritus and small inverte- brates in creeks and on the marsh surface. Mummichogs occur rarely in habitats besides marshes, and while mullet occur across a range of types, their numbers are highest near wetlands (Kneib 1986). Other vertebrates, such as rac- coons and hogs, are opportunistic foragers in tidal wetlands (Nifong and Silliman pers. observation), but some individuals may feed extensively in these habitats. The effects that vertebrates have on marsh structure and function are, with a few exceptions, poorly understood. Top- down effects are likely to be large but localized for many verte- brates, such as feral hogs and horses, nondetectable for some, such as otters, and huge and widespread for a few, such as mummichogs. Mummichogs have been relatively well stud- ied, and play critical roles in controlling invertebrate densities. They also play a key role in cross-ecosystem subsidies because FIG. 4.5. “Classic” marine biogeographic transitions at Cape Cod, Cape Hatteras, and Cape Canaveral. Biogeographic regions that may they are trophic intermediates that relay C and N from marsh be more appropriate to estuarine habitats (Engle and Summers 1999) invertebrates to estuarine habitats when they are consumed by are indicated by shading; UV, Upper Virginian; LV, Lower Virginian; larger (Kneib 1986, 1997). SC, South Carolinian; GA, Georgian; FL, Floridian.

Biogeography of Wetland Communities inson, et al. 2009). The transition from high to low latitudes across the mid-Atlantic region is associated with changes in The biogeographic paradigm for Atlantic coast marine com- climate that affect the life history and of Spar- munities involves transitions at Cape Cod, Cape Hatteras, and tina (Turner 1976; Kirwan, Guntenspergen, et al. 2009), a large Cape Canaveral (Fig. 4.5). These boundaries, however, may not increase in wetland habitat (Bertness 1999), a transition from apply to wetland communities. For example, the strong tran- dominance by S. patens to Juncus romerianus in the middle ele- sition zone at Cape Hatteras, where the Gulf Stream diverges vations of salt marshes, an increased abundance of salt-toler- from the coastal shelf (Briggs 1974), primarily affects species ant plant species such as Salicornia spp. (Pennings and Bert- with low dispersal ability and those distributed far out on the ness 1999), and turnover in dominant insect herbivore species continental shelf (Fischer 1960; Briggs 1974; Schwartz 1989; (Wason and Pennings 2008). These transitions lead to varia- Roy, Jablonski et al. 1998). In contrast, estuarine invertebrates tion in ecological interactions at different latitudes (Pennings show other biogeographic transitions associated with tempera- and Silliman 2005; Pennings, Selig, et al. 2003; Pennings, Ho, ture gradients (Engle and Summers 1999) (Fig. 4.5). Similarly, et al. 2009). phylogeographic surveys along the Florida coast indicate that the canonical transition zone at Cape Canaveral is strongest for species with restricted dispersal (Pelc, Warner, et al. 2009), Key Ecological Processes although the Florida does act as a barrier for many species (Avise 1992). Disturbance Phylogeographic studies of Spartina alterniflora show genetic transitions across Chesapeake (Blum, Bando, et al. 2007), The primary disturbance in South Atlantic tidal marshes is reflecting the transition between the Upper and Lower Vir- the deposition of floating mats of dead vegetation (wrack) ginian provinces documented by Engle and Summers (1999). onto the marsh by high tides (Fig. 4.2d). Wrack disturbance Similarly, the planthopper Prokelisia marginata is divided into is more common in North Atlantic than South Atlantic tidal

a mid-Atlantic and a South Atlantic – Gulf coast clade, with a marshes because the aboveground biomass of plants at high boundary in Virginia (Denno, Peterson, et al. 2008). A num- latitudes completely dies back in the winter (Turner 1976) and ber of other wetland , including fiddler crabs, bivalves, is vulnerable to erosion by ice. In contrast, plants at low lati- and sheepshead minnow, also display a transition between the tudes grow year-round, and tend to decompose in place (New- Upper and Lower Virginian provinces (Díaz-Ferguson, Rob- ell 1993). Wrack tends to be moved by wind and currents into

South Atlantic Tidal WetlandS 53

49756txt.indd 53 2012.02.29 06:14 predictable locations that are regularly disturbed (Fischer, engineers are likely also important in tidal brackish and fresh Klug, et al. 2000). Although heavy mats of wrack harm vegeta- marshes, but this has not been studied. tion, thin layers may benefit it by shading the soil and amelio- rating salinities or by leaching nutrients (Pennings and Rich- ards 1998). In addition, wrack creates habitat for spiders and Herbivory and Predation is a major food source for (Zimmer, Pennings, et al. 2004). Wrack exported from estuaries can trap sand and Early studies in the South Atlantic found that most of the nucleate the formation of on . Little is known carbon flow from Spartina alterniflora to the ecosystem was about wrack in tidal brackish or fresh marshes, but the tall veg- through detrital processing rather than herbivory (Teal 1962). etation in these marshes probably limits effects to the marsh From this arose the conclusion that herbivory was unimport- edge. ant in marsh processes. In fact, herbivory rates in salt marshes are similar to those in most terrestrial (Cebrian 1999). As described above, herbivores in salt marshes include Microbial Decomposition insects, crabs, and snails. Most of these can suppress plants when common (Denno, Peterson, et al. 2000; Silliman and Angiosperm production of South Atlantic wetlands enters the Zieman 2001; Stiling and Moon 2005; Ho and Pennings 2008), food web primarily through decomposition rather than herbiv- and two, the snail Littoraria irrorata and the crab Sesarma retic- ory. In salt marshes, the dominant grasses decay in a standing ulatum, have been implicated in contributing to localized die- position, and initial decomposition of dead stalks and leaves back of vegetation (Silliman et al. 2005; Hughes, Fitzgerald, et occurs in the air, with periodic wetting by rain and tides. Asco- al. 2009). Herbivory in salt marshes is affected by the abiotic mycetous fungi are the predominant mediators of this phase gradients across which the plants grow (Denno, Lewis, et al. of decomposition, and production of fungal organic mass is on 2005). For example, Littoraria caged at 600 m–2 reduced S. alter- the order of 535 g m–2 y–1 (Newell 2003). Fungi-laden decaying niflora biomass by 90% in creekbank plots, versus 65% in mid- leaves are attractive foods for a variety of consumers, including marsh plots (Silliman and Bertness 2002). How stress affects snails and amphipods (Graça 2000; Kneib, Newell, et al. 1997; herbivory differs as a function of plant and herbivore species Silliman and Newell 2003). These detritivores fragment leaves, (Moon and Stiling 2002a,b; Goranson, Ho, et al. 2004; Stiling which fall into sediments alongside collapsing stalks. Bacteria and Moon 2005). Little is known about herbivore communi- replace fungi as the dominant decomposers in salt-marsh sedi- ties and impacts in tidal brackish and fresh marshes. ments, but fungal activity remains high in low-salinity sedi- Herbivores are more abundant and do more damage to salt- ments (Newell 2003). Fungal biomass is low, but fungal activ- marsh plants in the South than in the North Atlantic (Pen- ity per unit of biomass is high, in low-salinity systems (Newell nings, Ho, et al. 2009). This pattern, which is probably driven 2003), and detritivorous periwinkles, amphipods, and crabs by cold climates limiting herbivore growth rates and densities are less abundant in fresh than in salty marshes (Graça, New- at high latitudes, may be an important selective factor on plant ell, et al. 2000; Newell and Porter 2000). The bulk of angio- traits. Salt-marsh plants are tougher, less nutritious, and more sperm biomass enters the sediments and as chemically defended at low versus high latitudes (Siska, Pen- detritus composed primarily of lignocellulose (Benner, New- nings, et al. 2002). As a result, high-latitude plants support bet- ell, et al. 1984), which is highly recalcitrant to decomposition. ter herbivore growth (Ho, Pennings, et al. 2010). Microbial decomposition of lignocellulose in the sediments is Predation rates vary with elevation, and are usually high- highest during the summer, and is primarily mediated by bac- est at the creekbank (Lin 1989; Silliman and Bertness 2002). teria (Benner, Maccubbin, et al. 1986). Predation rates are probably higher in South than in North Atlantic salt marshes, but the evidence is largely anecdotal. For example, the ribbed mussel occurs along creekbanks in Ecosystem Engineering the North Atlantic but is relegated to higher elevations in the South Atlantic. transplanted to lower elevations Several species in South Atlantic salt marshes are ecosystem were quickly eaten (Stiven and Gardner 1992), suggesting that engineers, changing the physical environment through non- southern marshes experience higher predation rates than trophic mechanisms. Spartina alterniflora creates the marsh northern ones; however, this hypothesis has not been tested platform by trapping sediment and producing peat (Grosholz, with rigorous comparative studies. Similarly, predation rates Levin, et al. 2009). Emergent plants also ameliorate desicca- in arthropod food webs are probably higher in South than in tion at low tide and hinder access by predators, benefitting North Atlantic salt marshes (Pennings pers. observation), but small animals that live in the marsh. Burrowing by fiddler again rigorous comparisons are lacking. Herbivorous arthro- crabs, Uca spp., oxygenates salt-marsh soils, and crabs excrete pod food webs are strongly structured by top-down control wastes in burrows, transporting nutrients from the marsh sur- from parasites and predators (Ho and Pennings 2008; Marc- face to plant root zones; consequently, crabs stimulate plant zak, Ho, et al. 2010). growth (Montague 1982). Patches of mussels, Geukensia dem- issa, on the marsh platform engineer mounds capped with vigorous plant growth (Kuenzler 1961; Smith and Frey 1985). Ecosystem Metabolism Mussels bind sediments and deposit nutrient-rich feces and pseudofeces onto the marsh surface (Kraeuter 1976; Newell The metabolism of South Atlantic estuaries has long been of and Krambeck 1995). Because mussels are largely absent from interest due to their high productivity and potential role in marsh edges in the South Atlantic due to predation (see below), subsidizing marine food webs (Odum 1961, 1968; Schelske they are less important engineers than in New England (Bert- and Odum 1962). The simplest depiction of the C cycle of ness 1984), but oyster reefs at the lower edge of South Atlan- an estuary includes production, respiration, organic C stor- tic salt marshes (Fig. 4.2e) may play a similar role. Ecosystem age and burial, and exchanges with the atmosphere, uplands,

54 Coastal Wetlands

49756txt.indd 54 2012.02.29 06:14 CO2 3941 2859 A a. Gross Production Ecosystem Respiration Benthic microalgae Microbes River Macrofauna input Marsh macrophytes Export

OC—265 Sediment and Water OC—1,347a DIC—180 Organic C 77b 20,000 339c Burial DIC—360 29 b.B Per m2 Marsh GPP 4,500 NPP Marsh 2,025 Marsh 738 Marsh autotrophs detritus heterotrophs NA

Resp. Burial 440 190 1,508 Resp. 2,475 29 Tide Rain MB 738 GPP 2,847 1,230 9,760 326 NPP 528 Aquatic 280 Aquatic Aquatic autotrophs heterotrophs FIG. 4.6. Three ecosystem views of South Atlantic detritus NA marshes. A. Simplified carbon budget. Units are –2 –1 –2 either gC m yr or gC m . Export fluxes with DOC 1,204 Resp. Resp. superscripts refer to: a mass balance of estuarine Burial POC 1,260 528 46 2,025 b 29 Storm 388 system; mass balance of nearshore heterotrophy; c Per m2 water MB 5,014 and measured export from North marshes in South Carolina. Abbreviations: OC: organic carbon; DIC: dissolved inorganic carbon. B. Carbon budgets Intertidal marsh Estuary/bay Inner shelf for linked marsh and aquatic estuarine subsystems. C Fluxes between marsh and aquatic systems are c. shown relative to both marsh and aquatic areas NPP/CO2 fixation = 10.1 (because there is more marsh than water, an output Degassing Degassing = 1.88 Degassing = 0.41 from each square meter of marsh becomes a much River input = 1.64 larger input to each square meter of water). Units –2 –1 DIC = 0.6 are gC m yr . Abbreviations: MB: mass balance; OC=0.9 Resp.: respiration; NPP: net primary production; Total terrestrial export GPP: gross primary production; NA: unknown. Marsh DIC export = 0.83 Net DIC export = 2.6–5.2 Expected marsh OC export = 5.5 DIC = 1.5 C. Conceptual carbon transport model and mass OC = 6.4 Expected OC export = 2.3–4.9? balance analysis for a marsh-estuary – inner shelf continuum scaled up to the entire South Atlantic 12 –1 OC burial = 0.29 Bight. Units are in 10 gC yr . Estimates are based Benthic recycling = 5.1 on a total marsh area of 5.0 × 109 m2.

and ocean (Fig. 4.6a). Few of these processes are easily mea- Estimates of production and respiration are similar through- sured. Consequently, most attempts to quantify C fluxes have out the South Atlantic and Gulf coasts, but are considerably employed indirect measures, such as mass balance of off- reduced in the North Atlantic (Hopkinson 1988). Estimates C budgets (Hopkinson 1985) or mass balance of all the of export to the ocean are considerably higher on the South producer and consumer communities (Wiegert, Christian, et Atlantic (up to 59%) than on the Gulf and Northeast coasts (1 al. 1981; Hopkinson and Hoffman 1984; Hopkinson 1988). to 38%), probably reflecting both high primary production Organic C fluxes associated with rivers are well documented and the high tidal range in the South Atlantic. (Mulholland and Kuenzler 1979; Hopkinson and Hoffman Salt-marsh estuaries are often conceptualized as separate 1984), but those associated with groundwater fluxes are just marsh and aquatic systems with linked C budgets (Fig. 4.6b). beginning to be defined (Moore, Blanton, et al. 2006). This approach indicates that the salt marsh is autotrophic (P/R Ecosystem metabolism (production and respiration) domi- = 4,500/3,213 = 1.4:1) while the aquatic system is heterotrophic nates the coastal C cycle, exceeding riverine inputs by an order (P/R = 326/574 = 0.56:1), and that each square meter of marsh of magnitude (Fig. 4.6a). Approximately two-thirds of fixed exports 1,500 gC yr–1 to estuarine creeks and bays. This is equiv- C inputs are returned to the atmosphere by respiration. Con- alent to an input of almost 10,000 gC to each square meter of siderable C is exported offshore; however, direct measures are water. Mass balance for the aquatic portion (tidal creeks and rare, and C export is usually estimated based on mass balance bays) suggests a flux in excess of 5,000 gC m–2 of water surface of the estuary (Hopkinson 1988) or heterotrophic demands of yr–1 to the ocean. In addition, rivers contribute 1,852 kgC m–1 the nearshore ocean (Hopkinson and Hoffman 1984; Hopkin- shoreline yr–1 to the coastal zone, much of which passes to the son 1988; Cai, Pomeroy, et al. 1999; Cai, Wang, et al. 2003). ocean with little alteration or loss during estuarine transit.

South Atlantic Tidal WetlandS 55

49756txt.indd 55 2012.02.29 06:14 Cai and coworkers (Cai, Pomeroy, et al. 1999; Cai, Wang, productivity of Spartina alterniflora (Pennings unpublished). et al. 2003; Wang, Cai, et al. 2005; Cai 2011) conceptualized Finally, drought promotes marsh die-back (below). southeastern estuaries as a benthic subsystem and an aquatic subsystem (Fig. 4.6c). They used free water measurements of

dissolved O2 and CO2 to document metabolism of both aquatic components and those portions of the benthic subsystem flooded at any time. This was a significant advance, as it did Eutrophication is increasing on the South Atlantic coast. not rely solely on transport of organic C to tidal creeks to sat- Nitrogen and phosphorus inputs to watersheds have isfy heterotrophic demands; instead, the water subsystem increased over the last 50 years, reflecting fertilizer input and moves onto the marsh and there integrates some aspects of an increase in the human population (Schaefer and Alber respiration occurring on the marsh. This approach indicated 2007b). Dissolved oxygen levels at the Skidaway Institute of that the estuarine, bay, and inner-shelf waters of the Georgia Oceanography in Georgia show a steady drop over 19 years Bight are heterotrophic and respire large quantities of organic (Verity, Alber, et al. 2006). Symptoms of eutrophication (nui- C exported from intertidal marshes. sance and toxic algal blooms, /anoxia, fish and shell- fish mortality) exist in nearly half of the major southeastern estuaries, with future deterioration predicted (Bricker, Long- Conservation Concerns staff, et al. 2007). In the recent National Coastal Condition Report (EPA 2008), 54% of the water-quality index ratings in Between 1980 and 2003, coastal counties of the Southeast the South Atlantic were fair or poor, and 59% of chlorophyll Atlantic had the largest rate of population increase (58%) of a concentrations were fair. Eutrophication would be expected any coastal region in the coterminous United States. Most of to stimulate microbial activity (Sundareshwar, Morris, et al. this growth occurred in Florida (EPA 2008), but tourists and 2003), increase plant productivity (Gallagher 1975), and favor retirees are also placing pressure on the Carolinas and Georgia, some plant species, especially Spartina alterniflora, over oth- which are projected to gain 11 million residents by 2025 (U.S. ers (Pennings, Stanton, et al. 2002). Moreover, because plants Census Bureau 2000). These human population changes will commonly respond to eutrophication by investing more bio- drive changes in land use and increase demand for water sup- mass aboveground and less below, eutrophication may reduce ply, wastewater disposal, and coastal resources. Conservation belowground production and thereby reduce the ability of concerns for the region include freshwater delivery, eutrophi- marshes to keep pace with rising sea levels (Darby and Turner cation, management of top consumers, climate change, and 2008). In addition, fertilization may increase the palatability marsh die-back. of plants to herbivores by increasing plant nitrogen content (Silliman and Zieman 2001; Moon, Rossi, et al. 2000; Moon and Stiling 2002a,b). Freshwater Delivery to the Coast

Changes in industrial and human demand for water are likely Management of Top Consumers to affect freshwater delivery to the coast. Because nutrients, pollutants, sediment, and organic material are all carried Humans have markedly affected the densities of many top along with freshwater, changes in freshwater delivery will consumers in southeastern estuarine systems. Alligator den- affect the delivery of these materials as well (Alber 2002). Simi- sities are rebounding from historic hunting, but landings of larly, changes in land cover, such as clearing and draining land commercially important fish and shellfish are declining (EPA for agriculture, will also affect the delivery of freshwater and 2008). Impacts of recreational anglers are difficult to assess but associated materials to the coast. Anthropogenic impacts on will likely increase as population densities rise. We lack good freshwater delivery will be layered on top of natural variabil- data on anthropogenic impacts on most top consumers in ity in freshwater discharge to estuaries. All five Georgia river- southeastern wetlands; however, humans typically reduce the ine estuaries exhibit at least a 29-fold interannual difference populations of large marine predators to a fraction of their nat- between minimum and maximum discharge (GCRC 2002). ural densities (Jackson, Kirby, et al. 2001; Myers, Baum, et al. For example, the onset of drought led to increasing salini- 2007), and so it is likely that populations of many predators in ties in the Satilla River as freshwater discharge declined from southeastern coastal wetlands have been similarly depressed. almost 150 m3s–1 in February 1999 to below 10 m3s–1 in May and The consequences of depressed predator densities for south- June 1999 (Blanton, Alber, et al. 2001). Freshwater inflow also eastern marsh food webs remain largely unexplored. undergoes a regular annual cycle, with seasonal maxima in discharge during the spring and minima in the fall. Potential changes in freshwater inflow are of concern Climate Change because they will affect estuarine resources (Alber 2002). For example, a tide gate and diversion canal near the Savannah Changing climate probably will lead to accelerated sea-level River National Wildlife Refuge displaced the salt wedge 6 to 8 rise and increased storm activity in the South Atlantic. The miles upstream, causing a shift toward salt-tolerant marsh veg- contemporary rate of relative sea-level rise (RSLR) along the –1 etation and changes in (Pearlstine, Kitchens, et al. 1993). South Atlantic is 2 – 3 mm yr (Craft, Clough, et al. 2009), and When the tide gate and canal were later removed, there was a vertical accretion rates in the region range from 2 mm yr–1 –1 shift back toward a tidal freshwater community. Similarly, nat- for salt marshes to 4 – 6 mm yr for brackish and tidal fresh- ural variation in freshwater inflow in the Altamaha River estu- water marshes (Craft 2007), indicating that they are able to ary between drought and wet years altered the distribution of keep pace with RSLR by trapping sediment and accumulating Spartina cynosuroides (White and Alber 2009) and affected sedi- soil organic matter. Climate projections suggest that SLR will ment deposition on the marsh surface (Craft unpublished) and accelerate in the coming century. Although marsh accretion

56 Coastal Wetlands

49756txt.indd 56 2012.02.29 06:14 rates increase with greater sea level (Morris, Sundareshwar, et rapidly emerging understanding of microbial diversity, and a al. 2002), accelerated RSLR is likely to lead to some losses of poor understanding of the ecology of top consumers. South tidal marshes, with losses unequal among tidal fresh, brack- Atlantic coastal wetlands are not pristine, but have been less ish, and salt marshes (Craft, Clough, et al. 2009). Rising sea lev- affected by anthropogenic impacts and climate change than els will also move saltwater farther into estuaries, which will coastal marshes elsewhere in the U.S.; however, they are likely likely accelerate decomposition of soil organic matter (Weston, to deteriorate in coming decades as sea levels and human Dixon, et al. 2006; Craft 2007), further limiting the ability of populations rise unless they are protected by proactive and low-salinity marshes to keep pace with RSLR. strong management policies that regulate land use, freshwa- Hurricanes and storms can drive saltwater upstream, uproot ter delivery to the coast, eutrophication, and harvesting of top vegetation, and either deposit or erode sediments (Nyman, consumers. Crozier, et al. 1995; Cahoon 2006). Hurricane effects on Gulf coast wetlands have been severe (Chabreck and Palmisano 1973). In North Carolina, heavy rainfall from hurricanes low- Acknowledgments ered salinity and increased N and organic C loadings to estuar- ies, with cascading effects on estuarine food webs (Paerl, Bales, We thank the National Science Foundation for ongoing funding et al. 2001). Georgia and South Carolina receive relatively few to the Georgia Coastal Ecosystems Long-Term Ecological Research hurricanes (Hopkinson, Lugo, et al. 2008); however, the fre- Program (OCE06-20959). quency of storms in the South Atlantic is projected to increase in the future (Hayden and Hayden 2003). References

Marsh Die-Back Alber M. 2002. A conceptual model of estuarine inflow manage-

ment. Estuaries 25:1246 – 61. Alber M, Swenson EM, et al. 2008. Salt marsh dieback: an over- In 2001 – 02, salt marshes in Georgia and South Carolina expe-

view of recent events in the US. Estuar. Coast. Shelf Sci. 80:1 – 11. rienced a sudden die-back event that left bare patches in multi- Alexander CR, Henry VJ. 2007. Wassaw and Tybee Islands — com- ple parts of marshes and affected both Spartina alterniflora and paring undeveloped and developed barrier islands. In Guide to Juncus roemerianus (Ogburn and Alber 2006). Many areas were fieldtrips: 56th annual meeting, southeastern section of the Geologi- naturally revegetating by 2009. Sudden die-back has also been cal Society of America, Rich F, editor. Statesboro: Geological Soci- observed in other years in the Southeast and in other areas ety of America, pp. 187 – 98. Avise JC. 1992. Molecular population structure and the biogeo- of the country (Alber, Swenson, et al. 2008; Osgood and Sil- graphic history of a regional fauna: a case history with lessons liman 2009). In the South Atlantic, die-back was associated for conservation biology. Oikos 63:62 – 76.

with low rainfall and low river inflow. In 2001 – 02, the Palmer Benner R, Maccubbin AE, Hodson RE. 1986. Temporal relation- Drought Severity Index for Georgia and South Carolina was ship between the deposition and microbial degradation of lig- characterized as “extreme drought,” and soils at several sites nocellulosic detritus in a Georgia salt marsh and the Okefeno-

kee . Microb. Ecol. 12:291 – 98. were cracked and desiccated. Die-back was also associated Benner R, Newell SY, et al. 1984. Relative contributions of bacteria with drought in Louisiana but not in other areas of the coun- and fungi to rates of degradation of lignocellulosic detritus in

try (Alber, Swenson, et al. 2008). salt-marsh sediments. Appl. Env. Microbiol. 48:36 – 40. The variety of die-back patterns makes it difficult to come Bertness MD. 1984. Ribbed mussels and Spartina alterniflora pro-

up with a single explanation for these events. When present at duction in a New England salt marsh. Ecology 65:1794 – 807. Bertness MD. 1999. The ecology of Atlantic shorelines. Sunderland, high densities, the snail Littoraria irrorata can strongly suppress MA: Sinauer. Spartina alterniflora, and drought may increase plant vulnera- Blanton J, Alber M, Sheldon J. 2001. Salinity response of the bility to (Silliman and Bertness 2002; Silliman, van Satilla river estuary to seasonal changes in freshwater dis- de Koppel, et al. 2005). An interaction between snail grazing charge. In Proceedings of the 2001 Georgia Water Resources Confer-

and drought may explain die-back events on barrier islands, ence, Hatcher KJ, editor. Athens, GA, pp. 619 – 22. Blum MJ, Bando KJ, et al. 2007. Geographic structure, genetic where snail densities are often high, but is less likely to explain diversity and source tracking of Spartina alterniflora. J. Biogeogr. die-back at inland locations, where snail densities are gener- 34:2055 – 69. ally low. Other possibilities include drought-induced changes Boyer EW, Goodale CL, et al. 2002. Anthropogenic nitrogen in soil chemistry or the presence of fungal pathogens (McKee, sources and relationships to riverine nitrogen export in the

Mendelssohn, et al. 2004; Osgood and Silliman 2009). Rigor- northeastern U.S.A. Biogeochem. 57/58:137 – 69. ous evaluation of the various hypotheses is difficult because Bradley PM, Morris JT. 1990. Physical characteristics of salt marsh sediments: ecological implications. Mar. Ecol. Prog. Ser. transient die-back events are often not noticed until they are 61:245 – 52. well developed, at which point the factor causing die-back may Bricker S, Longstaff B, et al. 2007. Effects of nutrient enrichment no longer be present. in the nation’s estuaries: a decade of change. NOAA Coastal Ocean Program Decision Analysis Series No. 26, 328. National Centers for Coastal Ocean Science, Silver Spring, MD. Briggs JC. 1974. Marine zoogeography. New York: McGraw Hill. Conclusions Buchan A, Newell SY, et al. 2003. Dynamics of bacterial and fun- gal communities on decaying salt marsh grass. Appl. Env. Micro-

The warm climate, high sediment supply, and high tidal range biol. 69:6676 – 87. of the South Atlantic have combined to produce geologi- Bull DC, Taillefert M. 2001. Seasonal and topographic variations cally resilient, biogeochemically dynamic, and biologically in porewaters of a southeastern USA salt marsh as revealed by

voltammetric profiling. Geochem. Trans. 13:1 – 8. productive wetlands. Gaps in our scientific understanding Caffrey JM, Bano N, et al. 2007. Ammonia oxidation and ammo- include a paucity of research on lower-salinity tidal marshes nia-oxidizing bacteria and archaea from estuaries with differ-

and swamps (but see Conner, Doyle, et al. 2007), a weak but ing histories of hypoxia. ISME Journal 1:660 – 62.

South Atlantic Tidal WetlandS 57

49756txt.indd 57 2012.02.29 06:14 Cahoon DR. 2006. A review of major storm impacts on coastal native and introduced populations. In Specialization, specia-

wetland elevations. Estuar. Coasts 29:889 – 98. tion, and radiation: the evolutionary biology of herbivorous insects,

Cai W-J. 2011. Estuarine and coastal ocean carbon paradox: CO2 Tilmon KJ, editor. Berkeley: Univ. Calif. Press, pp. 296 – 310. sinks or sites of terrestrial carbon incineration? Annu Rev. Mar. DePratter CB. 1978. Prehistoric settlement and subsistence sys-

Sci. 3:123–145. tems, Skidaway Island, Georgia. Early Ga. 6:65 – 80. Cai W-J, Pomeroy LR, et al. 1999. Oxygen and carbon dioxide DePratter CB. 1979. Shellmound Archaic on the Georgia coast.

mass balance for the estuarine-intertidal marsh complex of five S.C. Antiq. 11:1 – 69.

rivers in the southeastern U.S. Limnol. Oceanogr. 44:639 – 49. Díaz-Ferguson E, Robinson JD, et al. 2009. Comparative phylo- Cai W-J, Wang Z, Wang Y. 2003. The role of marsh-dominated geography of North American Atlantic salt marsh communi-

heterotrophic continental margins in transport of CO2 ties. Estuar. Coasts 33:828 – 39. between the atmosphere, the land-sea interface and the ocean. Duncan DA. 1972. High resolution seismic survey. In Port Royal

Geophys. Res. Lett. 30:1849, doi:10.1029/2003GL017633. environmental study, 85 – 106. Columbia: SC Water Cebrian J. 1999. Patterns in the fate of production in plant com- Resources Commission.

munities. Am. Nat. 154:449 – 68. Engle VD, Summers JK. 1999. Latitudinal gradients in benthic Chabreck RH, Palmisano AW. 1973. The effects of Hurricane community composition in Western Atlantic estuaries. J. Bio-

Camille on the marshes of the Mississippi . Ecology geogr. 26:1007 – 23.

54:1118 – 23. EPA. 2008. National coastal condition report III. Office of Coclanis PA. 1989. The shadow of a dream: economic life and death Research and Development/Office of Water, EPA, Washington,

in the South Carolina low country, 1670 – 1920. New York: Oxford DC. EPA-620/R-03/002. Univ. Press. First MR, Hollibaugh JT. 2008. Protistan bacterivory and benthic Coclanis PA. 1993. Distant thunder: the creation of a world mar- microbial biomass in an intertidal creek . Mar. Ecol.

ket in rice and the transformations it wrought. Am. Hist. Rev. Prog. Ser. 361:59 – 68.

98:1050 – 78. Fischer AG. 1960. Latitudinal variations in organic diversity. Evo-

Conner WH, Doyle TW, Drauss KW. 2007. Ecology of tidal fresh- lution 14:64 – 81. water forested wetlands of the southeastern United States. Dor- Fischer JM, Klug JL, et al. 2000. Spatial pattern of localized dis- drecht: Springer. turbance along a southeastern salt marsh tidal creek. Estuaries

Coultas CL, Calhoun FG. 1976. Properties of some tidal marsh 23:565 – 71.

soils of Florida. Soil Sci. Soc. Am. J. 40:72 – 76. Gallagher JL. 1975. Effect of an ammonium nitrate pulse on the Craft CB. 2007. Freshwater input structures soil properties, verti- growth and elemental composition of natural stands of Spar-

cal accretion, and nutrient accumulation of Georgia and U.S. tina alterniflora and Juncus roemerianus. Am. J. Bot. 62:644 – 48.

tidal marshes. Limnol. Oceanogr. 52:1220 – 30. Gallagher JL, Reimold RJ, et al. 1980. Aerial production, mortal- Craft CB, Broome SW, Seneca ED. 1986. Carbon, nitrogen and ity, and mineral accumulation-export dynamics in Spartina phosphorus accumulation in man-initiated marsh soils. In alterniflora and Juncus roemerianus plant stands in a Georgia salt

Proceedings of the 29th annual meeting of the Soil Science Society marsh. Ecology 61:303 – 12. of North Carolina, Raleigh, NC, USA, Amoozegar A, editor, pp. Galloway JN, Dentener FJ, et al. 2004. Nitrogen cycles: past, pres-

117 – 31. ent, and future. Biogeochem. 70:153 – 226. Craft CB, Broome SW, Seneca ED. 1988. Nitrogen, phosphorus Gardner LR, Smith BR, Michener WK. 1992. Soil evolution along and organic carbon pools in natural and transplanted marsh a forest-salt marsh transect under a regime of slowly rising sea

soils. Estuar. Coasts 11:272 – 80. level, southeastern United States. Geoderma 55:141 – 57. Craft C, Clough J, et al. 2009. Forecasting the effects of acceler- GCRC. 2002. The effects of changing freshwater inflow to estuar- ated sea-level rise on tidal marsh ecosystem services. Front. ies: a Georgia perspective. Georgia Coastal Research Council.

Ecol. Env. 7:73 – 78. www.gcrc.uga.edu/PDFs/inflow1119.pdf. Craft CB, Seneca ED, Broome SW. 1991. Porewater chemis- Goni CA, Thomas KA. 2000. Sources and transformations of try of natural and created marsh soils. J. Exp. Mar. Biol. Ecol. organic matter in surface soils and sediments from a tidal estu-

152:187 – 200. ary (North Inlet, South Carolina, USA). Estuar. Coasts 23:548 – 64. Craft CB, Seneca ED, Broome SW. 1993. Vertical accretion in mic- Goranson CE, Ho C-K, Pennings SC. 2004. Environmental gradi- rotidal regularly and irregularly flooded estuarine marshes. ents and herbivore feeding preferences in coastal salt marshes.

Estuar. Coast. Shelf Sci. 37:371 – 86. Oecologia 140:591 – 600. Crotwell AM, Moore WS. 2003. Nutrient and radium fluxes from Graça MA, Newell SY, Kneib RT. 2000. Grazing rates of organic submarine groundwater discharge to Port Royal Sound, South matter and living fungal biomass of decaying Spartina alter-

Carolina. Aquat. Geochem. 9:191 – 208. niflora by three species of salt-marsh invertebrates. Mar. Biol.

Crusoe D, DePratter CB. 1976. A new look at the Georgia coastal 136:281 – 89.

Shell Mound Archaic. Fla. Anthropol. 29:1 – 23. Gribsholt B, Kostka JE, Kristensen E. 2003. Impact of fiddler crabs Currin CA, Newell SY, Paerl HW. 1995. The role of standing dead and plant roots on sediment biogeochemistry in a Georgia salt-

and Spartina alterniflora and benthic microalgae in salt marsh marsh. Mar. Ecol. Prog. Ser. 259:237 – 51. food webs: considerations based on multiple stable isotope Griffin, J, Silliman BR. 2011. Predator diversity stabilizes and

analysis. Mar. Ecol. Prog. Ser. 121:99 – 116. strengthens trophic control of a keystone grazer. Biol. Letters Dame R, Alber M, et al. 2000. Estuaries of the south Atlantic coast 7:79–82. of North America: their geographical signatures. Estuaries Grosholz ED, Levin LA, et al. 2009. Changes in community struc-

23:793 – 819. ture and ecosystem function following Spartina alterniflora Daniels RB, Kleiss HJ, et al. 1984. Soil systems in North Carolina. invasion of Pacific estuaries. InHuman impacts on salt marshes: North Carolina Agricultural Research Service, Bulletin no. 467. a global perspective, Silliman BR, Grosholz ED, Bertness MD, edi-

Raleigh: NC State Univ. tors. Berkeley: Univ. Calif. Press, pp. 23 – 40. Darby FA, Turner RE. 2008. Below- and aboveground biomass of Haines E, Chalmers A, et al. 1977. Nitrogen pools and fluxes in a Spartina alterniflora: response to nutrient addition in a Louisi- Georgia salt marsh. In Estuarine processes, vol. 2: Circulation,

ana salt marsh. Estuaries and Coasts 31:326 – 34. sediments, and transfer of material in the estuary, Wiley M, editor.

Davis LV, Gray IE. 1966. Zonal and seasonal distribution of insects New York: Academic Press, pp. 241 – 54.

in North Carolina salt marshes. Ecol. Monogr. 36:275 – 95. Haines EB, Montague CL. 1979. Food sources of estuarine inverte- 13 12 Denno RF, Lewis D, Gratton C. 2005. Spatial variation in the rela- brates analyzed using C/ C ratios. Ecology 60:48 – 56. tive strength of top-down and bottom-up forces: causes and Hayden BP, Hayden NR. 2003. Decadal and century-long changes consequences for phytophagous insect populations. Ann. Zool. in storminess at long-term ecological research sites. In Climate

Fenn. 42:295 – 311. variability and ecosystem response at long-term ecological research Denno RF, Peterson MA, et al. 2000. Feeding-induced changes in sites, Greenland D, Goodin DG, Smith RC, editors. New York:

plant quality mediate interspecific competition between sap- Oxford Univ. Press, pp. 262 – 85.

feeding herbivores. Ecology 81:1814 – 27. Hayes M. 1994. Georgia Bight. In Barrier Islands, RA Davis Jr., edi-

Denno RF, Peterson MA, et al. 2008. Life-history evolution in tor. New York: Springer-Verlag, pp. 233 – 304.

58 Coastal Wetlands

49756txt.indd 58 2012.02.29 06:14 Higinbotham CB, Alber M, Chalmers AG. 2004. Analysis of tidal ing in a shallow tidal creek. J. Geophys. Res. 115, C01004, marsh vegetation patterns in two Georgia estuaries using aerial doi:10.1029/2008JC005204.

photography and GIS. Estuaries 27:670 – 83. McKee KL, Mendelssohn IA, Materne MD. 2004. Acute salt Ho C-K, Pennings SC. 2008. Consequences of omnivory for tro- marsh dieback in the Mississippi River deltaic plain: a drought

phic interactions on a salt marsh shrub. Ecology 89:1714 – 22. induced phenomenon? Glob. Ecol. Biogeogr. 13:65 – 73. Ho, CK, Pennings SC, Carefoot TH. 2010. Is diet quality an over- Meade RH. 1982. Sources, sinks, and storage of river sediment in

looked mechanism for Bergmann’s Rule? Am. Nat. 175:269 – 76. the Atlantic drainage of the United States. J. Geol. 90:235 – 52. Hopkinson CS. 1985. Shallow-water benthic and pelagic metabo- Milliman JD, Pilkey OH, Ross DA. 1972. Sediments of the conti- lism: evidence of heterotrophy in the nearshore Georgia Bight. nental margin of the eastern United States. Geol. Soc. Am. Bull.

Mar. Biol. 87:19 – 32. 83:1315 – 34. Hopkinson CS. 1988. Patterns of organic carbon exchange Montague CL. 1982. The influence of fiddler crab burrows and between coastal ecosystems: the mass balance approach in salt burrowing on metabolic processes in salt marsh sediments. In marsh ecosystems. In Coastal-offshore ecosystem interactions, Estuarine comparisons, VS Kennedy, editor. New York: Academic

Jansson B-O, editor. Berlin: Springer-Verlag, pp. 122 – 54. Press, pp. 283 – 301.

Hopkinson CS, Hoffman FA. 1984. The estuary extended — a Moon DC, Rossi AM, Stiling P. 2000. The effects of abiotically recipient-system study of estuarine outwelling in Georgia. In induced changes in host plant quality (and morphology) on a

The estuary as a filter, VS Kennedy, editor. New York: Academic salt marsh planthopper and its parasitoid. Ecol. Ent. 25:325 – 31.

Press, pp. 313 – 30. Moon DC, Stiling P. 2002a. The effects of salinity and nutrients

Hopkinson CS, Lugo AE, et al. 2008. Forecasting effects of sea- on a tritrophic salt-marsh system. Ecology 83:2465 – 76. level rise and windstorms on coastal and inland ecosystems. Moon DC, Stiling P. 2002b. Top-down, bottom-up, or side to side?

Front. Ecol. Env. 6:255 – 63. Within-trophic-level interactions modify trophic dynamics of

Huang H, Chen C, et al. 2008. A numerical study of tidal asym- a salt marsh herbivore. Oikos 98:480 – 90. metry in Okatee Creek, South Carolina. Estuar. Coast. Shelf Sci. Moon DC, Stiling P. 2004. The influence of a salinity and nutri-

78:190 – 202. ent gradient on coastal vs. upland tritrophic complexes. Ecology

Hughes ZJ, FitzGerald DM, et al. 2009. Rapid headward erosion of 85:2709 – 16. marsh creeks in response to relative sea level rise. Geophys. Res. Moore WS. 1999. The subterranean estuary: a reaction zone of

Lett. 36, L03602, doi:10.1029/2008GL036000. ground water and sea water. Mar. Chem. 65:111 – 25. Jackson JB, Kirby MX, et al. 2001. Historical overfishing and the Moore WS, Blanton JO, Joye S. 2006. Estimates of flushing

recent collapse of coastal ecosystems. Science 293:629 – 37. times, submarine groundwater discharge, and nutrient Kennedy VC. 1964. Sediment transported by Georgia streams. fluxes to Okatee River, South Carolina.J. Geophys. Res. 111, USGS Water-Supply Paper 1668. doi:10.1029/2005JC003041. Kirwan ML, Guntenspergen GR, Morris JT. 2009. Latitudinal Moore WS, Krest J, et al. 2002. Thermal evidence of water trends in Spartina alterniflora productivity and the response of exchange through a coastal aquifer: implications for nutrient

coastal marshes to global change. Glob. Chang. Biol. 15:1982 – 89. fluxes. Geophys. Res. Lett. 29:1 – 49. Kneib RT. 1986. The role of Fundulus heteroclitus in salt marsh tro- Morris JT, Sundareshwar PV, et al. 2002. Responses of coastal wet-

phic dynamics. Am. Zool. 26:259 – 69. lands to rising sea level. Ecology 83:2869 – 77. Kneib RT. 1997. The role of tidal marshes in the ecology of estua- Mulholland PJ, Kuenzler EJ. 1979. Organic carbon export from

rine . Oceanogr. Mar. Biol. Ann. Rev. 35:163 – 220. upland and forested wetland watersheds. Limnol. Oceanogr.

KneibRT, Newell SY, Hermeno ET. 1997. Survival, growth and 24:960 – 66. reproduction of the salt-marsh amphipod Uhlorchestia sparti- Myers RA, Baum JK, Shepherd TD, et al. 2007. Cascading effects of nophila reared on natural diets of senescent and dead Spartina the loss of apex predatory sharks from a coastal ocean. Science

alterniflora leaves. Mar. Biol. 128:423 – 31. 315:1846 – 50. Kostka JE, Gribsholt B, et al. 2002. The rates and pathways of car- Neubauer SC, Givler K, et al. 2005. Seasonal patterns and plant- bon oxidation in bioturbated saltmarsh sediments. Limnol. mediated controls of subsurface wetland biogeochemistry.

Oceanogr. 47:230 – 40. Ecology 86:3334 – 44. Kraeuter JN. 1976. Biodeposition by salt-marsh invertebrates. Mar. Neubauer SC, Miller WD, Anderson IC. 2000. Carbon cycling in a

Biol. 35:215 – 23. tidal freshwater marsh ecosystem: a carbon gas flux study. Mar.

Krest JM, Moore WS, et al. 2000. Marsh nutrient export supplied Ecol. Prog. Ser. 199:13 – 31. by groundwater discharge: evidence from radium measure- Newell SY. 1993. Decomposition of shoots of a salt-marsh grass:

ments. Glob. Biogeochem. Cycles 14:167 – 76. methodology and dynamics of microbial assemblages. Adv.

Kuenzler EJ. 1961. Structure and energy flow of a mussel popula- Microb. Ecol. 13:301 – 26.

tion in a Georgia salt marsh. Limnol. Oceanogr. 6:191 – 204. Newell SY. 2001. Spore-expulsion rates and extents of blade occu- Landmeyer JE, Stone PA. 1995. Radiocarbon and δ13C values pation by ascomycetes of the smooth-cordgrass standing-decay

related to ground-water recharge and mixing. Ground Water system. Bot. Mar. 44:277 – 85.

33:227 – 34. Newell SY. 2003. Fungal content and activities in standing-decay- Lasher C, Dyszynski G, et al. 2009. The diverse bacterial commu- ing leaf blades of plants of the Georgia Coastal Ecosystems

nity in intertidal, anaerobic sediments at Sapelo Island, Geor- research area. Aquat. Microb. Ecol. 32:95 – 103.

gia. Microb. Ecol. 58:244 – 61. Newell SY, Blum LK, et al. 2000. Autumnal biomass and poten- Lee S, Silliman B. 2006. Competitive displacement of a detritivo- tial productivity of salt marsh fungi from 29 to 43 north lati-

rous salt marsh snail. J. Exp. Mar. Biol. Ecol. 339:75 – 85. tude along the United States Atlantic coast. Appl. Env. Microbiol.

Lin J. 1989. Influence of location in a salt marsh on survivorship 66:180 – 85.

of ribbed mussels. Mar. Ecol. Prog. Ser. 56:105 – 10. Newell SY, Krambeck C. 1995. Responses of bacterioplankton to Loomis MJ, Craft CB. 2010. Carbon sequestration and nutrient tidal inundations of a saltmarsh in a flume and adjacent mussel

(nitrogen, phosphorus) accumulation in river-dominated tidal enclosures. J. Exp. Mar. Biol. Ecol. 190:79 – 95.

marshes, Georgia, USA. Soil Sci. Soc. Am. J. 74:1028 – 36. Newell SY, Porter D. 2000. Microbial secondary production from Lyons JI, Alber M, Hollibaugh JT. 2009. Ascomycete fungal com- saltmarsh-grass shoots, and its known and potential fates. In munities associated with early decay leaf blades of three Spar- Concepts and controversies in tidal marsh ecology, Weinstein MP,

tina species and a Spartina hybrid in the San Francisco Bay. Kreeger DA, editors. Dordrecht: Kluwer, pp. 159 – 85.

Oecologia 162:435 – 42. Nixon SW. 1980. Between coastal marshes and coastal waters: a Mallinson D, Burdette K, et al. 2008. Optically stimulated lumi- review of twenty years of speculation and research on the role of nescence age controls on late Pleistocene and Holocene coastal salt marshes in estuarine productivity and water chemistry. In

lithosomes. North Carolina, USA. Quaternary Res. 69:97 – 109. Estuarine and wetland processes with emphasis on modeling, Hamil- Marczak LB, Ho C-K, et al. 2010. Latitudinal variation in top- ton P, McDonald KB, editors. New York: Plenum, pp. 437–525. down and bottom-up control of a salt marsh food web. Ecology Nyman JA, Crozier CR, DeLaune RD. 1995. Roles and patterns 92:276–81. of hurricane sedimentation in an estuarine marsh landscape.

McKay P, Di Iorio D. 2010. Cycle of vertical and horizontal mix- Estuar. Coast. Shelf Sci. 40:665 – 79.

South Atlantic Tidal WetlandS 59

49756txt.indd 59 2012.02.29 06:14 Odum EP. 1961. The role of tidal marshes in estuarine production. North Carolina coastal oceanography symposium, George RY, Hul-

In The Conservationist. Albany: NY State Conservation Depart- bert AW, editors. Rockville, MD: NOAA, pp. 335 – 74.

ment, pp. 12 – 15. Sharma P, Gardner LR, et al. 1987. Sedimentation and bioturba- Odum EP. 1968. A research challenge: evaluating the productivity tion in a salt marsh as revealed by 210Pb, 137Cs and 7Be studies.

of coastal and estuarine water. In Proceedings of the Second Sea Limnol. Oceanogr. 32:313 – 26. Grant Conference. Kingston: Univ. RI. Sheldon JE, Alber M. 2002. A comparison of residence time cal- Ogburn MB, Alber M. 2006. An investigation of salt marsh die- culations using simple compartment models of the Altamaha

back in Georgia using field transplants.Estuar. Coasts 29:54 – 62. River Estuary, Georgia. Estuaries 25:1304 – 17. Osgood DT, Silliman BR. 2009. From climate change to snails: Silliman BR, Bertness MD. 2002. A regulates potential causes of salt marsh dieback along the U.S. eastern salt marsh primary production. Proc. Natl. Acad. Sci. USA

seaboard and Gulf coasts. In Human impacts on salt marshes: a 99:10500 – 505. global perspective, Silliman BR, Grosholz ED, Bertness MD, edi- Silliman BR, Layman CA, et al. 2004. Predation by the black-

tors. Berkeley: Univ. Calif. Press, pp. 231 – 54. clawed mud crab, Panopeus herbstii, in mid-Atlantic salt Paerl HW, Bales JD, et al. 2001. Ecosystem impacts of three marshes: further evidence for top-down control of marsh grass

sequential hurricanes (Dennis, Floyd, and Irene) on the United production. Estuaries 27:188 – 96. States’ largest lagoonal estuary, Pamlico Sound, NC. Proc. Natl. Silliman BR, Newell SY. 2003. Fungal farming in a snail. Proc.

Acad. Sci. USA 98:5655 – 60. Natl. Acad. Sci. USA 100:15643 – 48. Paludan C, Morris JT. 1999. Distribution and speciation of phos- Silliman BR, van de Koppel J, et al. 2005. Drought, snails, and phorus along a salinity gradient in intertidal marsh sediments. large-scale die-off of southern U.S. salt marshes. Science

Biogeochem. 45:197 – 221. 310:1803 – 06. Pearlstine LG, Kitchens WM, et al. 1993. Tide gate influences on a Silliman BR, Zieman JC. 2001. Top-down control of Spartina alter-

tidal marsh. Water Res. Bull. 29:1009 – 19. niflora by periwinkle grazing in a Virginia salt marsh. Ecology

Pelc RA, Warner RR, Gaines SD. 2009. Geographical patterns of 82:2830 – 45. genetic structure in marine species with contrasting life histo- Siska EL, Pennings SC, et al. 2002. Latitudinal variation in palat-

ries. J. Biogeogr. 36:1881 – 90. ability of salt-marsh plants: which traits are responsible? Ecol-

Pennings SC, Bertness MD. 1999. Using latitudinal variation to ogy 83:3369 – 81. examine effects of climate on coastal salt marsh pattern and Smalley AE. 1960. Energy flow of a salt marsh grasshopper popu-

process. Curr. Top. Wetl. Biogeochem. 3:100 – 11. lation. Ecology 41:672 – 77. Pennings SC, Grant M-B, Bertness MD. 2005. Plant zonation in Smith JM, Frey RW. 1985. Biodeposition by the ribbed mussel low-latitude salt marshes: disentangling the roles of flooding, Geukensia demissa in a salt marsh, Sapelo Island, Georgia. J. Sed.

salinity and competition. J. Ecol. 93:159 – 67. Res. 55:817 – 28. Pennings SC, Ho C-K, et al. 2009. Latitudinal variation in herbi- Soulé PT. 1998. Some spatial aspects of southeastern United States

vore pressure in Atlantic coast salt marshes. Ecology 90:183 – 95. climatology. J. Geogr. 97:142 – 50. Pennings SC, Moore DJ. 2001. Zonation of shrubs in western Stahle DW, Cleaveland MK. 1992. Reconstruction and analysis

Atlantic salt marshes. Oecologia 126:587 – 94. of spring rainfall over the southeastern U.S. for the past 1000

Pennings SC, Richards CL. 1998. Effects of wrack burial in salt- years. Bull. Am. Meteorol. Soc. 73:1947 – 61. stressed habitats: Batis maritima in a southwest Atlantic salt Stiling P, Bowdish TI. 2000. Direct and indirect effects of plant

marsh. Ecography 21:630 – 38. clone and local environment on herbivore abundance. Ecology

Pennings SC, Selig ER, et al. 2003. Geographic variation in posi- 81:281 – 85. tive and negative interactions among salt marsh plants. Ecology Stiling P, Moon D. 2005. Are trophodynamic models worth their

84:1527 – 38. salt? Top-down and bottom-up effects along a salinity gradi-

Pennings SC, Silliman BR. 2005. Linking biogeography and com- ent. Ecology 86:1730 – 36. munity ecology: latitudinal variation in plant-herbivore inter- Stiling PD, Strong DR. 1984. Weak competition among Spartina

action strength. Ecology 86:2310 – 19. stem borers, by means of murder. Ecology 64:770 – 78. Pennings SC, Stanton LE, Brewer JS. 2002. Nutrient effects on Stiven AE, Gardner SA. 1992. Population processes in the ribbed the composition of salt marsh plant communities along the mussel Geukensia demissa (Dillwyn) in a North Carolina salt southern Atlantic and Gulf coasts of the United States. Estuar- marsh tidal gradient: spatial pattern, predation, growth and

ies 25:1164 – 73. mortality. J. Exp. Mar. Biol. Ecol. 160:81 – 102. Pfeiffer WJ, Wiegert RG. 1981. Grazers on Spartina and their pred- Sullivan B. 2001. Early days on the Georgia tidewater: the story ators. In The ecology of a salt marsh, Pomeroy LR, Wiegert RG, of McIntosh County and Sapelo, 6th ed. Darien, GA: Darien

editors. New York: Springer-Verlag, pp. 87 – 112. Printing. Pinckney J, Zingmark R. 1993a. Biomass and production of ben- Sullivan MJ, Currin CA. 2000. Community structure and func- thic microalgal communities in five typical estuarine environ- tional dynamics of benthic microalgae in salt marshes. In

ments. Estuaries 16:887 – 97. Concepts and controversies in tidal marsh ecology, Weinstein MP,

Pinckney J, Zingmark R. 1993b. Modelling intertidal benthic Kreeger DA, editors. Dordrecht: Kluwer, pp. 81 – 106. microalgal annual production in estuarine ecosystems. J. Phy- Sundareshwar PV, Morris JT, et al. 2003. Phosphorus limitation of

col. 29:396 – 407. coastal ecosystem processes. Science 299:563 – 65. Pomeroy LR, Wiegert RG, editors. 1981. The ecology of a salt marsh. Teal JM. 1962. Energy flow in the salt marsh ecosystem of Geor-

New York: Springer-Verlag. gia. Ecology 43:614 – 24. Porubsky WP, Velasquez L, Joye SB. 2008. Nutrient-replete ben- Thomas DH. 2008. Native American landscapes of St. Catherines thic microalgae as a source of dissolved organic carbon to Island, Georgia. American Museum of Natural History, Anthro-

coastal waters. Estuar. Coasts 31:860 – 76. pological Papers, no. 88, 1 – 1136. Roy K, Jablonski D, et al. 1998. Marine latitudinal diversity gra- Thompson VD. 2007. Articulating activity areas and formation dients: tests of causal hypotheses. Proc. Natl. Acad. Sci. USA processes at the Sapelo Island shell ring complex. Southeast.

95:3699 – 702. Archaeol. 26:91 – 107. Schaefer SC, Alber M. 2007a. Temperature controls a latitudinal Thompson V, Turck JA. 2009. Adaptive cycles of coastal hunter-

gradient in the proportion of watershed nitrogen exported to gatherers. Am. Antiq. 74:255 – 78.

coastal ecosystems. Biogeochem. 85:333 – 46. Tobias C, Neubauer SC. 2009. Salt marsh biogeochemistry — an Schaefer SC, Alber M. 2007b. Temporal and spatial trends in overview. In Coastal wetlands: an integrated ecosystem approach, nitrogen and phosphorus inputs to the watershed of the Alta- Perillo GME, Wolanski E, et al., editors. Amsterdam: Elsevier,

maha River, Georgia, USA. Biogeochem. 86:231 – 49. pp. 445 – 92. Schelske CL, Odum EP. 1962. Mechanisms maintaining high pro- Trimble SW. 1974. Man-induced soil erosion on the southern

ductivity in Georgia estuaries. Proc. Gulf and Caribbean Fish. Piedmont, 1700 – 1970. Ankeny, IA: Soil Conserv. Soc. Am.

Inst. 14:75 – 80. Turner RE. 1976. Geographic variations in salt marsh macrophyte

Schwartz FJ. 1989. Zoogeography and ecology of fishes inhabit- production: a review. Contrib. Mar. Sci. 20:47 – 68. ing North Carolina’s marine waters to depths of 600 meters. In Tyler AC, Mastronicola TA, McGlathery KJ. 2003. Nitrogen fixa-

60 Coastal Wetlands

49756txt.indd 60 2012.02.29 06:14 tion and nitrogen limitation of primary production along a coastal zone. In Proc. 2003 Ga. Water Resource Conf., Hatcher KJ,

natural marsh chronosequence. Oecologia 136:431 – 38. editor. Athens: Univ. Georgia. Tyler AC, McGlathery KJ, Anderson IC. 2003. Benthic algae con- Weston NB, Joye SB. 2005. Temperature-driven decoupling of trol sediment-water column fluxes of organic and inorganic key phases of organic matter degradation in marine sediments.

nitrogen compounds in a temperate . Limnol. Oceanogr. Proc. Natl. Acad. Sci. USA 102:17036 – 40.

48:2125 – 37. Weston NB, Porubsky WP, et al. 2006. Porewater stoichiometry U.S. Census Bureau. 2000. Population projections for South Carolina. of terminal metabolic products, sulfate, and dissolved organic Washington, DC. carbon and nitrogen in estuarine intertidal creek-bank sedi-

Verity PG, Alber M, Bricker SB. 2006. Development of hypoxia in ments. Biogeochem. 77:375 – 408.

well-mixed estuaries. Estuar. Coasts 29:665 – 73. White SN, Alber M. 2009. Drought-associated shifts in Spartina Vogel RL, Kjerfve B, Gardner LR. 1996. Inorganic sediment bud- alterniflora and S. cynosuroides in the Altamaha River estuary.

get for the North Inlet salt marsh, South Carolina, U.S.A. Man- Wetlands 29:215 – 24.

groves & Salt Marshes 1:23 – 35. Wiegert RG, Christian RR, Wetzel RL. 1981. A model view of the Wang AZ, Cai W-J, et al. 2005. The southeastern continental marsh. In The ecology of a salt marsh, 184–218. Pomeroy LR,

shelf of the United States as an atmospheric CO2 source and Wiegert RG, editors. New York: Springer-Verlag. an exporter of inorganic carbon to the ocean. Cont. Shelf Res. Wiegert RG, Freeman BJ. 1990. Tidal salt marshes of the southeast

25:1917 – 41. Atlantic coast: a community profile. Biological Report 85 (7.29). Wason EL, Pennings SC. 2008. Grasshopper (Orthoptera: Tettigo- Washington, DC: USFWS. niidae) species composition and size across latitude in Atlantic Więski K, Guo H, et al. 2010. Ecosystem functions of tidal fresh,

coast salt marshes. Estuar. Coasts 31:335 – 43. brackish, and salt marshes on the Georgia coast. Estuar. Coasts

Weston NB, Dixon RE, Joye SB. 2006. Ramifications of increased 33:161 – 69. salinity in tidal freshwater sediments: geochemistry and Worth JE. 1995. The struggle for the Georgia coast: an eighteenth- microbial pathways of organic matter mineralization. J. - century Spanish retrospective on Guale and Mocama. Am. Museum phys. Res., Biogeosci. 111, G01009, doi:10.1029/2005JG000071. Natural Hist., Anthropol. Papers no. 75. Weston NB, Hollibaugh J, et al. 2003. Nutrients and dissolved Zimmer M, Pennings SC, et al. 2004. Salt marsh litter and detriti-

organic matter in the Altamaha River and loading to the vores: a closer look at redundancy. Estuaries 27:753 – 69.

South Atlantic Tidal WetlandS 61

49756txt.indd 61 2012.02.29 06:14 This page intentionally left blank