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Predation by the Black-Clawed Mud Crab, Panopeus Herbstii, in Mid-Atlantic Salt Marshes: Further Evidence for Top-Down Control of Marsh Grass Production

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Predation by the Black-Clawed Mud Crab, Panopeus Herbstii, in Mid-Atlantic Salt Marshes: Further Evidence for Top-Down Control of Marsh Grass Production Estuaries Vol. 27, No. 2, p. 188±196 April 2004 Predation by the Black-clawed Mud Crab, Panopeus herbstii, in Mid-Atlantic Salt Marshes: Further Evidence for Top-down Control of Marsh Grass Production BRIAN REED SILLIMAN*², CRAIG A. LAYMAN³, KANE GEYER, and J. C. ZIEMAN Department of Environmental Sciences, University of Virginia, Charlottesville, Virginia 22903 ABSTRACT: Although top-down control of plant growth has been shown in a variety of marine systems, it is widely thought to be unimportant in salt marshes. Recent caging experiments in Virginia and Georgia have challenged this notion and shown that the dominant marsh grazer (the periwinkle, Littoraria irrorata) not only suppresses plant growth, but can denude marsh substrate at high densities. In these same marshes, our ®eld observations suggest that the black- clawed mud crab, Panopeus herbstii, is an abundant and potentially important top-down determinant of periwinkle density. No studies have quantitatively examined Panopeus distribution or trophic interactions in marsh systems, and its potential impacts on community structure remained unexplored. We investigated distribution and feeding habits of Panopeus in eight salt marshes along the Mid-Atlantic seashore (Delaware±North Carolina). We found that mud crabs were abundant in tall (4±82 ind m22), intermediate (0±15 ind m22), and short-form (0±5 ind m22) Spartina alterni¯ora zones in all marshes and that crab densities were negatively correlated with tidal height and positively correlated with bivalve density. Exca- vation of crab lairs routinely produced shells of plant-grazing snails (up to 36 lair21) and bivalves. Lab experiments con®rmed that mud crabs readily consume these abundant marsh molluscs. To experimentally examine potential com- munity effects of observed predation patterns, we manipulated crab and periwinkle densities in a 1-mo ®eld experiment. Results showed that Panopeus can suppress gastropod abundance and that predation rates increase with increasing snail density. In turn, crab suppression of snail density reduces grazing intensity on salt marsh cordgrass, suggesting presence of a trophic cascade. These results indicate that this previously under-appreciated consumer is an important and indirect determinant of community structure and contribute to a growing body of evidence challenging the long-standing notion that consumers play a minor role in regulating marsh plant growth. Introduction cades, indirectly enhancing plant biomass by sup- Predators can have strong effects on the struc- pressing densities of potent grazers (Lubchenco ture of marine communities, both directly by con- 1978; Silliman and Bertness 2002; Trussell et al. trolling prey abundance through consumption 2002). (Menge 1976; Lubchenco 1978) and behavioral- In shallow-water habitats, members of the crab mediation (Trussell et al. 2002) and indirectly family Xanthidae (mud crabs) are important, but through the facilitation of lower trophic levels via often overlooked (because of small size and cryptic trophic cascades (Paine 1966; Estes and Palmisano behavior), benthic predators. Xanthid crabs are 1974). Top-down control of community structure equipped with disproportionately large crushing has been demonstrated in a variety of benthic sys- claws and have voracious appetites for small inver- tems, including rocky shores (Menge 1976), kelp tebrates (Williams 1984). Mud crabs typically main- ; beds (Estes and Palmisano 1974), coral reefs (Hay tain shallow ( 4±10 cm in depth), excavated lairs in soft substrate, under rocks or in shell piles (Wil- 1984), seagrasses (Heck and Valentine 1995), and liams 1984; Kneib and Weeks 1990). Many studies mud (Posey and Hines 1991) and sand ¯ats (Am- have suggested that these shell-crushing decapods brose 1984). In these habitats, decapod crabs are are important community structuring forces, lim- widely recognized as important predators that can iting abundance of gastropods, barnacles and bi- limit distribution and abundance of prey (Knudsen valves, in both oyster reef (McDermott 1960; Lee 1960; Menge 1976; Bertness et al. 2003) and, at and Kneib 1994; Meyer 1994) and seagrass (Whet- times, act as keystone predators in trophic cas- stone and Eversole 1981; Zieman 1982; Holmquist et al. 1989) systems; their role in salt marshes has * Corresponding author; e-mail: [email protected] not been explored (but see Seed 1980 for lab ex- ² Current address: Department of Ecology and Evolutionary periments). Mud crabs are widely distributed in Biology, Brown University, Providence, Rhode Island 02906. ³ Current address: Department of Wildlife and Fisheries Sci- subtidal habitats and are often locally abundant, at 22 ences, Texas A & M University, College Station, Texas 77843- times reaching densities up to 80 ind m (Kneib 2258. and Weeks 1990; Meyer 1994). Q 2004 Estuarine Research Federation 188 Top-down Control by Mud Crabs 189 In salt marshes along the Mid-Atlantic coast of openings, distance between openings, and num- the United States, the dominant Xanthid is the ber, size, and sex of occupants and co-inhabitants. black-clawed mud crab, Panopeus herbstii (Daiber Other mud crabs found included the depressed or 1982; Williams 1984). Studies on oyster reefs sug- ¯at-backed mud crab, Europanopeus depressus, and gest this crab is primarily carnivorous, consuming the oyster mud crab, Neopanopeus sayi, but these molluscs, crustaceans, and annelids (McDermott were in insigni®cant densities (,0.4 ind marsh21). 1960; Meyer 1994). Its distribution in salt marshes Studies have shown that juvenile and adult Pan- is generally thought to be limited to creek banks opeus associate with live oysters and oyster shells in tall-form Spartina alterni¯ora (salt marsh cord- (Lee and Kneib 1994; Meyer 1994). To test wheth- grass) zones and, in creeks speci®cally, in intersti- er distribution of oysters in the tall Spartina zone tial spaces of oyster reefs (Teal 1958; Daiber 1982; (the zone where oysters are most abundant) affects Lee and Kneib 1994; but see Seed 1980). In Vir- Panopeus abundance, we recorded percent cover of ginia marshes, we observed that Panopeus takes up oysters in each 1-m2 quadrat in randomly selected residency (in lairs) throughout the entire extent of subset of sites (Hog Island, Virginia; Cobb Island, the lower marsh, consumes resident invertebrates Virginia; and Tar Landing, North Carolina, marsh- and ®sh, and preys on the plant-grazing snail, Lit- es; n 5 10 quadrats per tall zone per site). To assess toraria irrorata (Silliman and Zieman 2001; Silliman percent cover of oyster shell, we used a quadrat and Bertness 2002). To quantify these observa- divided into 100 equally-sized parts, and character- tions, and to test their generality and potential ized each cell as empty, half full, or full. The hun- community consequences, we investigated distri- dred cells were summed to provide an estimate of bution and abundance of Panopeus in eight salt cover for the 1 m2 quadrat. In a preliminary study, marshes along the mid-Atlantic seashore, potential we compared this method with displacement vol- food-web interactions through lair excavation and ume of oysters (Meyer 1994) and found the per- lab feeding trials, and the effect of crab predation cent cover and volume method in salt marshes on the intensity of marsh plant-grazer interactions. were highly correlated, so we analyzed only per- We hypothesized that contrary to present notions, cent cover estimates. A linear regression model was Panopeus is widely distributed and abundant used to relate percent cover of oyster shells to den- throughout East Coast salt marshes and that by sity of Panopeus. suppressing densities of plant-grazing snails, black- clawed mud crabs indirectly facilitate Spartina alter- POTENTIAL FOOD-WEB INTERACTIONS ni¯ora growth. To identify potential food-web interactions be- tween Panopeus and marsh fauna, we counted and Materials and Methods identi®ed shells in the middens of lairs. We also estimated density of live epifaunal macro-inverte- DISTRIBUTION AND ABUNDANCE SURVEY brates in each survey-quadrat and examined how We surveyed mud crab abundance, lair charac- middens compared to prey availability. teristics, and midden (i.e., shell refuse from past To further examine potential food-web interac- predation encounters) composition in eight tions, we starved mud crabs (n 5 10 for each run, marshes along the Mid-Atlantic seaboard, from all ;30±40 mm in carapace width) for 48 hr and Delaware to North Carolina, in the summer of then, in the laboratory, presented them with one 1998 (North Carolina: Tarlanding Marsh near At- potential prey item in no-choice predation exper- lantic Beach; Virginia: Cobb Island, Chincoteague iments. Organisms included in trials were the most Island, Hog Island, Parramore Island, and Rac- abundant potential prey in the marsh (see Table coon Island; Maryland: Assateague Island; Dela- 1). Each crab and prey item were housed in a 500 ware: Bethany Spit). All sites were exposed to full ml square (15 3 15 3 4 cm) plastic container with strength seawater (29±34½). Within each marsh, recirculating seawater to a depth of 3 cm. This lev- we randomly threw ten 1-m2 quadrats in each of el approximated water depth on the marsh surface three Spartina height-form zones (tall, intermedi- when crabs are most actively feeding (just after and ate, and short-form), and enumerated density of before ¯ood tide, Teal 1962). Containers were mud crabs . 5 mm (carapace width) by examining capped with a perforated lid. Both water level and crab species in all visible burrows (using a stick container architecture prevented potential prey probe inserted behind the burrow to coax crabs to items from employing escape responses. Each feed- the surface) and number of crabs in mussel and ing trial ran for 8 hr and afterwards containers oyster clumps through excavation with shovel. Bi- were examined to assess predation. Because we valve clumps were carefully disassembled and were interested only in identifying potential food- rinsed with seawater to dislodge all organisms. Lair web interactions, we did not use statistics to sepa- attributes included depth, number, and size of rate species effects.
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