22000088 O.J. Pung, CS.BO.U GTrHinEsAteSaTdE, RKN. KNeArTstUeRn,A aLnIdS TC.L. Edenfield 7(4):717–772187 Spatial Distribution of Hydrobiid Snails in Salt Marsh along the Skidaway River in Southeastern Georgia with Notes on their Larval Trematodes Oscar J. Pung1,*, C. Brad Grinstead1, Kraig Kersten2, and Catherine L. Edenfield3 Abstract - Populations of hydrobiid snails and their larval trematode parasites in salt marsh along the Skidaway River were studied to determine their distribution. Additionally, the prevalence of larval trematodes infecting the snails was examined to investigate definitive host distribution patterns on the Skidaway River and to identify sites for future studies on second intermediate host susceptibility to trematode infection. To do so, surface sediment and vegetation were collected at low tide from 0.5-m2 quadrats along 20 vertical transects beginning in high marsh at the forest edge and salt meadow, passing through high, medium, and low Spartina alternifl ora zones, and ending in the low marsh at creekbed level. Samples were filtered through sieves to concentrate snails, which were then counted and identified. Two species of hydrobiid snails, Spurwinkia salsa (4201 specimens) and Onobops jacksoni (136 specimens) were collected. Hydrobiid snails were found in sediments and on plant stems throughout the S. alternifl ora zones, and snail density was greatest in the higher Spartina zones. Sediments from the 3 Spartina zones differed with respect to percent sand, but not percent silt or clay. Salinity and chlorophyll-a levels did not differ between the 3 Spartina zones, and there was no relationship between hydrobiid abundance and the abundance of other snail species. The mean prevalence of trematode infection in S. salsa and O. jacksoni snails was 5.5% and 7.5%, respectively. Snails were infected most commonly with either an oculate monostome, possibly the heterophyid Phagicola diminuta, or 2 types of xiphidiocercariae, one of which likely includes the microphallid Microphallus turgidus. No infected snails were found in over half of the collection sites, and the distribution of infected snails was patchy and unpredictable. Introduction Hydrobiid snails are common inhabitants of soft substrate tidal marshes along the coast of the southeastern US (Heard et al. 2002, Hershler and Thompson 1992). Perhaps as a result of their small size, often only a few mm in length, hydrobiids are inconspicuous and frequently overlooked. Hydrobiids snails are herbivores that graze on diatoms and other microalgae found on the surface of intertidal sediments and vegetation (Jensen and Siegismund 1980). Despite the fact that these deposit feeders 1Department of Biology, Georgia Southern University, PO Box 8042, Statesboro, GA 30460. 2Department of Biology, Armstrong Atlantic State University, Savannah, GA 31419. 3Department of Biology, Berry College, Mount Berry, GA 30149. *Corresponding author - opung@georgiasouthern.edu. 718 Southeastern Naturalist Vol. 7, No. 4 are a significant component of intertidal communities, their abundance and spatial distribution patterns in the extensive salt marshes of southeast Georgia have not been examined thoroughly. This knowledge may prove important in future evaluations of the impact of real estate development and other human activities that now threaten the coastal ecosystems of Georgia (Kleppel et al. 2006). Hydrobiid snails are also noteworthy because they serve as first intermediate hosts for a variety of digenetic trematodes. For example, over 50 kinds of trematode larvae have been described in hydrobiids collected on the coast of France (DeBlock 1980). These parasites, in turn, utilize economically and ecologically important crustacean and vertebrate organisms as second intermediate and definitive hosts. Some of the trematodes that infect hydrobiids in the southeast have been identified (Font et al. 1984; Heard 1970, 1976; Heard and Overstreet 1983). One of particular interest to us is Microphallus turgidus Leigh. This parasite is abundant in a variety of hosts in brackish water marshes along much of the coast of the southeastern US. Several hydrobiid snail species, including Litterodinops monroensis Frauenfeld, serve as first intermediate host for this parasite and grass shrimp, Palaemonetes Heller, are the second intermediate hosts in coastal marshes (Heard and Overstreet 1983). Many different crustacean-eating birds and mammals, including Rallus longirostris Boddaert (Clapper Rail) and Procyon lotor Linnaeus (Raccoon), are definitive hosts (Leigh 1958, Heard 1970). Work performed in our laboratory indicates that the geographic distribution of this parasite in Palaemonetes pugio Holthuis (Daggerblade Grass Shrimp) may be affected by salinity levels (Pung et al. 2006) and that infected P. pugio are more susceptible to predation (Kunz and Pung 2004). The primary goal of the present study was to determine the spatial distribution of hydrobiid snails along the readily accessible tidal marshes of the Skidaway River in Georgia and to investigate the possibility that other biotic and abiotic parameters characteristic of the collection sites would be of predictive value with respect to snail abundance. Our secondary goal was to examine the distribution and prevalence of trematode larvae infecting the snails as a means of examining the distribution patterns of definitive hosts and to identify potential collection sites for use in future studies concerning the biology of the parasite M. turgidus. Methods Hydrobiid snails were collected during low tide in salt marsh along the Skidaway River adjacent to Skidaway Island and the Isle of Hope southeast of the city of Savannah, GA from May 2004 through July 2004. The Skidaway is a subtropical tidal river (typical tidal range is 2–3 m), a portion of which is dredged for the Intercoastal Waterway. As the tide rises, water fl ows 2008 O.J. Pung, C.B. Grinstead, K. Kersten, and C.L. Edenfield 719 into the Skidaway River from the Savannah River system via the Wilmington River in the north and from the Ogeechee River via the Vernon River in the south. The Skidaway River is surrounded by extensive salt marshes dominated by Spartina alternifl ora Loisel (Salt Marsh Cordgrass). Hydrobiid snails were collected from sediment and S. alternifl ora stems along 20 vertical transects (from 31°59'12"N, 81°01'47"W in the north to 31°56'38"N, 81°03’55"W in the south; Fig. 1) through the intertidal zone beginning in the high marsh and ending in low marsh at creekbed level. At Figure 1. Hydrobiid snail collecting sites along the Skidaway River southeast of the city of Savannah, GA. Snails were collected within 0.5-m2 quadrats along vertical transects extending through the intertidal zone beginning in the high marsh and ending in low marsh or at creekbed level. 720 Southeastern Naturalist Vol. 7, No. 4 15 of these transects, snails were collected within a 0.5-m2 quadrate in each of 3 S. alternifl ora zones (high, middle, and low), and at 5 sites, snails were collected only in the high zone. The high zone was defined as areas close to the salt meadow or forest edge with firm sediment and short Spartina (mean stem length = 42 cm; Table 1). The middle Spartina zone consisted of softer sediment and medium height Spartina (mean stem length = 64 cm). The low zone was immediately adjacent to tidal creeks and was characterized by tall Spartina stems (mean stem length = 94 cm) and very soft, loose sediment. Samples were also collected from salt meadow and creekbed sediments at 5 transects. Standing water temperatures were recorded, and salinity was measured with a handheld temperature-compensated refractometer (Fisher Scientific, Atlanta, GA). Within each quadrat, plant stems and the top 1 cm of sediment were collected. The length of 10 Spartina stems from each quadrat were measured. Seawater was used to filter sediments through a series of 21 cm (8 inch) diameter brass sieves (ASTM E-11 Specification, Fisher Scientific) stacked in order of decreasing mesh-size order (2, 1.8, 0.71, and 0.6 mm). All vegetation was agitated in a bucket containing seawater to dislodge snails, and the water was then poured through sieves. Material collected in the 1.8-, 0.71-, and 0.6-mm sieves was transported to the laboratory in seawater and examined under a dissecting microscope (10X magnification). Snails were counted, removed for identification, and examined for trematode infection. Snail identification was based on shell and verge morphology (Heard et al. 2002, Hershler and Thompson 1992). Sediment grain size analyses were performed using the protocol described by Bouyoucos (1962). One sediment sample from each quadrat was Table 1. Distribution of the hydrobiid snail Spurwinkia salsa (Salt Marsh Hydrobe) in Spartina alternifl ora (Salt Marsh Cordgrass) marsh along 20 transects on the Skidaway River in Georgia. Surface sediment chlorophyll-a levels and sediment characteristics in different Spartina zones are included. Values represent means ± 1 s.d. A total of 4201 S. salsa snails were collected. In addition, a few specimens of Onobops jacksoni (Fine-lined Hydrobe) (n = 136) were found in all three Spartina zones. Spartina alternifl ora zone High Middle Low Number of snails/0.5 m2 113.1 ± 116.2 135.1 ± 144.1 27.9 ± 42.3A Spartina stem length (cm)B 42.0 ± 8.9 64.1 ± 19.5 94.0 ± 13.5 Chlorophyll-a (mg/m2) 94.7 ± 14.3 85.3 ± 14.3 108.1 ±15.0 Sediment (percent) SandC 70.7 ± 26.4 53.0 ± 33.0 33.8 ± 19.4 Silt 8.1 ± 9.8 12.0 ± 9.6 17.4 ± 7.5 Clay 21.1 ± 16.8 35.1 ± 24.7 48.8 ± 15.7 ASpurwinkia salsa snail density in the low Spartina zone significantly lower than snail density in high (P = 0.01) and middle Spartina zones (P = 0.01). BSpartina stem length significantly different from zone to zone (P < 0.0001). CSignificant difference between Spartina zones with respect to percent sand (P = 0.02). 2008 O.J. Pung, C.B. Grinstead, K. Kersten, and C.L. Edenfield 721 dried, ground using a mortar and pestle, and sifted through a 2-mm sieve. A 50-g portion was mixed with 100 ml of 5% sodium metaphosphate, diluted with distilled water to a final volume of 300 ml, and shaken for 24 h (125 rotations/min). Samples were then diluted to a volume of 1 liter in a graduated cylinder and mixed by inversion. Temperature and concentration scale (ASTM 152H) soil hydrometer (Fisher Scientific) readings were recorded 40 sec and 2 h after inversion and subtracted from control (0.5% sodium metaphosphate) readings for calculations. To measure chlorophyll-a levels, triplicate samples of the top 1 cm of sediment were collected at each site in cut-off 10-cc syringe barrels and kept on ice in the dark until frozen. Subsequent pigment extraction steps were performed in a darkened room. Samples were thawed, ground with a mortar and pestle for 3 min in 90% acetone, transferred to 15-ml tubes, refrigerated for 16–18 h, and then centrifuged for 5 min at 1200 x g. The absorbance of the extract was determined in a Spectronic 21D spectrophotometer (Spectronic Instruments, Inc., Rochester, NY) at 750 nm and 664 nm before and after acidification with 1 N HCl to account for phaeopigments (Lorenzen 1967). Equations for chlorophyll-a calculation were modified for benthic microalgal concentration following Colijn and Dijkema (1981). To determine the prevalence of larval trematode infection, individual snails were incubated up to 5 wk at 30 °C in the wells of 24-well tissue culture plates (Falcon, Becton-Dickinson, Franklin Lakes, NJ) filled with brackish water (salinity = 23 ppt). Wells were examined twice a week with an inverted microscope for the presence of cercariae, after which snails were given fresh seawater and fed microalgae. In some cases, infection was determined by microscopic examination of individual snails crushed under a coverslip. Live cercariae were stained with 0.01% neutral red, examined using a compound microscope, and identified to type using Heard (1976), Deblock (1980), Heard and Overstreet (1983), and Ostrowski de Núñez (1993). Specimens were gently heat-fixed with no coverslip pressure for measurements. Due to low sample sizes, analyses were not performed on data collected for Onobops jacksoni Bartsch (Fine-lined Hydrobe). The nonparametric Kruskal-Wallis test was used to compare numbers of Spurwinkia salsa Pilsbry (Saltmarsh Hydrobe) snails between marsh zones. Mann-Whitney U-tests were used to identify pairs of means that were significantly different, and probability values were adjusted for multiple mean comparisons (Wright 1992). One-way analyses of variance (ANOVA) were used to compare salinity, S. alternifl ora stem length, and chlorophyll-a levels across marsh zones, and the Tukey-Kramer honest significant difference test was used to identify pairs of means that were significantly different. Friedman’s 2-way nonparametric analyses were used to determine if there were differences in numbers of S. salsa across sediment types and in parasite prevalence across 722 Southeastern Naturalist Vol. 7, No. 4 marsh zones. The relationship between hydrobiid snail density and salinity and between hydrobiid density and the density of Nassarius obsoletus Say (Eastern Mudsnail) and Littoraria irrorata Say (Marsh Periwinkle) were examined using Spearman’s Rho correlation. Results Two species of hydrobiid snail were collected: Spurwinkia salsa and Onobops jacksoni. Most of the snails collected were S. salsa (4201 specimens, 97% of total), while 136 specimens of O. jacksoni were found. Both species of snails were found in all 3 Spartina zones. At low tide, 88.5% of the snails were collected from sediment and the remainder from Spartina stems. The density of S. salsa snails differed between zones (Kruskal-Wallis H = 10.9, df = 2, P = 0.004). Fewer snails were found in the low Spartina zone than in either the high zone (U-test: S = 244.5, Z = 2.6, P = 0.03) or the middle zone (U-test: S = 159.5, Z = -3.0, P = 0.01; Table 1). No hydrobiid snails were found in salt meadow, and only 1 snail was found in creekbed sediments (5 creekbed quadrats examined). Chlorophyll- a levels did not differ between the 3 Spartina zones (ANOVA: df = 2, 34, F-ratio = 0.6, P > 0.5). Spartina zones differed with respect to percent sand (Friedman’s χ2 = 7.82, df = 2, P = .02), but not percent silt (Friedman’s χ2 = 3.4, df = 2, P > 0.2) or clay (Friedman’s χ2 = 5, df = 2, P > 0.05) (Table 1). Salinity, which averaged 29.5 ± 2.4 ppt (range = 29–35 ppt), did not differ between zones, and there was no relationship between hydrobiid density and salinity. There was no correlation between S. salsa density in the Spartina zones and the density of other snails (L. irrorata: rs = 0.32, P = 0.06; N. obsoletus: rs = 0.09, P = 0.78). Spartina stem lengths differed from zone to zone (ANOVA: df = 2, 41, F-ratio = 44.2, P < 0.0001). A total of 1035 S. salsa snails and 40 O. jacksoni snails were examined for trematode infection. A total of 118 S. salsa snails (11.4%) were trematode- infected, and parasite prevalence did not differ between zones. Three O. jacksoni snails (7.5%) were infected. The distribution of infected snails was patchy; the mean prevalence of infection in S. salsa was 5.5% ± 11.8 and ranged from 0% (at 56% of collection quadrats) to as high as 66% at a single quadrat. The component community of hydrobiid parasites consisted of 4 types of larval trematode. Sixty-four S. salsa snails were parasitized with oculate monostome cercariae (mean prevalence = 2.2% ± 6.6, range = 0–39.4%). These parasites were characterized by a pair of eyespots in the anterior one-third of the body, oral sucker with lip-like spines, no ventral sucker, and paired penetration glands in 2 diagonal rows on each side of the body. The body was lanceolate when extended, broadly so at the anterior, and pyriform when retracted. The body of heat-fixed specimens measured 70–80 μm long by 42–45 μm wide. The tail was 75–90 μm in length, with a small posterior spine. 2008 O.J. Pung, C.B. Grinstead, K. Kersten, and C.L. Edenfield 723 Fifty-six S. salsa snails were infected with either of two types of xiphidiocercariae (hereafter referred to as Type I and Type II). Two O. jacksoni snails were infected with Type I and one with Type II xiphidiocercariae. Both types had simple tails and lacked eye spots and ventral suckers. The Type I xiphidiocercariae (mean prevalence = 1.3% ± 4.7, range = 0–28.7%) were characterized by a narrow stylet and 4 pairs of penetration glands extending into the posterior of the parasite. Type II xiphidiocercariae (mean prevalence = 2.2% ± 4.8, range = 0–21.3%) had a broad stylet, 2 pairs of anterior penetration cysts and 2 pairs of lighter staining glands extending into the posterior of the body. The body size of both xiphidiocercariae was similar: 100–122 μm long by 25–32μm wide. The tail measured 115–133 μm in length. Additionally, a single S. salsa snail was infected with both the oculate monostome and Type II xiphidiocercariae, and one specimen of S. salsa was infected with sanguinicolid trematode larvae. Discussion Spurwinkia salsa was the most abundant snail collected in the Skidaway River marshes. This hydrobiid is found along the Atlantic coast from Maine in the north to Cumberland Island, GA in the south (Hershler and Thompson 1992). In Massachusetts and Maine, S. salsa is reported to inhabit various low-salinity habitats including high-marsh pools, sediments between marsh grass stems, and channel and creek bottoms (Davis et al. 1982). In contrast, we collected S. salsa primarily on and amongst Spartina stems and in small, open mudfl ats within the Spartina zones. We found virtually no hydrobiids in creekbeds, and the salinity at all of our collection sites was relatively high (i.e., ≥29 ppt). The spatial distribution patterns of deposit-feeding snails in softsubstrate intertidal communities are not fully understood and likely due to complex interactions between numerous biotic and abiotic factors (Kneib 1984). These include inter- and intraspecific competition (Levinton 1985, Levinton et al. 1985), predation (Joyce and Weisberg 1986, Rochette and Dill 2000), salinity (De Francesco and Isla 2003, Fenchel 1975), water flow (Levinton et al. 1995), food abundance (Drake and Arias 1995, Levinton 1985), and sediment type and particle size (Bick and Zettler 1994, Forbes and Lopez 1990, Levinton and DeWitt 1989). We collected hyrdobiids throughout the Spartina zones of the Skidaway River marshes and found that hydrobiid density is greatest in the high and middle Spartina zones. Based on our current findings, we are not able to explain this apparent zonal preference. Chlorophyll-a levels and salinity did not differ between Spartina zones, and there was no relationship between hydrobiid density and that of other snails. We did find that sediment composition, at least with respect to percent sand, varied from zone to zone. Hydrobiid 724 Southeastern Naturalist Vol. 7, No. 4 growth rates may be greater on sand than on smaller size sediments (Forbes and Lopez 1990), and snail abundance has been positively correlated with increasing sediment grain size in at least one instance (Bick and Zettler 1994). Consequently, maximal snail growth on the sandier sediments of the high and middle Spartina zones along the Skidaway might account for the higher densities of adult snails we observed. However, other investigators have shown that hydrobiid snails feed fastest on intermediate-size particles (i.e., particles smaller than sand) that may also have greater diatom abundance (Levinton and DeWitt 1989). These sorts of analyses are complicated by the fact that natural sediment consists of a mix of different size-class particles and the relationship between sediment size and microalgal abundance is not clear (Cahoon et al. 1999). Finally, since predation can affect snail abundance and distribution (Joyce and Weisberg 1986, Rochette and Dill 2000), greater hydrobiid density in the high and middle Spartina zones could simply reflect the fact that these zones are inundated with water for less time than the low Spartina zone and adjacent creekbeds and that, as a result, snails in the higher zones are exposed to swimming predators, such as crabs and juvenile fish, for shorter periods of time. We have no evidence to support this hypothesis. Hydrobiid snails and other gastropods are obligatory first intermediate hosts for most digenetic trematodes and, as such, are considered keystone species for these parasites (Esch et al. 2001). Trematodes, in turn, have dynamic effects on gastropod communities and can infl uence host reproductive capacity, distribution, and behavior (Curtis 1987). The component community of larval trematode species in hydrobiid snails in the Skidaway River marshes comprises at least 4 types of cercariae. This trematode community is smaller than that observed in other marine systems (Al-Kandari et al. 2000, Deblock 1980, Kube et al. 2002). The size of these communities varies both spatially and temporally (Kube et al. 2002) and is infl uenced by multiple factors. Perhaps primary among those is the presence and abundance of infected definitive hosts (Esch et al. 2001, Gerard 2001). The definitive hosts for the parasites we observed include many species of crustacean- and fish-eating birds and mammals. These kinds of hosts are common in the Skidaway marshes, but their density is low and their distribution sporadic. As a result, it is not surprising that the parasite distribution in hydrobiid snails in Skidaway River marshes is variable. The Type II xiphidiocercariae observed in S. salsa resemble cercariae of the microphallid trematodes M. turgidus and Microphallus basodactylophallus Bridgman as described by Heard and Overstreet (1983). As is true of most trematode cercariae, they are best identified to species level by experimental infection of second intermediate hosts. Palaemonetes spp. grass shrimp are second intermediate hosts of M. turgidus, and Callinectes sapidus Rathbun (Blue Crab) is a second intermediate host of M. basodactylophallus 2008 O.J. Pung, C.B. Grinstead, K. Kersten, and C.L. Edenfield 725 (Heard and Overstreet 1983). As part of a recent host-susceptibility study, we infected juvenile P. pugio shrimp with Type II xiphidiocercariae found in Skidaway River hydrobiids (data not shown). Thus, it is probable that a percentage of the Type II xiphidiocercariae observed in the present study are M. turgidus. We did not attempt to identify the Type I xiphidiocercariae. Other microphallid trematodes reported to infect hydrobiid snails in the southeast include Maritrema prosthometra Deblock and Heard that utilizes O. jacksoni and other hydrobiids as first intermediate host, Uca minax LeConte (Redjointed Fiddler Crab) and other fiddlers as second intermediate hosts, and the Clapper Rail as definitive host (Heard 1976). Hydrobiid snails in the southeast are also reported to be infected with heterophyid trematode larvae. For example, Ascocotyle gemina Font, Heard, and Overstreet utilizes Litterodinops monroensis Frauenfeld as its hydrobiid host, cyprinodontid and poeciliid fishes as second intermediate hosts and the Clapper Rail and other fish-eating birds as definitive host (Font et al. 1984). The heterophyid we observed in S. salsa snails resembles Ascocotyle (Phagicola) diminuta Stunkard and Haviland as described by Ostrowski de Núñez (1993). The reported molluscan hosts of this parasite include the hydrobiids O. jacksoni and Littoridinops tenuipes Couper (Henscomb Hydrobe), metacercariae encyst on the gills of brackish water cyprinodont fishes, and the adults are common in coastal herons, Raccoons, and Clapper Rails (Heard 1970). In conclusion, hydrobiid snails can be collected readily from sediments and plant stems in the easily accessible, higher Spartina zones along the Skidaway River, but we are unable to explain this distribution pattern. The mean prevalence of trematode-infected hydrobiids in these localities is low, and their distribution unpredictable at present. In order to obtain M. turgidus cercariae for future work, we are investigating ways to infect hydrobiids in the laboratory and surveying the marsh for locations frequently visited by potential avian and mammalian definitive hosts. Acknowledgments We thank C. Ray Chandler for assistance with statistical analyses, Risa Cohen for demonstrating chlorophyll-a and sediment grain size determination, Lance Durden for reviewing the manuscript, Richard Heard and Robert Hershler for advice on snail identifications, Edward D. Brown for assistance with sample collection, the anonymous reviewers and the guest editor for their helpful suggestions and criticisms, and the Skidaway Institute of Oceanography (SKIO) for permitting access to collection sites on Skidaway Island. We are grateful to Mike Robinson of SKIO for mapping our collection sites and for sharing his extensive knowledge of the Skidaway River and its marshes. This study was supported by a grant to O.J. 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