The Society for Integrative and Comparative Biology
Long Term Monitoring of Grass Shrimp Palaemonetes spp. Population Metrics at Sites with Agricultural Runoff Influences1,,2
1 Cooperative Oxford Laboratory, Center for Coastal Environmental Health and Biomolecular Research, National Oceanic and Atmospheric Administration, National Ocean Service, 904 South Morris Street, Oxford, Maryland 21654
2 Center for Coastal Environmental Health and Biomolecular Research, National Oceanic and Atmospheric Administration, National Ocean Service, 219 Fort Johnson Road, Charleston, South Carolina 29412
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SYNOPSIS |
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Rising concern over pesticide usage near estuarine systems and evidence of physical and physiological impacts on estuarine organisms have strengthened the need to better identify the ecological effects of nonpoint source runoff. Grass shrimp, Palaemonetes spp., are ecologically important and abundant marsh inhabitants that may be impacted by anthropogenic contamination. Populations of grass shrimp were sampled monthly, over a period of ten years, at four sites in South Carolina with varying upland land use characteristics. Spatial and temporal trends in grass shrimp densities were noted over time and between sites. Agricultural and golf course land usage corresponded with decreased grass shrimp population levels, overall shrimp size, and percentage of gravid females. Conservation methods, such as the use of best management practices (BMPs) and integrated pesticide management (IPM) at agricultural fields, corresponded with increased grass shrimp population density.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Along the southeastern coast of the United States, grass shrimp Palaemonetes spp. populations can constitute as much as 56% of the overall annual pelagic macrofaunal density in tidal creeks (Scott et al., 1994
). They are important consumers and serve as a key prey item for many ecologically and recreationally important crustacean and fish species (Welsh, 1975; Williams, 1984). In bioassay studies, a number of contaminants, including pesticides, polycyclic aromatic hydrocarbons (PAHs), and metals have been shown to impact grass shrimp growth, size, reproductive capacity, and survival (Burton and Fisher, 1990; Key et al., 1998; Key and Fulton, 1993; Lee et al., 2000; McKenney et al., 1998; Wirth et al., 1998, 2002). Some of these laboratory findings positively correlate with field biomonitoring assessments of grass shrimp population metrics (Scott et al., 1994). Recent research suggests that some chemical contaminants are able to affect reproductive hormone function in grass shrimp (Oberdorster et al., 2000).
Urban and agricultural use of land adjacent to estuaries and their tributaries have been shown to increase the potential for contaminant influx to the environment through nonpoint source runoff (Fulton et al., 1993; Scott et al., 1994). In addition, industrial and urban land use has been positively correlated with poor water quality, such as extreme salinity fluctuations and severe, prolonged hypoxia (Lerberg et al., 2000). Some best management practices (BMP), such as drainage to retention ponds, and integrative pest management (IPM), which attempts to use more specific and less persistent crop pesticides, may be useful to help abate runoff of contaminants from agriculture.
Several sites for long term monitoring of grass shrimp populations in waters adjacent to agricultural lands have been established in South Carolina tidal creeks (Fig. 1). One site (CTL) is on the western branch of Leadenwah Creek (32°38.930'N, 80°13.340'W) with several single-family dwellings nearby and is bordered mostly by wooded upland. The TRT site, on the eastern branch of Leadenwah Creek (32°39.360'N, 80°10.360'W), is surrounded by vegetable crop fields (primarily tomato). Cultivated fields (primarily tomato) have historically surrounded the KWA site, which is on a narrow, straight creek that extends off the Kiawah River (32°36.320'N, 80°08.470'W). The sample site NIOL is located on Clambank Creek in North Inlet, a relatively pristine NOAA National Estuarine Research Reserve and Sanctuary (33°21.010'N, 79°11.280'W) where relatively unaltered, forested upland surrounds most of the creek and adjacent areas.
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A chemical characterization of these sites was conducted in the late 1980s and early 1990s (Finley et al., 1999
; Jenkins, 2001). Focusing on those chemicals for which criteria have been generated, chemical contaminant levels were compared to sediment quality criteria predictive of threshold effects (ERL) and probable effects (ERM) (Hyland et al., 1999) (Table 1). Contaminant levels above the ERL were found only at KWA for arsenic and DDT. No ERM violations were detected. Measurements of pesticide levels in creek waters and sediments following storm events were also taken (Scott et al., 1994) (Table 2). Samples taken from CTL had only negligible levels of pesticides, possibly carried in with tidal waters. Significant levels of the pesticides fenvalerate and deltamethrin were detected at the TRT site samples, corresponding to numerous pesticide related fish kills that had occurred at the TRT site prior to the start of this study (Scott et al., 1994) and to mortalities of grass shrimp in situ bioassays (Scott et al., 1999). After the completion of retention ponds and better regulation of pesticide application regimes at the TRT site, analyses of water and sediments from this site revealed no detectable concentrations of pesticides (Finley et al., 1999). In 1999, agricultural practices around TRT were discontinued and residential development with dock construction began upstream. Relatively high levels of insecticides, particularly azinphosmethyl, were detected in water at the KWA site (Table 2) and pesticide related grass shrimp and fish kills occurred in the late 1980s (Fulton et al., 1993) and early 1990s (Finley et al., 1999). No BMP or IPM efforts were employed on these fields. In 1997, agricultural activities were abandoned at KWA and in 1998 the upland on the eastern side of the creek was heavily altered to construct a golf course, which opened in the fall of 2000. A number of water and sediment contaminant chemistry analyses showed no biologically significant levels of any contaminants at the NIOL site (Jenkins, 2001).
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Finley et al. (1999)
examined grass shrimp populations from these sites from April 1993 to March 1994. They found that the densities of grass shrimp at the agriculturally influenced KWA site were 50% lower than those at the NIOL site, and that KWA had the highest numbers of gravid females. However, they were limited in their analyses by only having one year of data. The objectives of this current study were to compile and analyze longer term data from these monitoring sites in order to examine grass shrimp population dynamics over long periods of time and the potential long term impacts of nonpoint source runoff (principally from agricultural) on these dynamics. |
MATERIALS AND METHODS |
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SYNOPSISINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Grass shrimp populations were sampled monthly from four estuarine tidal creek sites in South Carolina (Fig. 1). From 1991 to 2000 grass shrimp populations were sampled by pushnetting from the four long term monitoring sites CTL, TRT, KWA, and NIOL. All creeks were of relatively similar size (width) and general topography.
Sampling by pushnet was conducted along three consecutive 25 m stretches of each creek. Pushnets with mouth openings of approximately 25 cm high by 40 cm wide (1,009 cm2) and mesh size of 4 mm were used. Tows were made by walking along adjacent creek banks during ebbing tides, concurrent with the fall of the waterline out of the marsh and into the main channel of the creek. The number of grass shrimp was counted and the total weight was measured in grams. Different species of grass shrimp were not identified or separated from one another at this stage.
Starting in 1993, all grass shrimp, after being counted and weighed in the laboratory as whole samples, were examined for species and sex determinations. Species identification was based on the morphologies of the rostrum and the 5th pleura (Holthius, 1952). Sex determination was based on the morphology of the first pleopod and brood pouch if present (Holthius, 1952). The length (in mm) and weight (in mg) of each individual shrimp were measured and the presence of any ectoparasites was recorded. The number of eggs per gravid female was determined by gently removing the eggs from the clutch and counting them under the dissecting microscope. Results for each sampling stretch were averaged to predict grass shrimp population measures for site and month.
Concurrent with grass shrimp sampling, water quality parameters [temperature (°C), salinity (ppt), dissolved oxygen (mg/L and %), and pH] were measured using a YSI 55 (YSI Environmental, Yellow Springs, Ohio) meter and pH meter (Cole Parmer Inst. Co., Vernon Hills, Illinois).
Statistical comparisons were made on log transformed density values from each replicate. Grass shrimp population metrics were compared within sites over time and between sites by ANOVA and Tukey's multiple comparison test following checks of normality and variance. Comparison of water quality data to grass shrimp densities was performed with a step-wise multiple regression. Statistical differences were considered significant when P 
0.05. All statistical tests were conducted using SAS software (SAS Institute, Cary, North Carolina).
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RESULTS |
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Palaemonetes pugio was the primary grass shrimp in all samples, constituting 99.5% of all grass shrimp sampled, with Palaemonetes vulgaris accounting for the other 0.5%. The average grass shrimp density for all years of pushnetting data (1991–2000) ranged from 40.0 shrimp/m3 at NIOL to 7.7 shrimp/m3 at KWA (Fig. 2). The average grass shrimp density at NIOL was twice as great as any other site. Grass shrimp density at CTL was significantly higher (P < 0.0001) than that for both TRT and KWA.
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Annual Palaemonetes spp. densities at the TRT and KWA sites were significantly lower (P < 0.05) than both NIOL and CTL for most years. NIOL had the highest grass shrimp density of all sites for all sample years, and KWA had the lowest densities for six of the ten years (Fig. 3). The density of Palaemonetes spp. at KWA was significantly lower (P = 0.014) after the conversion of the surrounding upland from agricultural fields to a golf course (1999 and 2000) than before (1991 to 1998) (Fig. 4). Population densities at NIOL and CTL were statistically similar for eight of the ten years.
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The length measurements of the grass shrimp collected at the four sites showed significant differences between sites (Fig. 5). When all length data was pooled for each site for all years, NIOL shrimp were significantly longer and TRT shrimp were significantly shorter (P < 0.05). Overall, length estimates for TRT were significantly shorter (P < 0.05) than those for CTL and NIOL during five of the ten sampling years, and KWA estimates were significantly shorter for three years (P < 0.05). Grass shrimp lengths at KWA were significantly shorter (P < 0.0001) for shrimp collected after the conversion of the upland to a golf course than in the previous years. Weight estimates showed very similar results to length estimates indicating trends in overall shrimp size (Fig. 5).
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Sex ratio analyses revealed a range from an approximately 2:1 male to female ratio at NIOL to a ratio of approximately 1:1 male to female ratio at TRT (Table 3). NIOL had the greatest percentage of gravid females in the population (5.1%) while KWA had the lowest (3.3%) (Table 3). At NIOL, 20% of the average annual number of females were gravid, whereas only 7.2% were gravid at the TRT site. The highest percentage of gravid females was about 12.5% at NIOL for 1995 and the lowest percentage was 0.5% for TRT in 2000. Conversely, NIOL had the lowest average annual percent of total females (gravid and non-gravid) (30.6%) and the TRT site had the highest average annual percent of total females (50.1%). Sex ratios for NIOL in the present study were similar to those found by Sikora (1977)
in which grass shrimp populations in creeks very close to the NIOL site were about 60% male annually with a high of 79% in August.
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Numbers of eggs per gravid female were compared between sites for all years pooled. Gravid females at KWA had significantly lower (P = 0.0041) numbers of eggs per clutch than gravid females at both the CTL and NIOL sites (Fig. 6).
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The primary ectoparasite counted was the bopyrid isopod, Probopyrus pandalicola. The incidence of ectoparasites in grass shrimp from the four creeks in this study remained low (below 3%) for all years of sampling and there were no notable trends in parasitism based on site, changes in land usage, or population size.
Significant differences in average, yearly physicochemical properties of each site existed for dissolved oxygen and salinity (Table 4). However, there were no strong relationships between the water quality parameters measured at these sites and corresponding shrimp densities as tested by multiple stepwise regression analysis. Although grass shrimp densities were significantly related to dissolved oxygen (P = 0.0134), pH (P < 0.001), and temperature (P < 0.001), the r-squared values for these variables were all below 0.11.
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DISCUSSION |
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Sanger (1998)
found that grass shrimp populations in South Carolina tidal creeks were significantly higher in creeks surrounded by forested upland than in industrial, urban, or suburban creeks. The current study notes that the amount of agricultural land use adjacent to some South Carolina tidal creek sites and the amount of agricultural runoff management corresponded with significant reductions in the densities of grass shrimp. Fairly low grass shrimp densities were found for most years at TRT and KWA, both sites with historic, extensive upland agricultural activity. Enhanced agricultural management at TRT, which reduced pesticide loading by approximately 90% in some cases (Scott et al., 1999), may have accounted for the slightly higher population levels of grass shrimp at TRT compared with KWA, but population densities at TRT remained lower than at both control sites for most years.
The change in land use at KWA, from agricultural fields to a golf course, matches a decrease in shrimp density and average shrimp length, both of which dropped in 1998 after golf course construction had begun. In a study on golf course runoff in Florida, pore water from sediments collected near the golf course complex were acutely toxic to P. pugio embryos (Lewis et al., 2001). In the same study, the shrimp Mysidopsis bahia exposed to sediments from sites adjacent to the golf course weighed less and the females were less often gravid than shrimp exposed to reference sediments (Lewis et al., 2001). Golf course runoff may contain high mercury levels (Mathews et al., 1995) and has been implicated in alterations in contaminant tolerance in killifish (Weis and Weis, 1984).
Patterns in population densities for these sites likely result from the trends that were detected in grass shrimp reproductive measures. When compared to the control sites, TRT and KWA grass shrimp populations contained fewer males and gravid females and, in the case of KWA, smaller clutch sizes. These patterns indicate the possible occurrence of chronic impacts from pesticides on grass shrimp at the agricultural sites. Similar trends were noted by Finley et al. (1999) for urbanized areas, where reduced percentages of gravid females among overwintering shrimp correlated with levels of polycyclic aromatic hydrocarbons. The lower percentage of males at the agricultural sites, particularly KWA, may indicate selective effects of land use on small shrimp, as male shrimp tend to be smaller than female. Moore (1988) found that for azinphosmethyl and endosulfan (two insecticides that have been used on South Carolina agricultural fields), grass shrimp showed selective mortality based on size, with increased size correlating with decreased mortality. Similarly, Wirth et al. (2001) reported that male grass shrimp were nearly twice as sensitive as females when exposed to endosulfan. Increased male sensitivity to pesticides has also been noted in the fiddler crab, Uca pugilator (Naewthong, 2001). Despite the larger percentage of total females at TRT and KWA, the lower percentage of females becoming gravid also suggests chronic impacts of contaminants by affecting the reproductive capabilities of female grass shrimp at those sites.
It is possible that these trends in reproductive measures and population dynamics may have resulted from endocrine disruption activity by contaminants. Oberdoerster et al. (2000) found that exposure of grass shrimp to pyrene, a polycyclic aromatic hydrocarbon (PAH), resulted in delayed molting in males and elevated production of lipovitellin (a yolk protein of crustacea) in female grass shrimp and that elevated lipovitellin corresponded with decreased egg viability. Some of the pesticides (e.g., atrazine, endosulfan) that have been used historically at the agricultural sites in this study have also been implicated as endocrine disruptors (Pait and Nelson, 2002). Although not directly testing endocrine activity, Wirth et al. (2002) found in laboratory-based studies that chronic exposure to endosulfan, a pesticide that was once commonly applied to the agricultural fields in this study, corresponded with significant decreases in the percent of female grass shrimp that became gravid. Research examining endocrine disrupting indicators, such as elevated lipovitellin levels, in grass shrimp from agriculturally influenced waters needs to be conducted.
Despite the presence of fewer male grass shrimp, the average size of individual shrimp at KWA was significantly smaller than at NIOL or CTL. There tended to be a lack of a spring peak in shrimp size at KWA which was likely related to the death or disappearance of some overwintering adults. Likewise, the less dramatic decline in shrimp size during early fall at NIOL, despite the higher numbers of shrimp at that site, may indicate a more suitable habitat for adult shrimp to survive or remain located.
In addition to differences in populations between sites, differences existed for annual grass shrimp population metrics within each site. For example, reductions in annual densities were noted for NIOL and CTL that did not correspond with any marked change in adjacent land use. For example, NIOL tended to have much greater grass shrimp densities in the years 1991 to 1995 than any year thereafter. A similar trend was seen for CTL with large density levels between 1991 and 1994, and relatively low levels thereafter. However, densities of shrimp in these populations remained significantly higher than TRT and KWA for most years, and no changes were seen in any population measure other than density. One hypothesis for this decline is the possible exposure of grass shrimp to an exotic virus or bacteria, similar to the potential impact of white spot virus on harvested penaeid shrimp populations of the southeastern U.S. from 1995 to 1998 (McIlwain et al., 1997). Whatever the cause, densities at TRT and KWA did not fall on the same scale as NIOL and CTL and the change in grass shrimp densities at NIOL and CTL seems to be pervasive and long lasting.
Two trends were noted in grass shrimp population dynamics which provided evidence for the importance of land conservation and runoff management. The presence of methods for preventing runoff of pesticides from agricultural land, namely retention ponds and pesticide application appropriate to pest type and quantity, corresponded to the slightly higher densities at the TRT site than at the KWA site, which employed no management techniques. Low percentages of gravid females existed for both the TRT and KWA populations, but clutch sizes at the TRT site were not significantly different than the CTL and NIOL site. Futhermore, the population at the National Estuarine Research Reserve and Sanctuary site (NIOL) contained the greatest number of shrimp and greatest percentage of gravid females than the CTL site, suggesting a link between land use conservation and grass shrimp population health.
Some trends in Palaemonetes spp. population dynamics have been noted in relation to land use in this study. Agricultural land use activities and associated runoff management relates significantly to effects in grass shrimp populations as does the development and maintenance of golf courses. Changes in population densities over time at the relatively pristine sites (NIOL and CTL) also existed but did not affect the overall comparisons between sites. Further tracking of these populations coupled with rigorous water and/or sediment contaminant monitoring may add significantly to our understanding of their mechanisms and strengthen the ability to predict impacts based on particular influences. Moreover, further work on elucidating the distribution patterns of these shrimp in various salt marsh systems would allow better prediction of impacts over the life span of individual grass shrimp.
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ACKNOWLEDGMENTS |
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The authors wish to thank the numerous individuals involved in sample and data collection at various times during this research, including but not limited to John Waldren, Pete Key, Shawn Laymen, Erich Strozier, John Devane, Dana Finley, Rob Sumner, and Blaine West.
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FOOTNOTES |
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1 From the Symposium EcoPhysiology and Conservation: The Contribution of Endocrinology and Immunology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5–9 January 2004, at New Orleans, Louisiana.
2 The research in this article does not signify that the contents necessarily reflect the views and policies of the agencies involved nor do trade names or commercial products constitute endorsement or recommendation for use.
3 E-mail: ak.leight{at}noaa.gov
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References |
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