6.0 Benthic Communities in the Cape Fear Estuary

Martin Posey and Troy Alphin

6.1 Summary
   For the 1998-1999 Lower Cape Fear River Program report, we have emphasized analysis of site characteristics, annual and seasonal variations in community structure, effects of Hurricane Bonnie, and correlations with selected physical parameters monitored as part of the overall Cape Fear River Program monitoring effort. These analyses are very preliminary in nature, based upon only 3 years of data (2 of which were affected by hurricanes) and only 4 sampling sites. However, they provide an initial insight into biotic community structure in the lower Cape Fear River system. Basic findings for this report are:

6.2 Background
   Benthic organisms (benthos) are those aquatic organisms living in or on the bottom. In estuarine systems, the benthic community is dominated primarily by species that burrow into the sediments (infauna), often living within tubes or burrow systems. Taxa dominating the infauna in most estuaries include small worms (polychaetes and oligochaetes), amphipod crustaceans, clams, and insect larvae, depending on salinities. Benthic animals generally consume detrital or planktonic food sources, with some predatory species present, and are in turn prey for larger fish, shrimp and crabs. In many estuarine systems there is a strong link between timing of predator recruitment (e.g. larval fish) and their benthic prey.
    Benthic fauna are considered important indicators of water quality and are used in a variety of monitoring programs to assess overall estuarine health and to follow long-term trends in estuarine communities, especially related to anthropogenic impacts (Boesch et al. 1976, Aschan and Skullerod 1990, Simboura et al. 1995, Hyland et al. 1996). From a monitoring perspective, benthos offer 3 positive features: 1) they are relatively sedentary and long-lived, 2) they occupy an important intermediate trophic position, and 3) they respond differentially to varying environmental conditions. After settlement, most benthos remain within a relatively constrained area, often less than 5 m2, for their entire adult lives. Therefore, unlike many other biotic or chemical measures, benthos reflect conditions at a specific location. Although a few opportunistic species may live for only a few weeks, most benthic animals have lifespans ranging from months to over a year, leading to a community structure that reflects average physical conditions over a time period of months. However, benthos vary greatly in their responses to changes in water quality. Some taxa are relatively tolerant of organic enrichment and low dissolved oxygen while others are quickly eliminated under low DO conditions (Boesch et al. 1976, Simboura et al. 1995). Increased nutrient inputs can strongly affect abundances of some species, through indirect and direct influences on food availability and sediment conditions, while not affecting others. Similarly, there is a wide variation in tolerance to pesticides and metal contaminants such as mercury and cadmium. In general, sediment type (clays, silts, sands, etc.), organic content, deposition of sediments (such as from upstream erosion), dissolved oxygen, salinity and temperature are considered most important in determining abundances and types of animals in bottom communities. By examining shifts in the benthic community over time (years), one can gain an understanding of the major environmental processes affecting the local biota (Hyland et al. 1996).
    A variety of indices have been developed to quantify the health of estuarine systems based on the relative proportions of species tolerant or susceptible to specific water quality parameters (e.g.; EPA Benthic Index; Ampelisca toxicity tests; suspension feeder : deposit feeder ratios; deep burrower : shallow burrower ratios; the Chandler Score, and the BMWP Score Index) (Whitehurst and Lindsey 1990). However, application of most indices requires long-term monitoring sufficient in duration to separate seasonal or annual variations from variations due to changes in water quality. Benthic community studies are a major component of the national EPA Environmental Monitoring and Assessment Program for estuaries as well as regional monitoring efforts, such as in Chesapeake Bay, Florida Bay, Long Island Sound, Pamlico Sound, and Tampa Bay.
    In Spring 1996, the Benthic Ecology Laboratory of the UNCW Center for Marine Science Research began long-term studies of benthic infauna in the Cape Fear River as part of the basic monitoring plan of the Cape Fear River Program. Preliminary samples were also taken during winter 1996 as part of other research efforts. The benthic monitoring component has four major long-term objectives: 1) characterize the benthic communities in the lower Cape Fear River and compare them with that of other river-dominated estuaries to gain a first-order assessment of estuarine health, 2) determine seasonal, annual and spatial patterns of variability, 3) establish correlations between benthic abundances and physical measures, and 4) establish a baseline for detecting changes in the estuarine community through examination of changes in abundances of specific indicator taxa and eventual application of standard benthic indices.
    In the 1997-1998 Cape Fear River report, we established that there are strong differences between sites, as expected with salinity differences. Site differences may also reflect differential response to and recovery from hurricane disturbance in 1996 and 1998. Differences between sites will be revisited in future reports as we get more information from non-hurricane years. This report (1998-1999) focuses on temporal patterns and environmental correlates with faunal distributions at each of the distinct sites and represents a preliminary attempt to connect the health of these sites with factors that may be most strongly affecting community composition at each. We focus on trends in total faunal abundance and the dominant species over time at each site. Additionally, we examine which physical factors correlate most strongly with patterns of faunal abundance. With the addition of further monitoring data, in future reports we hope to develop some predictive ability for estimating community responses to selected physical perturbations.

6.3 Methodology
   Four stations are sampled as part of basic monitoring for benthic infauna: NCF6 in the Northeast Cape Fear River, NAV in the mainstem Cape Fear River, and M54 and M31 in the lower estuary (Figure 6.1). These stations span the oligohaline to mesohaline/polyhaline zones of the estuary and correspond to stations sampled as part of water quality monitoring. The basic monitoring of benthos involves quarterly sampling at each station. Samples are collected in winter (January-February), spring (mid March-May), summer (July-early September), and fall (October-November). Following hurricanes Bertha and Fran in late summer 1996 and Hurricane Bonnie in September 1998, additional samples were also taken to observe recovery patterns (September 1996, December 1996, February 1997, September 1998 and November 1998). This additional sampling was supported by the Benthic Ecology Laboratory. Post-hurricane samples collected on 1 October 1996 were only taken from stations M54 and M31 because of debris at the other 2 stations. During 1998, samples were collected in January, April/May, August, September (to examine effects of Hurricane Bonnie), and October/November. Confirmation of identifications for the spring 1998 samples is ongoing and the results from this sampling will not be reported until all identifications have been completed, confirmed, and QA/QC completed (data will be presented in the next annual monitoring report).
    At each sampling station, benthic infaunal samples are taken with a Petite Ponar grab, 15cm x 15cm opening (0.023m2) and 15cm depth. Five grab samples are taken at each sampling location on each sampling date. Grabs were retained only if the grab was full in order to standardize volume sampled. Grab samples are taken from a boat at stations specified by GPS coordinates and all sampling locations are in approximately 6-8 feet (2-3 m) of water (studies in other estuaries have indicated greater abundances in shallow areas as compared to deep channels within an estuary). Immediately after collection, the samples are sieved through a 0.5 mm mesh screen, preserved in 10% buffered formalin with rose bengal dye added, and transferred to 70% ethanol after 3 days for later sorting and identification. Separation of animals from remaining sediment is done under a dissecting microscope. All animals are identified to the lowest reliable taxonomic level, with random specimens verified by outside taxonomists. These procedures follow standard formats for benthic sampling outlined by the EPA Environmental Monitoring and Assessment Program and used in other monitoring programs (Hyland et al. 1996, Posey et al. 1997).
    In order to determine correlations between faunal abundance and selected water quality factors, we conducted a correlation analysis between 7 biotic variables and 8 physical measures separately for each site. The biotic variables were total polychaete abundance, total bivalve abundance, total insect abundance, total amphipod abundance, total oligochaete abundance, total numbers of surface burrowers/tube dwellers, and total infaunal abundance. Polychaetes, bivalves, insects, amphipods and oligochaetes represent the dominant bottom fauna in the lower Cape Fear River system, though their relative importance varies between sites. Surface burrowers and tube dwellers represent a group of infauna, including certain polychaetes, amphipods, bivalves and insects, that may be particularly susceptible to changes in dissolved oxygen, siltation rates, or planktonic food availability. Because of their accessibility to fish and crabs, they may also be particularly important as fishery food resources. All groupings were based upon Fauchauld and Jumars (1979) and Posey et al. (1996) and species were not classified according to feeding type or living position if there was conflicting or inadequate information. The eight water quality measures included salinity, temperature, dissolved oxygen (DO), total nitrate+nitrite (NO3/NO2), suspended solids, DO from the month prior to benthic sampling, chlorophyll a, and turbidity. Salinity and temperature are well known to affect benthic abundances and vary seasonally, providing a proxy for seasonal variations. Dissolved oxygen varies with temperature and can also have a seasonal aspect. However, DO can also decline due to major storm events or anthropogenic causes, and thus may act independently of seasonal variations. The effects of DO may not only be immediate, but also may have a delayed influence through effects on recruitment and subsequent growth of individuals, hence the inclusion of previous DO readings in the analysis. NO3/NO2 provides a proxy for runoff and may directly affect benthic and water column productivity (and hence food availability to bottom animals). Chlorophyll a levels also reflect water column productivity. Suspended solids and turbidity can be strongly affected by river flow and runoff. They can influence bottom animals negatively through burial or clogging of gills and positively, at small levels, through increased input of detrital food.
    A Spearman’s rank correlation analysis was used to examine relationships between the biotic and physical variables. The monthly means for each physical measure and biotic measure were obtained for each site from the monthly monitoring program and used to determine rank observations. A single observation for these analyses was a month with corresponding mean faunal and mean physical measures. This meant the sample size for correlations ranged from n=8 at M31 to n=11 at NAV and NCF6. It is important to note that a rank correlation analysis is a conservative statistic that only tests whether a biotic measure increases or decreases consistently with a specified physical measure. It does not take into account the magnitude of changes and only detects relatively strong relationships. A lack of significant correlation between variables thus should not be taken as indicating they are not related; rather, just that the relationship, if it does exists, is weaker than can be detected by this test given the limited data set. The inclusion of more data (continued sampling) will increase the ability to detect significant correlations in future analyses. A rank test was conducted in this case rather than a test that may be more sensitive to patterns because of high variability in the data and the relatively low sample size.

6.4 Results and Discussion
   A total of 176 taxa have been collected since Spring 1996. The dominant taxa are listed and described in Table 6.1 and abundances of all taxa collected through 1997 were presented in the 1997-1998 report (Mallin et al. 1998). A summary of cumulative patterns of dominance and abundances for the 1998 collections are discussed below. In general, less than half of the species were collected at any single site and most species were relatively rare (Tables 6.10-6.13).

6.4a. Site NCF6 – Northeast Cape Fear River
    NCF6 is located in the Northeast Cape Fear River (Figure 6.1). This site is characterized by relatively low salinity and fine sediments. Salinity for the months in which benthos were sampled averaged 1.8 ppt, with lower salinity during winter months (0.67 ppt) and higher during summer (5.47 ppt). Water temperature ranged from 5.9 oC to 28.3 oC. Dissolved oxygen varied seasonally, with a winter average of 8.8 and a summer average 3.7. DO exhibited severe declines immediately after the passage of Hurricanes Fran and Bonnie (Mallin et al. 1999; Chapter 9 this report).
    The NCF6 site is characterized by relatively high species richness but low abundances. 38 taxa were identified from this site during 1998 sampling (Table 6.10), compared to only 23 taxa from the other low salinity site sampled (NAV). However, most taxa were relatively rare, with total faunal abundances averaging only 10.2 per grab since 1996 (Table 6.2). This is only 20-40% of the other sites sampled. As expected from the low salinities, this site is dominated by oligohaline to freshwater organisms, especially insect larvae (Chironomidae, Procladius, Polypedilum and Chaoborus), certain amphipods (Gammarus spp.) and oligochaetes. Seasonality is not strong, though there is a trend towards lower overall abundances in fall sampling (possibly reflecting the influence of hurricanes in 2 of the 3 years sampled) and higher abundances in the spring (Table 6.2). However, a few specific taxa, especially the polychaete worm Maranzellaria, do show strong seasonal peaks in dominance. There was no clear pattern for long-term declines or increases in benthic abundances. However, we have limited ability to detect such trends at this early stage in the monitoring effort because of only 3 years of data and the influence of hurricanes in 2 of those years. One clear pattern is high variability between years, emphasizing the need for long-term data sets in determining benthic community trends and cautioning against using data from only 2 or 3 years.
    The passage of Hurricane Bonnie in 1998 affected the infaunal community. An average of only 0.8 individuals per grab (equivalent to 4 total individuals) was found in samples taken after the hurricane compared to 3.2 individuals per grab immediately before the hurricane. The abundances observed at this site after Hurricane Bonnie represented the lowest at any site on any date since our monitoring began in 1996. However, it should be noted that abundances in August 1998, before the hurricane, were already low, possibly reflecting a period of natural decline in the community.
    Relatively few correlations were identified between the physical parameters tested and benthic faunal abundances (Table 6.6). There was a positive correlation between bivalve abundances and prior DO levels, a negative relationship between chlorophyll a and insect abundances, and a trend towards a negative relationship between salinity and insect numbers. We believe the relationship between prior DO and bivalve abundances reflects the strong effects that low DO from hurricanes had on this group as well as the long time needed for bivalve recovery after the hurricane had passed. Insect larvae are primarily freshwater, so declines with increasing salinity are expected. Chlorophyll a at this site was positively correlated with salinity (r=0.66, p<0.02), and the relationship between chlorophyll a and insect numbers may simply reflect salinity effects on both variables.
    To summarize patterns at this site, the most important characteristics are relatively high numbers of species but low abundances. A major question is whether the Northeast Cape Fear River in general has low faunal abundances or whether this is a site-specific phenomenon. If so, a key to understanding community health at this site is an understanding of the factors that cause such low densities. The average dissolved oxygen levels are not low relative to other sites, so preliminary hypotheses might center on short-term events, food availability, and recruitment limitation. Relatively few physical parameters correlated with faunal abundances at the site, possibly reflecting the consistently low abundances and low statistical power of our preliminary analyses.

6.4.b Site NAV – Cape Fear River
    NAV is located in the mainstem Cape Fear River. Like NCF6, this site is characterized by relatively low salinity and fine sediments. Salinity for the months in which benthos was sampled averaged 1.2 ppt, with lower salinity during winter months (0.3 ppt) and higher during summer (4.0 ppt). Water temperature ranged from 4.2 oC to 28.3 oC. Dissolved oxygen varied seasonally, with a winter average of 9.2 and a summer average 3.9 mg/L. DO exhibited declines to near anoxic levels for over two weeks after the passage of Hurricanes Fran and Bonnie (Mallin et al. 1999; Chapter 9 this report).
    NAV differs fundamentally from NCF6 by having high faunal abundances but low diversity of fauna. In 1998 there were a total of only 23 taxa collected from this site (Table 6.11); however, total faunal abundances since 1996 have averaged 88.8 individuals per grab, 8 times that of the NCF6 site (Table 6.3). As expected from the low salinities, this site is dominated by oligohaline to freshwater organisms, especially insect larvae (Chironomidae, Tanypodinae, Procladius, and Polypedilum), oligochaetes, and certain polychaetes (Maranzellaria and Mediomastus). The NAV site had generally similar species composition as NCF6, with the exception of high polychaete numbers. These polychaetes have planktonic development, possibly indicating better recruitment conditions at the NAV site. Seasonality was strong at the NAV site, with lower overall abundances in summer and fall (possibly reflecting the influence of hurricanes in 2 of the 3 years sampled) and higher abundances in winter and spring. These seasonal patterns are characteristic of estuarine benthic communities, with winter and spring being periods of high recruitment and summer and fall declines often caused at least partly by predation and, for insects, growth into flying forms. As with NCF6, there is little clear evidence of long-term trends in abundance.
    Hurricane Bonnie had similar qualitative effects at NAV as at the other low salinity site. An average of 3.2 individuals per grab was found in samples taken after the passage of the hurricane compared to 10 individuals per grab immediately before the hurricane (Table 6.3). The abundances observed after Hurricane Bonnie were the lowest observed at this site for any date since monitoring began in 1996. Research elsewhere has indicated that dissolved oxygen concentrations less than 2.0 mg/L are required before severe effects on benthos are noted (Boesch et al. 1976; Gaston 1985; Gaston and Edds 1994; Rhoads and Morse 1971. Dissolved oxygen at Navassa fell below 1.0 mg/L for several days. However, it should be noted that abundances in August 1998, before the hurricane, were already low (representing the second lowest recorded value), suggesting the community was already in decline before the hurricane hit.
    There were strong correlations between salinity, temperature, DO and past DO for several of the taxa examined (Table 6.7). However, the pattern of these correlations suggests strong seasonal trends and co-variance in effects. Salinity and temperature are lowest in winter while DO is highest in winter and spring (the correlation between DO and temperature is –0.900, p<0.0001 for this site). Lower abundances during summer and fall may represent a cumulative effect of these variables, along with seasonally high predation and low recruitment, or may represent the strong effects of only a few variables, with other correlations simply reflecting seasonal co-variation in physical factors. More spatially extensive sampling over a variety of habitats in this region of the river will help to separate which factor(s) is(are) most important in producing seasonal variation. We believe the negative correlations between temperature and salinity and faunal abundances and the positive correlation between DO and faunal abundance reflects seasonality in benthic populations rather than direct causality. This is supported by the observation that DO was greater than 4 mg/L at this site during the time benthic infaunal samples were taken for most summer dates (the exceptions being post-hurricane samples). Also, that many of the common benthic fauna (e.g. oligochaetes and Mediomastus) burrow in hypoxic sediments and are tolerant of low DO levels in the average range observed. The strong correlation between temperature and abundances suggests seasonality is more important than hurricane events in determining long-term correlative patterns. Such seasonality may reflect life histories of the component species as well as the combined effects of several environmental factors.
    To summarize patterns at this site, the most important characteristics are relatively high faunal abundances but low numbers of species. This suggests that the NAV community is controlled by very different factors than the NCF6 community and that it may have a greater food resource importance for fish and crabs. As with the Northeast Cape Fear River site, a major question exists concerning whether this site is representative of the mainstem Cape Fear River or whether observed patterns represent site-specific phenomenon. Inclusion of additional sites for a 2 year period is needed to address this question. Several physical parameters monitored by the Cape Fear River Program correlated strongly with faunal abundances at the site. However, this may be more representative of seasonality than direct causation of patterns.

6.4.c Site M54 – Cape Fear River estuary
    M54 is located in the mainstem Cape Fear River below the confluence of the Cape Fear and Northeast Cape Fear rivers. It is characterized by higher but more variable salinities than the NCF6 and NAV sites. Salinity for the months in which benthos was sampled averaged 5.2 ppt but ranged from 0 to 18 ppt. Salinity was lower during winter months (3.4 ppt) and higher during summer (11.9 ppt). Water temperature ranged from 8.4 oC to 28.2 oC. Dissolved oxygen varied seasonally, with a winter average of 8.9 and a summer average 4.8 mg/L for the months sampled. DO exhibited severe declines immediately after the passage of Hurricanes Fran and Bonnie (Mallin et al. 1999; Chapter 9 this report).
    M54 has a relatively high species richness but intermediate to low abundances of fauna. In 1998 there were a total of 34 taxa collected from this site (Table 6.12), but total faunal abundances since 1996 have averaged only 23.9 individuals per grab (Table 6.4). As expected from the fluctuating salinities, this site is dominated by a mix of oligohaline/ freshwater organisms and more marine forms. Dominant taxa included polychaetes (Maranzellaria and Mediomastus), oligochaetes, and certain amphipods (Gammarus spp., Lembos, Monoculodes). Insects were generally less common than at the upstream sites, as expected from the higher salinity. Seasonality was strong at the M54 site, with lower overall abundances in summer and fall (possibly reflecting the influence of hurricanes in 2 of the 3 years sampled) and higher abundances in late winter and spring. As with the other sites, there is little clear evidence of long-term trends in abundance based on the 3-year database available.
    Unlike the 2 upstream sites, there was little evidence for declines in faunal abundance associated with the passage of Hurricane Bonnie. Before the hurricane, total faunal abundance was 7.6 per grab, while after the hurricane abundances were 26.8 per grab (Table 6.4). The September 1998 abundances were higher than found in September 1997 or in October 1996 (after Hurricane Fran). It is possible that abundances at this site were elevated after Hurricane Bonnie because of wash down of fauna from upstream areas associated with increased water flow, but more than 1 non-hurricane year is needed to establish baseline trends.
    There were correlations between salinity, temperature, DO, and past DO for several of the taxa examined (Table 6.8). However, as with NAV, some of these correlations may represent concordant seasonal trends in environmental factors, predation pressures and recruitment rather than direct causality. Salinity and temperature are lowest in winter while DO is highest in winter and spring (the correlation between DO and temperature is –0.833, p<0.01 for this site). We believe the negative correlations between temperature and salinity and faunal abundances and the positive correlation between DO and faunal abundance reflects seasonality in benthic populations caused by recruitment and predation variations rather than direct causality. This is supported by the observation that DO was greater than 4 mg/L at this site for 10 of the 12 infaunal sampling dates (the exceptions being post-hurricane samples in 1996 and 1998), above tolerances for many estuarine burrowing worms. Many polychaetes consume detrital material deposited from the water column, including Mediomastus, which was common at this site. Thus, positive correlations between polychaete abundances and suspended solids and turbidity may reflect enhanced recruitment and food availability effects. This site is also near the turbidity maximum zone for the Cape Fear River, and turbidity patterns at this site may reflect other relationships. However, extreme levels of suspended solids may be expected to have detrimental effects of certain polychaete taxa. Particulate loading may also be related to seasonality, but the relationship between turbidity and temperature and suspended solids and temperature were both non-significant.
    To summarize patterns at this site, the most important characteristics are high numbers of taxa but relatively low overall faunal abundances. Additionally, there is significant seasonal variability in physical conditions, faunal abundances and faunal composition. Several physical parameters monitored by the Cape Fear River Program correlated strongly with faunal abundances at the site. However, this may be more representative of seasonality than direct causation of patterns.

6.4.d Site M31 – Cape Fear estuary
    M31 is located in the Cape Fear estuary and is the furthest downstream site sampled as part of the basic benthic monitoring program. It is characterized by higher salinities than at any of the other sites. Salinity for the months in which benthos was sampled averaged 10.8 ppt, ranging from 0.1 (immediately after Hurricane Bonnie) to 26.1 ppt. Salinity was lower during winter months (8.9 ppt) and higher during summer (18.5 ppt). Water temperature ranged from 6.8 oC to 28.6 oC. Dissolved oxygen varied seasonally, with a winter average of 9.3 and a summer average 5.0 mg/L. DO exhibited a decline immediately after the passage of Hurricane Bonnie (current report), but less so after Hurricane Fran (Mallin et al. 1999).
    M31 has similar species richness to the other main estuarine site, M54, but has generally high abundances. In 1998 there were a total of 38 taxa collected from this site (Table 6.13) and total faunal abundances since 1996 have averaged 58.1 individuals per grab (Table 6.5). As expected from the higher salinities, this site is dominated by more marine forms. The dominant fauna at this site are polychaete worms, including Maranzellaria, Mediomastus, and Streblospio, all of which are common constituents of the bottom community in other estuaries (Mahoney et al. 1982, van Dolah et al. 1984, Shaffner et al. 1987, Holland et al. 1987, Posey et al. 1993, Posey et al. 1997). Although less common, certain amphipods and bivalves also were seasonally abundant. Insects and oligochaetes were less dominant compared to the upstream sites, as expected with the higher salinity. Although highest abundances were observed during winter and spring (total abundance of 194 in December 1996 and 144 in April 1996), the pattern was not consistent. During 1997, highest numbers were actually observed in late summer. As with the other sites, there is little clear evidence of long-term trends in abundance from the limited data available.
    Like the NAV and NCF6 sites, there was evidence for significant declines in faunal abundance associated with the passage of Hurricane Bonnie. Before the hurricane, total faunal abundance was 67.8 per grab, while after the hurricane abundances were 4.4 per grab (Table 6.5). As at the NCF6 and NAV sites, the post-Bonnie faunal densities were the lowest recorded for the site since monitoring began. Unlike the other sites, there was no evidence that faunal abundances were in decline before the hurricane. Possible causes for faunal declines after Hurricane Bonnie include the exceptionally low salinity at the site (0.1 ppt) and low DO.
    The only significant correlation between the physical factors tested and biotic abundances was an increase in abundances of surface burrowers with increasing temperature (Table 6.9). The lack of significant correlations most likely reflects an inconsistency in seasonal patterns combined with the low statistical power of analyses due to limited sample size to date. The one positive correlation that was observed reflected higher abundances of certain tube dwelling/surface burrowing fauna during summer months (especially the worm Streblospio)
    To summarize patterns at this site, the most important characteristics are a combination of relatively high numbers of taxa and high overall faunal abundances. The dominant faunal present are typical of moderately impacted estuaries studied elsewhere along the mid-Atlantic and southeastern coasts. Seasonal patterns are present but variable and the site experiences significant impacts from Hurricane Bonnie.

 6.5 Literature Cited

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Boesch, D.F., R.J. Diaz and R.W. Virnstein. 1976. Effects of tropical storm Agnes on soft-bottom macrobenthic communities of the James and York River estuaries and the lower Chesapeake Bay. Chesapeake Science 17:246-259.

Fauchauld, K. and P.A. Jumars. 1979. The diet of worms: a study of polychaete feeding

guilds. Oceanography and Marine Biology Annual Revue 17:193-284.

Gaston, G.R. 1985. Effects of hypoxia on macrobenthos of the inner shelf off Cameron, Louisiana. Estuarine, Coastal and Shelf Science 20:603-613.

Gaston, G.R. and K.A. Edds. 1994. Long-term study of benthic communities on the continental shelf off Cameron, Louisiana: a review of brine effects and hypoxia. Gulf Research Reports 9:57-64.

Holland, A.F., A.T. Shaughnessy and M.H. Hiegel. 1987. Long-term variation in mesohaline Chesapeake Bay macrobenthos: spatial and temporal patterns. Estuaries 10:227-245.

Hyland, J.L., T.J. Herlinger, T.R. Snouts, A.H. Ringwood, R.F. Van Dolah, C.T. Hackney, G.A. Nelson, J.S. Rosen and S.A. Kokkinakis. 1996. Environmental quality of estuaries of the Carolinian Province: 1994. Annual statistical summary for the 1994 EMAP - Estuaries Demonstration Project in the Carolinian Province. NOAA Technical Memorandum NOS ORCA 97. NOAA/NOS, Office of Ocean Resources Conservation and Assessment, Silver Spring, MD. 102p.

Mahooney, B.M.S. and R.J. Livingston. 1982. Seasonal fluctuations of benthic macrofauna in the Apalachicola Estuary, Florida, USA: The role of predation. Marine Biology 69:207-213.

Mallin, M.A., M.H. Posey, M.L. Moser, G.C. Shank, M.R. McIver, T.D. Alphin, S.H. Ensign and J.F. Merritt. 1998. Environmental Assessment of the Lower Cape Fear River System, 1997-1998. CMSR Report No. 98-02, Center for Marine Science Research, University of North Carolina at Wilmington, Wilmington, N.C.

Mallin, M.A., M.H. Posey, G.C. Shank, M.R. McIver, S.H. Ensign and T.D. Alphin. 1999. Hurricane effects on water quality and benthos in the Cape Fear Watershed: Natural and anthropogenic impacts. Ecological Applications 9:350-362.

Posey, M.H., T.D. Alphin and C.M. Powell. 1997. Plant and infaunal communities associated with a created marsh. Estuaries 20:42-47.

Posey, M.H., W. Lindberg, T. Alphin and F. Vose. 1996. Influence of storm disturbance on an offshore benthic community. Bulletin of Marine Science 59:523-529.

Posey, M.H., C.W Wigand and J.C. Stevenson. 1993. Effects of an introduced aquatic plant, Hydrilla verticillata, on benthic communities in the upper Chesapeake Bay. Estuarine, Coastal and Shelf Science 37: 539-555.

Rhoads, D.c. and J.C. Morse. 1971. Evolutionary and ecological significance of oxygen-deficient marine basins. Lethaia 4:413-428.

Shaffner, L.C., R.J. Diaz, C. R. Olsen and I.L. Larsen. 1987. Faunal characteristics and sediment accumulation processes in the James River Estuary, Virginia. Estuarine, Coastal and Shelf Science 25: 211-226.

Simboura, N., A. Zenetus, P. Panayotides and A. Makra. 1995. Changes in benthic community structure along an environmental pollution gradient. Marine Pollution Bulletin 30:470-474.

van Dolah, R.F., D.R. Calder and D.M. Knott. 1984. Effects of dredging and open water disposal on benthic macroinvertebrates in a South Carolina estuary. Estuaries 7:28-37.

Whitehurst, I. T. and B.I. Lindsey. 1990. The impact of organic enrichment on the benthic macroinvertebrate communities of a lowland river. Water Research 24:625-630.

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