An estuarine benthic index of biotic integrity for the Mid-Atlantic region of the United States. II. Index development

A benthic index of biotic integrity was developed for use in estuaries of the mid-Atlantic region of the United States (Delaware Bay estuary through Albemarle-Pamlico Sound). The index was developed for the Mid-Atlantic Integrated Assessment Program (MAIA) of the U.S. Environmental Protection Agency using procedures similar to those applied previously in Chesapeake Bay and southeastern estuaries, and was based on sampling in July through early October. Data from seven federal and state sampling programs were used to categorize sites as degraded or non-degraded based on dissolved oxygen, sediment contaminant, and sediment toxicity criteria. Various metrics of benthic community structure and function that distinguished between degraded and reference (non-degraded) sites were selected for each of five major habitat types defined by classification analysis of assemblages. Each metric was scored according to thresholds established on the distribution of values at reference sites, so that sites with low scoring metrics would be expected to show signs of degradation. For each habitat, metrics that correctly classified at least 50% of the degraded sites in the calibration data set were selected whenever possible to derive the index. The final index integrated the average score of the combination of metrics that performed best according to several criteria. Selected metrics included measures of productivity (abundance), diversity (number of taxa, Shannon-Wiener diversity, percent dominance), species composition and life history (percent abundance of pollution-indicative taxa, percent abundance of pollution-sensitive taxa, percent abundance of Bivalvia, Tanypodinae-Chironomidae abundance ratio), and trophic composition (percent abundance of deep-deposit feeders). The index correctly classified 82% of all sites in an independent data set. Classification efficiencies of sites were higher in the mesohaline and polyhaline habitats (81–92%) than in the oligohaline (71%) and the tidal freshwater (61%). Although application of the index to low salinity habitats should be done with caution, the MAIA index appeared to be quite reliable with a high likelihood of correctly identifying both degraded and non-degraded conditions. The index is expected to be of great utility in regional assessments as a tool for evaluating the integrity of benthic assemblages and tracking their condition over time.     

The soft-bottom macrobenthos of North Carolina estuaries

The structure of macro infaunal (>0.5 mm sieve size) assemblages was examined in samples of unconsolidated substrates collected during the summers of 1994–1997 at 208 stations throughout North Carolina estuaries. Numerical classification (cluster analysis) of stations resulted in 14 distinct site groups that reflected discernible habitatrelated patterns in species distributions. Multiple discriminant analysis, performed on synoptic abiotic variables (depth, salinity, dissolved oxygen, pH, percent silt-clay), showed that the separation of site groups was related primarily to salinity. Percent silt-clay had a secondary influence on the separation of sites within similar salinity zones. Species diversity among site groups generally decreased with decreasing salinity and increasing mud content of sediment. Nodal analysis showed a wide range in constancy and fidelity of species assemblages within site groups. Some assemblages dominated by euryhaline species had no particular affinity with any one site group. The strongest affinities, as evidenced by high values of both constancy and fidelity, were displayed by an assemblage of oligochaetes, insect larvae, gammaridean amphipods, and the clamCorbicula fluminea in tidal freshwater muds; and an assemblage of haustoriid amphipods, the bivalveDonax variabilis, the polychaeteParaonis fulgens, and unidentified echinoids at high-salinity sites in outer Pamlico Sound near ocean inlets. A series of stations with impaired benthic assemblages in polluted habitats emerged from the cluster analysis and was distinguishable from other site groups that reflected a greater influence of natural controlling factors (such as salinity and sediment type) on species distributions. These results suggest that the interaction of both anthropogenic and natural environmental controlling factors is important in defining the structure of these infaunal assemblages.     

Discovery of the “Phantom” dinoflagellate in Chesapeake Bay

Since its discovery in natural estuarine habitat of North Carolina in 1991, the widespread impact of the toxic dinoflagellate, Pfiesteria piscicida (gen. et sp. nov.), popularly called the “phantom” dinoflagellate, on North Carolina fish stocks has been established, yet little is known about its influence outside of North Carolina estuaries. Here, we document the presence of P. piscicida in Chesapeake Bay. A fish kill was observed after inoculating an aquarium containing mummichogs with sediment samples from Jenkins Creek, a brackish creek (salinity 11‰) of the Chesapeake Bay system. P. piscicida was the cause of the kill, as supported by morphological, physiological, and histological evidence. The appearance and behavior of the algae and symptoms associated with fish mortality were consistent with those previously observed in P. piscicida-associated aquaria fish kills in North Carolina. The discovery of P. piscicida in Chesapeake Bay supports the speculation that these toxic dinoflagellates have a dramatic and far-reaching impact on fish stocks in shallow, eutrophic estuaries along the eastern United States.     

Paleoecological evidence of human impacts on the Neuse and Pamlico estuaries of North Carolina,USA

Sediment cores were collected from the Neuse and Pamlico River estuaries, North Carolina, at seven different sites, and the data show strong anthropogenic influence on water quality. The sediments from these cores were dated using²¹⁰Pb,¹³⁷Cs,¹⁴C, and pollen horizon techniques. Specific parameters investigated include bulk density, sedimentation rates, diatom assemblage changes, nutrient and trace metal flux, and vegetation changes as recorded in the pollen record. The greatest increases in sedimentation, nutrient and metal flux and changes in diatom assemblages have occurred in the past 50–60 yr in the Pamlico and Neuse. Diatom diversity has decreased and small planktonic forms have become dominant over time, most likely due to eutrophication and increased turbidity and sedimentation. Major changes occur before phytoplankton surveys and monitoring were initiated. Overall trends are similar to those found in Chesapeake Bay, although the time frame of major changes is more recent. Dominant small planktonic diatom species differ between Chesapeake Bay and the Neuse and Pamlico. Variance in paleoecological indicators between these mid-Atlantic estuaries may be due to geomorphology and land use history.     

Expression of the Estuarine species minimum in littoral fish assemblages of the Lower Chesapeake Bay Tributaries

Species richness declines to a minimum (artenminimum) in the oligohaline reach of estuaries and other large bodies of brackish water. To date, observations of this feature in temperate estuaries have been largely restricted to benthic macroinvertebrates. Five years of seine data collected during the summers of 1990–1995 in the major tidal tributaries to the lower Chesapeake Bay were examined to see if this feature arose in estuarine fish assemblages. Estimates of numerical species richness (alpha diversity) and rates of species turnover between sites (beta diversity) were generated via rarefaction and detrended correspondence analysis. Two spatial attributes of the distribution of littoral fish species along salinity gradients in the tributaries of the lower Chesapeake Bay were revealed: (1) a species richness depression in salinities of 8–10% and (2) a peak in the rate of species turnover associated with the tidal freshwater interface (salinities of 0–2%). Expression of the minimum is influenced by the physical length of the salinity gradient and the interaction between a species’ salinity preferences and tendency to make long excursions from favorable habitats.     

Responses of fish and macrobenthic assemblages to hydrologic disturbances in Tijuana Estuary and Los Peñasquitos Lagoon,California

Changes in the assemblages of fishes and benthic macro-invertebrates were evaluated in relation to wastewater inflows at Tijuana Estuary and impounded streamflows and mouth closure at Los Peñasquitos Lagoon. Freshwater from sewage spills or winter rains lowered water salinities and had major impacts on the channel organisms of both southern California coastal wetlands. Benthic infaunal assemblages responded more rapidly to reduced salinity than did fishes, with continued salinity reduction leading to the extirpation of most species. Both the fish and benthic invertebrate assemblages became dominated by species with early ages of maturity and protracted spawning seasons. Between-system comparisons showed that good tidal flushing reduced negative impacts on both the fish and benthic assemblages.     

Hidden Components in Tropical Seascapes: Deep-Estuary Habitats Support Unique Fish Assemblages

Tropical coastal seascapes are biodiverse and highly productive systems composed of an interacting mix of habitats. They provide crucial ecosystem services that support people’s livelihoods, yet key components of these seascapes remain unstudied. We know little about the deep (>2 m) subtidal areas of tropical estuaries, because, due to gear restrictions, there have been no detailed studies of the habitats they contain and the fish that use them. Consequently, potentially important functions and linkages with surrounding habitats remain unknown. Using unbaited videos, an approach capable of sampling the full breadth of benthic habitats and whole fish assemblages, we investigated patterns of fish occupancy of the deep subtidal habitats (2–20 m) in one of Australia’s largest tropical estuaries. We identified 19 taxa not previously recorded from estuaries of tropical eastern Australia, along with 36 previously identified estuary taxa. Three recognisable fish assemblages were associated with distinct benthic habitat types: open bottom fine sediment, seagrass and structurally complex rocky areas. In deep water, habitats often overlooked in shallow water become important, and there are sharp differences in habitat function. Deep subtidal habitats are potentially an important zone for direct interaction between estuary and marine fauna, with a range of consequences for intertidal habitat use and nursery ground functioning. The interface between marine areas and the shallow-water estuary may be richer and more complex than previously recognised.     

Effects of low dissolved oxygen events on the macrobenthos of the lower Chesapeake Bay

The effects of low dissolved oxygen or hypoxia (<2 mg l^?1) on macrobenthic infaunal community structure and composition in the lower Chesapeake Bay and its major tributaries, the Rappahannock, York, and James rivers are reported. Macrobenthic communities at hypoxia-affected stations were characterized by lower species diversity, lower biomass, a lower proportion of deep-dwelling biomass (deeper than 5 cm in the sediment), and changes in community composition. Higher dominance in density and biomass of opportunistic species (e.g., euryhaline annelids) and lower dominance of equilibrium species (e.g., long-lived bivalves and maldanid polychaetes) were observed at hypoxia-affected stations. Hypoxia-affected macrobenthic communities were found in the polyhaline deep western channel of the bay mainstem north of the Rappahannock River and in the mesohaline region of the lower Rappahannock River. No hypoxic effects on the infaunal macrobenthos were found in the York River, James River, or other deep-water channels of the lower Chesapeake Bay.     

Small-scale spatial variation of macrobenthic community structure

Examination of small-scale spatial variation in essential to understanding the relationships between environmental factors and benthic community structure in estuaries. A sampling experiment was performed in October 1993 to measure infauna association with sediment composition and salinity gradients in Nueces Bay, Texas, USA. The bay was partitioned into four salinity zones and three sediment types. Higher densities of macrofaua, were found in sediments with greater sand content and in areas with higher salinity. High diversity was also associated with high homogeneous salinity (31–33‰) and greater sand content. Macrofauna biomass and diversity were positively correlated with bottom salinity, porewater salinity, and bottom dissolved inorganic nitrogen (DIN). Furthermore, species dominance shifted along the estuarine gradient.Streblospio benedicti dominated at lower salinity, but,Mediomatsus ambiseta andMulinia lateralis were the dominant species at higher salinity. Statistical analyses revealed significant correlations for sediment characteristics (i.e., increased fine sediments, water content, and total organic carbon) with decreased total abundance and diversity. Increased salinity and DIN were correlated with increased total biomass, diversity, and macrofauma community structure. These physico-chemical variables are regulated by freshwater inflow, so inflow is an important factor influencing macrofauna community structure by indirectly influencing the physico-chemical environment.     

The response of fishes to submerged aquatic vegetation complexity in two ecoregions of the mid-Atlantic bight: Buzzards Bay and Chesapeake Bay

Estuarine seagrass ecosystems provide important habitat for fish and invertebrates and changes in these systems may alter their ability to support fish. The response of fish assemblages to alteration of eelgrass (Zostera marina) ecosystems in two ecoregions of the Mid-Atlantic Bight (Buzzards Bay and Chesapeake Bay) was evaluated by sampling historical eelgrass sites that currently span a broad range of stress and habitat quality. In two widely separated ecoregions with very different fish faunas, degradation and loss of submerged aquatic vegetation (SAV) habitat has lead to declines in fish standing stock and species richness. The abundance, biomass, and species richness of the fish assemblage were significantly higher at sites that have high levels of eelgrass habitat complexity (biomass >100 wet g m^?2; density <100 shotts m^?2) compared to sites that have reduced eelgrass (biomass <100 wet g m^?2; density <100 shoots m^?2) or that have completely lost eelgrass. Abundance, biomass, and species richness at reduced eelgrass complexity sites also were more variable than at high eelgrass complexity habitats. Low SAV complexity sites had higher proportions of pelagic species that are not dependent on benthic habitat structure for feeding or refuge. Most species had greater abundance and were found more frequently at sites that have eelgrass. The replacement of SAV habitats by benthic macroalgae, which occurred in Buzzards Bay but not Chesapeake Bay, did not provide an equivalent habitat to seagrass. Nutrient enrichment-related degradation of eelgrass habitat has diminished the overall capacity of estuaries to support fish populations.     

Comparison of the Salinity Structure of the Chesapeake Bay,the Delaware Bay and Long Island Sound Using a Linearly Tapered Advection-Dispersion Model

Long records of monthly salinity observations along the axis of Chesapeake Bay, Delaware Bay, and Long Island Sound are used to test a simple advection–dispersion model of the salt distribution in linearly tapered estuaries developed in a previous paper. We subdivide each estuary into three to five segments, each with linear taper allowing a distributed input of fresh water, and evaluate the dispersion in each segment. While Delaware Bay has weak dispersion and a classical sigmoidal salinity structure, Long Island Sound and Chesapeake Bay are more dispersive and have relatively small gradients in the central stretches. Long Island Sound is distinguished by having a net volume and salt flux out of its low-salinity end resulting in a smaller range of salinity and increasing axial gradients at its head rather than the usual asymptotic approach to zero salinity. Estimates of residence times based on model transport coefficients show that Long Island Sound has the most rapid response to fresh-water flux variations. It also has the largest amplitude cycle in river discharge fluctuation. In combination, these cause the large seasonal variation in the salinity structure relative to interannual variability in Long Island Sound as compared with Chesapeake Bay and Delaware Bay.     

Geographic signatures of North American West Coast estuaries

West Coast estuaries are geologically young and composed of a variety of geomorphological types. These estuaries range from large fjords to shallow lagoons; from large to low freshwater flows. Natural hazards include E1 Niños, strong Pacific storms, and active tectonic activity. West Coast estuaries support a wide range of living resources: five salmon species, harvestable shellfish, waterfowl and marine birds, marine mammals, and a variety of algae and plants. Although populations of many of these living resources have declined (salmonids), others have increased (marine mammals). West Coast estuaries are also centers of commerce and increasingly large shipping traffic. The West Coast human population is rising faster than most other areas of the U.S. and Canada, and is distributed heavily in southern California, the San Francisco Bay area, around Puget Sound, and the Fraser River estuary. While water pollution is a problem in many of the urbanized estuaries, most estuaries do not suffer from poor water quality. Primary estuarine problems include habitat alterations, degradation, and loss; diverted freshwater flows; marine sediment contamination; and exotic species introductions. The growing West Coast economy and population are in part related to the quality of life, which is dependent on the use and enjoyment of abundant coastal natural resources.     

A metabolism-based trophic index for comparing the ecological values of shallow-water sediment habitats

We determined fluxes of oxygen and nutrients between water and sediments at 21 sites primarily in Virginia and North Carolina estuaries, over the past 15 yr. These sites represented broad ranges in salinity, tidal amplitude, hydrology, nutrient availability, turbidity, light availability, depth, sediment grain size, and anthropogenic disturbance. In general, we found that heterotrophically dominated sediments had the potential to degrade water quality, whereas photoautotrophy in the sediments ameliorated this impact. We propose a benthic trophic state index as a management tool to make general assessments of the degree to which sediments support ecological processes related to photoautotrophy. The index can be based on simple measurements of metabolic parameters. We also evaluated the relative significance of variability in the index across a number of spatial and temporal scales. Reduced photoautotrophy and/or enhanced heterotrophy tended to be associated with finer-grained, organic-rich sediments. This sediment type was common in oligohaline areas at water depths exceeding 2 m. Temporally, autotrophy declined from winter to spring particularly at sandy sites, while interannual variability was more pronounced for mud sites. *** DIRECT SUPPORT *** A01BY074 00011     

Development and validation of an estuarine biotic integrity index

We tested hypotheses about how estuarine fish assemblages respond to habitat degradation and then integrated these responses into an overall index, the Estuarine Biotic Integrity Index (EBI), which summarized observed changes. Fish assemblages (based on trawl catches) and habitat quality were measured monthly or biweekly at nine sites in two estuaries from March 1988 to June 1990. Submerged aquatic vegetation habitats were classified as low or medium quality based on year-round measurements of chemical and physical characteristics (phytoplankton blooms; macroalgae; dissolved oxygen; nutrients; dredged channels). We tested 15 metrics and selected 8 for inclusion in the EBI: total number of species, dominance, fish abundance (number or biomass), number of nursery species, number of estuarine spawning species, number of resident species, proportion of benthic-associated fishes, and proportion abnormal or diseased. Fish assemblages in low-quality sites had lower number of species, density, biomass, and dominance compared with medium-quality sites. Fish abundance peaked in July and August, and was lowest in January to March. The seasonal cycle in low-quality sites was damped compared with medium-quality sites. Abundances of fishes using estuaries as a spawning and nursery area and of benthic species were lower in low-quality sites compared to medium-quality sites. The individual metrics and the overall index correlated with habitat degradation. The EBI based on biomass did not do better than the EBI based on number, indicating that the extra effort to obtain biomass may not be warranted. We suggest the EBI is a useful indicator of estuarine ecosystem status because it reflects the relationship between anthropogenic alterations in estuarine ecosystems and the status of higher trophic levels.     

Habitat utilization by small flatfishes in a North Carolina estuary

Distribution and abundance of flatfish species (<150 mm standard length) were related to habitat characteristics in the Newport River and Back Sound estuaries in North Carolina. Salinity, turbidity, depth, distance from marsh edge, benthic composition, and grain size were used to describe the different shallow water habitats from April through October 1994. One Scophthalmidae, seven Paralichthyidae, one Achiridae, and one Cynoglossidae species were collected during the study including juvenileParalichthys albigutta (gulf flounder),P. dentatus (summer flounder), andP. lethostigma (southern flounder) along with multiple age classes ofCitharichthys spilopterus (bay whiff),Etropus crossotus (fringed flounder),Symphurus plagiusa (blackcheek tonguefish), andTrinetes maculatus (hogchoker). Incidental catches ofAncylopsetta quadrocellata (ocellated flounder),C. macrops (spotted whiff), andScopthalmus aquosus (windowpane) were also made. Flatfish distributions among habitats varied by species, size within species, and season. Regardless of season, the highest densities of flatfishes were found in the upper estuary. All habitats were used by one or more species and most species occurred at several habitats. Some species were significantly more abundant at specific habitat types. Ontogenetic shifts in habitat utilization were found for several species. High densities of smallP. lethostigma, C. spilopterus, S. plagiusa, andT. maculatus occurred in the upper estuary on muddy substrates. LargeP. dentatus, C. spilopterus, S. plagiusa, andT. maculatus utilized sand flats and channels in the lower estuary.     

Fish-Habitat Relationships Along the Estuarine Gradient of the Sacramento-San Joaquin Delta,California: Implications for Habitat Restoration

Estuaries are highly variable environments where fish are subjected to a diverse suite of habitat features (e.g., water quality gradients, physical structure) that filter local assemblages from a broader, regional species pool. Tidal, climatological, and oceanographic phenomena drive water quality gradients and, ultimately, expose individuals to other habitat features (e.g., stationary physical or biological elements, such as bathymetry or vegetation). Relationships between fish abundances, water quality gradients, and other habitat features in the Sacramento-San Joaquin Delta were examined as a case example to learn how habitat features serve as filters to structure local assemblages in large river-dominated estuaries. Fish communities were sampled in four tidal lakes along the estuarine gradient during summer-fall 2010 and 2011 and relationships with habitat features explored using ordination and generalized linear mixed models (GLMMs). Based on ordination results, landscape-level gradients in salinity, turbidity, and elevation were associated with distinct fish assemblages among tidal lakes. Native fishes were associated with increased salinity and turbidity, and decreased elevation. Within tidal lakes, GLMM results demonstrated that submersed aquatic vegetation density was the dominant driver of individual fish species densities. Both native and non-native species were associated with submersed aquatic vegetation, although native and non-native fish populations only minimally overlapped. These results help to provide a framework for predicting fish species assemblages in novel or changing habitats as they indicate that species assemblages are driven by a combination of location within the estuarine gradient and site-specific habitat features.     

Salt-marsh benthic invertebrates: Small-scale patterns of distribution and abundance

Monitoring of small-scale distribution patterns of benthic invertebrates has demonstrated distinct trends in faunal abundances with position relative to individual culms of saltmarsh cordgrass,Spartina alterniflora, at Tar Landing Bay Marsh, near Morehead City, North Carolina. Samples containing culms ofSpartina yielded significantly higher abundances (at least three times) than did samples without them. Among common species, onlyNereis succinea did not show this effect. Matrix-arranged and randomly placed sets of samples have confirmed a positive relationship between cross-sectional area of culms in a sample (at the sediment-water interface) and contained numbers of macrofauna, juvenile macrofauna and meiofauna. These patterns occurred despite a decreased volume of sediment in samples containing culms. Heightened abundances of benthic invertebrates associated with structural elements at the sediment-water interface may result from either nonrandom recruitment (either active via recruit selectivity or passive through hydrogeographic effects of culms) or differential post-recruitment mortality (resulting from inhibition of epibenthic predators or from variable habitat quality).     

A possible effect of salinity fluctuation on abundance of benthic vegetation and associated fauna in Northeastern Florida Bay

In southern Florida, a vast network of canals and water control structures mediate freshwater discharge into the coastal zone. Management protocol for one such canal network (C-111) is being modified in part to try to improve habitat for estuarine fish and wading birds in northeastern Florida Bay, an estuarine part of Everglades National Park. Changes in canal management could alter the spatial and temporal salinity regime in the estuary. To better predict the effect of such changes on estuarine habitat, abundances of submersed vegetation and benthic animals were sampled repeatedly at 12 stations that differed in salinity. A variety of other parameters were also measured (nutrients, light, temperature, oxygen, sediment characteristics, and others). Mean salinity among stations ranged from 11.4‰ to 33.1‰. Densities of benthic plants and animals differed among stations by several orders of magnitude. The standard deviation of salinity was the best environmental correlate with mean plant biomass and benthic animal density: less biota occurred at stations with greater fluctuations in salinity. The two stations with the least plant biomass also had the highest mean water temperatures. In a stepwise multiple regression analysis, standard deviation of salinity accounted for 59% of the variation in the logarithm of mean plant biomass among stations. For every 3‰ increase in the standard deviation, total benthic plant biomass decreased by an order of magnitude. Mean water temperature accounted for only 14% of the variation, and mean salinity was not included for lack of significance. At stations with widely fluctuating salinities, not only was biomass low, but species dominance also frequently changed. Severe fluctuation in salinity may have prevented abundant benthos by causing physiological stress that reduced growth and survival. Salinity may not have remained within the range of tolerance of any one plant species for long enough to allow the development of a substantially vegetated benthic community. Hence, gaining control over salinity fluctuation may be the key to estuarine habitat improvement through canal management in southern Florida.     

Sediment grain size effect on benthic microalgal biomass in shallow aquatic ecosystems

Benthic microalgal biomass is an important fraction of the primary producer community in shallow water ecosystems, and the factors controlling benthic microalgal biomass are complex. One possible controlling factor is sediment grain-size distribution. Benthic microalgal biomass was sampled in sediments collected from two sets of North Carolina estuaries Massachusetts and Cape Cod bays, and Manukau Harbour in New Zealand. Comparisons of benthic microalgal biomass and sediment grain-size distributions in these coastal and estuarine ecosystems frequently showed a negative relationship between the proportion of fine-grained sediments and benthic microalgal biomass measured as chlorophylla. The highest sedimentary chlorophylla levels generally occurred in sediments with lower percentages of fine particles (diameter <125 mm). A negative relationship between the proportion of fine sediments and benthic microalgal biomass suggests anthropogenic loadings of fine sediment may reduce the biological productivity of shallow-water ecosystems.