Spatial Distribution of Modern Dinoflagellate Cysts in Polluted Estuarine Sediments from Buzzards Bay (Massachusetts, USA) Embayments
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MARINE ECOLOGY PROGRESS SERIES Vol. 292: 23–40, 2005 Published May 12 Mar Ecol Prog Ser Spatial distribution of modern dinoflagellate cysts in polluted estuarine sediments from Buzzards Bay (Massachusetts, USA) embayments Vera Pospelova1, 2,*, Gail L. Chmura1, Warren S. Boothman3, James S. Latimer3 1Department of Geography and Centre for Climate and Global Change Research, McGill University, 805 Sherbrooke Street West, Montreal, Quebec H3A 2K6, Canada 2School of Earth and Ocean Sciences, University of Victoria, Petch 168, PO Box 3055 STN CSC, Victoria, British Columbia V8W 3P6, Canada 3US Environmental Protection Agency, Office of Research and Development, NHEERL, Atlantic Ecology Division, Narragansett, Rhode Island 02882, USA ABSTRACT: Analysis of the spatial distribution of the dinoflagellate cyst assemblages in 19 surface sediment samples collected from 3 Buzzards Bay (Massachusetts, USA) embayments revealed the potential applicability of dinoflagellate cysts as biological indicators of environmental conditions in estuarine systems. Sites with the highest levels of toxic pollution and hypertrophic conditions are characterized by the lowest dinoflagellate cyst species-richness and concentrations. Among the abi- otic factors influencing the distribution of dinoflagellate cysts, nutrients and toxic pollution are the major controls, as in these embayments salinity and temperature variability is low. Principal compo- nent analysis, based on the proportions of cyst taxa, indicated that cyst assemblages gradually change when moving away from the sources of nutrient pollution, sewage outfalls in particular. KEY WORDS: Dinoflagellate cyst · Eutrophication · Heavy metals · Sewage · Wastewater treatment plant · PCBs · Apponagansett Bay · New Bedford Harbor Resale or republication not permitted without written consent of the publisher INTRODUCTION have proven to satisfy all the above criteria (Fensome et al. 1996). Human activities such as nutrient enrichment and Dinoflagellates are single-celled organisms that con- toxic pollution cause water-quality degradation and stitute an important part of the phytoplankton population habitat loss. These activities are most intensive in estu- in aquatic ecosystems. During their life cycle some di- aries with highly urbanized and industrialized water- noflagellates produce hypnozygotes, or resting cysts, sheds. Concern about water-quality degradation in which can be preserved in sediments (Fensome et al. estuarine waters has stimulated a demand for develop- 1993). The assemblages of dinoflagellate cysts in sedi- ment of indicators of nutrient enrichment and toxic ments encode information on the dinoflagellates in the contamination to examine paleo- and modern environ- upper water column (Dale 1976, Reid & Harland 1978). mental conditions and trends caused by intensified In turn, the population of dinoflagellates is influenced by anthropogenic activities in watersheds. environmental factors such as temperature and salinity, To be a useful biological indicator of environmental nutrients, turbidity and pollution (Taylor 1987). Dinofla- conditions, an organism has to satisfy certain criteria gellate cysts recovered from coastal sediments have the (Gibson et al. 2000). In general, a biological indicator potential to provide substantial information on biological should be ubiquitous, well preserved in sediments, processes and interactions within aquatic systems. numerous enough for statistical treatment, and reflect Several studies have examined the temporal devel- certain environmental parameters. Dinoflagellate cysts opment of estuarine eutrophication and pollution by *Present address: Victoria. Email: [email protected] © Inter-Research 2005 · www.int-res.com 24 Mar Ecol Prog Ser 292: 23–40, 2005 analyzing the dinoflagellate cyst records in sediment ° ° N Acushnet River 70 54’ W 70 52’ W cores (Dale & Fjellså 1994, Sætre et al. 1997, Thorsen & Boston Dale 1997, Dale et al. 1999, Matsuoka 1999, 2001, Dale MA 2001, Pospelova et al. 2002). A recent study of the his- RI Sediment Sites CT torical records of dinoflagellate cysts from shallow un- Sewage Outfall Combined Sewer stratified embayments of Buzzards Bay (New Bedford Overflows NBH146 an Atlantic Oce Flood-tidal Harbor and Apponagansett Bay) found that species NBH154 current direction richness (number of taxa), total cyst concentrations and NBH2c Core sites New Bedford Harbor fluxes, proportions of some heterotrophic species, as NBH204 NBH5c FAIRHAVEN well as abundance of indicator species changed as a re- Inner Harbor Popes Island 41° 38’ N sult of eutrophication and toxic pollution (Pospelova et NBH236 Fairhaven S.O. al. 2002). In oligotrophic systems, such as New Bedford NBH247 Harbor in its early history (Pospelova et al. 2002), nutri- NEW Group I BEDFORD ent enrichment initially increases dinoflagellate cyst hurricane barrier species-richness. However, under highly eutrophic and Outer Harbor polluted conditions, species diversity declines, as seen 41° 36’ N during the 20th century in New Bedford Harbor. These DARTMOUTH Clarks extreme conditions are also characterized by large fluc- Clarks NBH317 Apponagansett Cove point tuations in total cyst concentrations and fluxes. The CPC Bay New Bedford S.O. proportion of cysts of heterotrophic dinoflagellates, AB1 CPB AB2 NBH325 Polykrikaceae and Diplopsalidaceae in particular, AB3 NBH324 CPE AB4 CPG tends to increase with increasing nutrient enrichment. AB5 AB1c NBH331 Group III If the dinoflagellate cyst record reflects the temporal 41° 34’ N 1 km changes of the environmental conditions in an estuary, Group II NBH346 Buzzards Bay it must also show spatial change, as environmental con- ditions in an estuary are non-uniform. If so, dinoflagel- Fig. 1. New Bedford Harbor, Clarks Cove and Apponagansett late cyst assemblages from surface samples can be used Bay showing location of surface sediment samples. Direction to support or discard some of the conclusions previously of tidal-flood current from Howes et al. (1996), locations of 3 made about the ‘eutrophication and pollution signals’ core sites from Pospelova et al. (2002) drawn from analyses of dinoflagellate cysts in the cores. No previous studies have investigated spatial distribu- tidal range is about 1 m; the direction of tidal-flood cur- tions of dinoflagellate cysts in relation to eutrophication rent is shown in Fig. 1. and toxic pollution in estuarine systems. This work rep- Mean summer (June, July and August) water salinity resents the first analysis of this kind. varies from 28 to 31 and summer temperatures from 21 In this study we document the dinoflagellate cyst to 23°C (Howes et al. 1999). Concentrations of nutri- assemblages on a ~1 km scale in 3 side embayments of ents and chlorophyll a for the studied embayments are Buzzards Bay, Massachusetts. Comparison of these provided in Table 1. Ammonium is the major form of assemblages to known gradients of nutrient and toxic inorganic nitrogen available throughout the Bay and pollution allows us to assess the utility of cysts as indi- its concentrations are heavily influenced by the cators of plankton response. sewage outfall (Borkman & Turner 1993). A study of economic growth and environmental change in Buz- zards Bay (Terkla et al. 1990) has identified population MATERIAL AND METHODS growth as the dominant factor currently affecting the environmental health of Buzzards Bay. Study area. New Bedford Harbor, Clarks Cove and New Bedford Harbor: New Bedford Harbor, also Apponagansett Bay are side embayments of the north- known as the Acushnet River estuary, has a moderate western shore of Buzzards Bay, Massa- chusetts, USA (Fig. 1). The embay- Table 1. Comparison of mean summer (June to August) concentrations of nutri- ents and chlorophyll a in embayments of Buzzards Bay ments are shallow, with water depths ranging from 1 to 12 m (mean 6 m), generally well mixed, and unstratified. Location Nitrate Ammonium Phosphate Chlorophyll a (µM) (µM) (µM) (µg l–1) There are no major bottom currents in Buzzards Bay, and most of the environ- Inner New Bedford Harbor 11.00 5.7 1.8 8.5 mental energy is in tidal currents and Clarks Cove 1.5 0.9 1.5 3.7 Apponagansett Bay 1.3 2.2 1.6 4.7 waves (Summerhayes et al. 1985). The Pospelova et al.: Dinoflagellate cysts in polluted estuaries 25 freshwater input (median flow 0.54 m3 s–1) from the Clarks Cove: In contrast to New Bedford Harbor, the river flowing into the northern part of the harbor. This neighboring Clarks Cove (Fig. 1) has relatively good harbor is heavily urbanized, as it is surrounded by 35% water quality because of the absence of major freshwa- of the population of the entire Buzzards Bay watershed ter sources and a sewered watershed, with discharges (Howes et al. 1999). As a result, ~20 combined sewer located at Clarks Point (New Bedford Wastewater overflows (CSO) discharge into the inner part of New Treatment Plant). Clarks Cove water quality is main- Bedford Harbor, in addition to the outfall of the tained primarily by its tidal dynamics (Howes et al. Fairhaven Wastewater Treatment Plant (Fig. 1). From 1999). Despite the fact that Clarks Cove is a compara- 1974 to 1996, the Fairhaven facility has continuously tively deep (~9 m) and well-flushed embayment, the discharged primary-treated sewage to the harbor, total nitrogen level here is higher than in the waters of resulting in a load of 140 t N yr–1 (SAIC 1991). A hurri- outer Buzzards Bay. This enrichment of Clarks Cove cane barrier greatly reduces water circulation relative waters comes from the