Aureococcus anophageflerens: Causes and ecological consequences of brown tides in U.S. mid-Atlantic coastal waters

Aureococcus anq~ha&erens is a picoplanktonic alga that since 1985 has bloomed in coastal embayments of the western mid-Atlantic, ranging from Narragansett Bay, Rhode Island, to Barnegat Bay, New Jersey, with greatest incidence of rccurrencc in Long Island bays, New York. Blooms of this small alga, referred to as “brown tide,” can persist for several months during late spring and summer at densities in excess of 1.0X 10” cells ml-‘. They are not associated with anomalous chlorophyll a, dissolved oxygen, or inorganic macronutricnt (N, P) levels. Meterologically induced rcduccd flushing rates, elevated salinities, and delivery of micronutrients (e.g. iron) from the watershed have been implicated in bloom initiation. Brown tides have had severe detrimental cflccts on the bcnthos, especially celgrass (Zosteru marinn) and suspension-feeding bivalves, including bay scallops (Argopecten ivrudicms) and blue mussels (Mytilus erlulis). Adult bivalves experience sublethal effects (e.g. inhibition of clearance rates) at Aureococcus concentrations as low as -2X 10” cells mlI and mortalities at -10” cells ml I, attributed to toxicity of this microalga. Impacts of brown tide on zooplankton arc less clear, but reduced egg production rates of copepods and reduced population growth rates of’ ciliates are documented at higher brown tide concentrations (21.0X 10” cells ml .I). We summarize the state of knowledge about the physical, chemical, and biological factors that may contribute to brown tide initiation, maintenance, and decline and assess its ecological effects. Summer algal blooms of a small (-2-pm diam) picoplankter, Aureococcus anophngefferens, referred to as “brown tide” due to the resulting water discoloration, have occurred since 1985 in several noncontiguous bays of the midwestern Atlantic coast of the U.S. These include Narragansett Bay, Rhode Island, the Peconics-Gardiners Bay system and south-shore bays of Long Island, New York, and New Jersey bays (Fig. 1). Brown tides have been associated with major deleterious ecosystem effects within this region, most notably on herbivorous grazers. The causative organism, A. anophagefSerens Hargraves et Sieburth, a coccoid, nonmotile alga, has been classified as a chrysophyte (Sieburth et al. 1988). However, molecular phylogenctic studies support its inclusion within the Pelagophyceae, together with the species responsible for brown tides in the Laguna MadreBaffin Bay ecosystem, Texas (DeYoe et al. 1995). Absorption and fluorescence spectra of A. anophagefferens are more typical of oceanic phytoplankton, such as the related chrysophyte Pelagococcus .subviridis, thus suggesting an oceanic origin for this species (Yentsch et al. 1989). Despite widespread distribution of cells from the Gulf of Maine, to Great Bay, New Jersey, confirmed by immunofluorescent detection (Anderson et al. 1993), development of brown tides has been restricted to shallow, relatively unstratified estuaries (Fig. 1). They have not occurred in Long Island Sound, although Au’ Present address: Institute for Marine Biosciences, National Restarch Council, 14 11 Oxford Street, Halifax, Nova Scotia B3H 321. Acknowledgments WC thank R. Nuzzi and R. Waters for providing unpublished data used in this review. This paper is a result of research funded by NOAA award NA46RG0090 to the Research Foundation of SUNY for the New York Sea Grant Institute. This is contribution 1057 from the Marine Sciences Research Center. reococcus cells are present at low levels in nearshore Connecticut waters (Anderson et al. 1993). The first Aureococcus bloom occurred in summer 1985 and attained maximum densities of 0.9-I .5X 10” cells ml ’ in Narragansett Bay (Sieburth et al. 1988; Smayda and Villareal 1989). In Long Island bays Aureococcus cell densities exceeded 2.5X10” cells ml-’ (Fig. 2, Nuzzi and Waters 1989), but we note that A. anophagefferens identification by immunofluorescence (Anderson et al. 1989) was not available in 1985; thus this early estimate may be inaccurate due to inadvertent inclusion of’ morphologically similar species. In Long Island bays brown tides have reappeared over the past decade with varying intensity, duration, and geographic spread since the first outbreak in 1985 (Fig. 2). Although spatial distribution can be patchy, Aureococcus cell densities during blooms are generally highest at the western end of the Peconic-Gardiners Bay estuary, and decline toward the eastern end (Nuzzi and Waters 1989). Bloom densities (>0.5X 10b cells ml-‘) have occurred at localized sites (e.g. confined bays such as West Neck Bay) in years when brown tide did not extend thoughout the estuary (Fig. 2). Widespread, high concentrations (0.5-1.0X 10” cells ml ‘I) of Aureococcus cells recurred in summer 1995, with maxima >1.7X 10” cells ml-’ at some locations. Brown tide, presumed to have occurred in Barnegat Bay, New Jersey, in the mid1980s (Olsen 1989), was verified in New Jersey coastal waters in 1995 (Fig. 1). Sieburth and Johnson (I 989) identified A. unophageflerens as a minor component of Narragansett Bay plankton in water samples taken 3 yr before the 1985 brown tide. Although brown tide has not developed in Rhode Island waters since 1985, its presence has been repeatedly documented in experimental mesocosms fed Narragansett Bay water (Keller and Rice 1989; Nixon et al. 1994), suggesting that it may pose a threat to this ecosystem under favorable environmental conditions. Aureococcus blooms typically develop in late May, attain