ARTICLE IN PRESS · 2003. 10. 6. · ARTICLE IN PRESS UNCORRECTED PROOF 140 and August are the warmest months of the year, 141 while January and February are the coldest with 142

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FEnvironmental factors in£uencing the spatial distribution ofdino£agellate cyst assemblages in shallow lagoons of southern

New England (USA)

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Vera Pospelova a;�, Gail L. Chmura a, Henry A. Walker b4a Department of Geography and Centre for Climate and Global Change Research, McGill University, 805 West Sherbrooke Street,

Montreal, QC, Canada H3A 2K6b U.S. Environmental Protection Agency, O⁄ce of Research and Development, NHEERL, Atlantic Ecology Division, Narragansett, RI

02882 USA

5678

9 Abstract1011 Surface sediment samples from 24 sites within eleven back-barrier lagoons of Rhode Island and Massachusetts12 (USA) contain abundant (200^6000 cysts cm33) and diverse (up to 40 taxa) dinoflagellate cyst assemblages. The13 lowest cyst concentrations and diversity are observed in lagoons with low salinity (6 10). The pattern of spatial14 distribution of dinoflagellate cysts in these shallow estuarine environments is described. We assessed the relationship15 between the available multi-year water quality data and the composition of the dinoflagellate cyst assemblages using16 canonical correspondence analysis. Temperature and salinity are found to be the primary abiotic factors influencing17 cyst distribution in the coastal lagoons.18 : 2003 Published by Elsevier B.V.1920 Keywords: dino£agellate cysts; estuaries; nutrients; Waquoit Bay; temperature; salinity21

22 1. Introduction

23 Coastal lagoons and bays are characteristic fea-24 tures of the southern New England coastline. La-25 goons are generally de¢ned as estuarine systems26 characterized by shallow depth, a well-mixed27 water column, slow £ushing, and minimal input28 of freshwater (Boynton et al., 1982). In the past29 few decades these ecosystems have undergone sig-30 ni¢cant changes as a result of watershed develop-31 ment (Darnell and Soniat, 1981; Nixon, 1982;

32Lee and Olsen, 1985; Avanzo and Kremer,331994). In some lagoons, coastal eutrophication34has become a serious threat, and so programs35has been established to monitor water quality.36These monitoring programs have made available37long-term databases of water chemistry measure-38ments at high temporal and spatial resolution.39The availability of multi-year water chemistry40data for the southern New England estuaries cre-41ates a unique opportunity to evaluate the impor-42tance of the abiotic factors that a¡ect the distri-43bution of the dino£agellate cyst assemblages in a44variety of lagoons, all located within the same45climatic zone. Our research program is the ¢rst46detailed study of the dino£agellate cyst assem-47blages in surface sediment samples from the

1 0034-6667 / 03 / $ ^ see front matter : 2003 Published by Elsevier B.V.2 doi:10.1016/S0034-6667(03)00110-6

* Corresponding author. Tel. : +1-250-721-5346; Fax: +1-514-398-7437.

E-mail address: [email protected] (V. Pos-pelova).5

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48 back-barrier lagoons of Rhode Island and Massa-49 chusetts (USA). The aim of this paper is to docu-50 ment the occurrence of the dino£agellate cyst51 taxa, their spatial distribution and relationship52 to hydrographic conditions.53 It is widely recognized that the distribution of54 modern dino£agellate cysts in oceanic and marine55 environments is mostly controlled by water tem-56 perature, salinity and the availability of nutrients57 (Dale, 1996; de Vernal et al., 1997; Rochon et al.,58 1999; Devillers and de Vernal, 2000; de Vernal et59 al., 2001). Our study questions whether the same60 factors can be related to the distribution of dino-61 £agellate cysts at the much smaller spatial scales62 needed to characterize variability in hydrographic63 conditions in lagoons. The variability in hydro-64 graphic conditions in lagoons is responsible for65 the recognized patchy character in the distribution

66of phytoplankton (Smayda, 1980), which should67lead to a similarly heterogeneous pattern of dino-68£agellate cyst distribution (Blanco, 1995). Because69lagoons are characterized by relatively rapid sed-70imentation rates, it is possible to create a set of71surface analogues that can be paired to measure-72ments from recent monitoring programs. If sedi-73mentary assemblages of dino£agellate cysts re£ect74the living population in overlying waters, then we75expect to ¢nd cyst assemblages to vary with di¡er-76ences in water chemistry.77The results of this study have application to78paleoenvironmental studies in estuaries. They79also contribute to our understanding of how hu-80man alteration of environmental conditions in la-81goons a¡ect populations of cyst-producing dino-82£agellates.

11 Fig. 1. (A) Map of southern New England showing the locations of lagoons on the Rhode Island (I) and Massachusetts (II)2 coasts. (B) Locations of the sample stations (represented by black dots) in Waquoit Bay and Jehu Pond. (C) Locations of the3 sample stations in the nine Rhode Island lagoons.

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83 2. Study area

84 Our study includes 11 back-barrier lagoons in85 southern New England. Nine lagoons are located86 in southern Rhode Island, on Block Island Sound.87 The remaining two are on the coast of Massachu-88 setts’ Vineyard Sound (Fig. 1). Although called89 Waquoit ‘Bay’, this system on the Massachusetts90 coast is a shallow semi-enclosed estuary and can91 be classi¢ed as a large lagoon.

92 2.1. Physical characteristics

93 Coastal lagoons, locally called salt ponds, are94 situated behind narrow (200^300 m wide) sandy95 dunes, up to 3^4 m high. The barriers are topped96 by ocean waters only during severe storm events97 (e.g. hurricanes). The lagoons are elongated (Fig.98 1) and are parallel to the barriers, with the excep-99 tion of Point Judith, Potter Pond, and Waquoit

100 Bay that have their long axis oriented perpendic-101 ular to the coast.102 Physical characteristics of the lagoons are com-103 pared in Table 1. Waters are shallow with an104 average depth of V1^2 m, unstrati¢ed, and char-105 acterized by low turbidity (Lee, 1980; WBNERR,106 1996). The primary variant among these estuaries107 is the exchange with oceanic waters. Twice a day108 V2^4% of the lagoon water exchanges with109 ocean waters through barrier inlets (Sheath and110 Harlin, 1988). The tidal range averages 1.1 m on

111the ocean side and is 7^12 cm in most of the112lagoons, but about 50 cm in Waquoit Bay.113In the past, ephemeral, natural inlets were the114primary mechanism for the introduction of ocean115waters. Today many inlets or ‘breachways’ have116been permanently stabilized by jetties constructed117during the ¢rst half of the twentieth century.118Point Judith Pond has the largest inlet (75 m119wide, 9 9 m deep) maintained for access by a120commercial ¢shing boats. Potter Pond has no di-121rect opening to the sound but receives o¡shore122waters by way of a narrow channel (7 m wide,1236 1.3 m deep) dug between it and Point Judith124Pond. Green Hill Pond receives marine waters125through a smaller channel from neighboring Ni-126nigret Pond. Waquoit Bay has two inlets. Its east-127ern inlet connects directly to the Bay, and the128western inlet is on the adjacent Eel Pond. Jehu129Pond is indirectly linked to marine waters through130permanent channels to Waquoit Bay. Trustom,131Maschaug, and Card’s Ponds have no permanent132inlets. These three ponds are isolated from marine133waters except for occasional breaching.

1342.2. Environmental characteristics

135Southern Rhode Island and eastern Massachu-136setts are characterized by a humid, continental137climate with strong maritime in£uence. This pro-138duces a moderate annual temperature range with139mild winters and prolonged, cool summers. July

Table 1Characteristics of the lagoons in this study (Boothroyd et al., 1985; Giblin, 1990; Lee et al., 1997; Brawley et al., 2000)

Area (hectares) Average depth Average Aug. temperature Average salinity1

Waterbody Watershed (m) (‡C)2

Rhode Island3Point Judith 613 1432 1.8 22 294Potter 133 1341 0.6 22 275Card’s 17 737 0.4 23 46Trustom 65 322 0.4 25 57Green Hill 175 1231 0.8 23 198Ninigret 693 2440 1.2 23 249Quonochontaug 298 934 1.8 21 2910Winnapaug 181 929 1.5 23 2811Maschaug 19 140 2.1 24 712Massachusetts13Waquoit Bay 375 4955 0.8 24 2914Jehu 78 422 2.0 23 2915

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140 and August are the warmest months of the year,141 while January and February are the coldest with142 the mean high temperature through the winter143 above freezing. The average winter water temper-144 ature in the lagoons is V3‡C and the average145 summer temperature is V23‡C (Lee et al., 1997;146 WBNERR, 1996). There are large variations in147 mean summer temperature between the lagoons148 and sometimes between di¡erent stations within149 the same lagoon. The lowest mean summer tem-150 perature is measured in Point Judith Pond, with151 little di¡erence between two stations152 (V19‡CQ0.5‡C). Waquoit Bay and Card’s Pond153 have the warmest waters with the mean summer154 temperature V25‡C. The largest range of mean155 summer temperature within a single lagoon156 (s 3‡C) is recorded in Potter Pond.157 Salinity within the lagoons depends upon pre-158 cipitation events and its connection to the sea is159 permanent or temporary. The average annual pre-160 cipitation in the area is about 105 cm with the161 maxima occurring in November^December and162 the minima in June^July (Hoare, 1996). Trustom,163 Maschaug, and Card’s Ponds, with no permanent164 inlets to Block Island Sound, have the lowest sa-165 linity (4^7) whereas Point Judith, Quonochontaug166 Ponds and Waquoit Bay have the highest salinity167 (V29) (Table 1). The largest range in the mean168 summer salinity within a single system (V5) is169 observed in Ninigret Pond.170 As a result of the low freshwater runo¡ into the171 lagoons, nutrient inputs to these systems are gen-172 erally lower than in other estuaries (Nixon, 1982).173 Concentrations of nutrients in the waters are sea-174 sonally variable. The concentration of nitrates,175 which varies from 0.2 to 43.6 WM l31, is highest176 in February^March, decreases during the spring177 and reaches its minimum in July^August. In con-178 trast, the concentration of inorganic phosphorus,179 which ranges from 0.1 to 2.2 WM l31, is lowest in180 the spring (March^April), rises through summer181 and reaches its maximum in late summer (Lee et182 al., 1997). The concentration of phosphorus with-183 in the lagoons is always lower than the concen-184 trations observed o¡shore, whereas the concentra-185 tion of nitrogen is higher.

1863. Materials and methods

1873.1. Station locations and sediment collection

188Surface sediments were collected from 24 water189quality monitoring stations (Fig. 1). Samples were190taken at multiple stations in most of the lagoons.191Distance among the stations within the lagoons192varies from 150 to 2000 m and averages about193500 m. Stations 6, 7, and 8 of Potter Pond are194located in coves where water circulation is re-195stricted. Potter Pond station 5 is near the inlet196on a sandy subtidal £at. Point Judith station 1197is situated at the northern end of the pond in a198cove that receives the discharge of the Saugatuck-199et River. Thus, freshwater in£ow to upper Point200Judith Pond is considerably higher than to the201other lagoons. Ninigret Pond has three stations:20212, 13 and 14. Stations 12 and 14 are located in203low-energy basins. Green Hill Pond stations 9, 10204and 11 are in the coves where circulation is re-205stricted. Stations 16 and 16A of Quonochontaug206Pond are located in the western part of the pond,207whereas station 18 is in the eastern part. Winna-208paug Pond has three stations: stations 19 and20919A are in the western part of the lagoon, which210is the most distant from the inlet, and station 21 is211in the northern low-energy basin. Waquoit Bay212has one station (65) in its northern section. Sta-213tion 66 is in the central part of Jehu Pond in a214cove with restricted water circulation.215Surface sediments were collected with a grab216corer deployed from a small boat or by hand,217using a mini-piston corer. The top 2 cm were re-218tained from each of 3 replicate cores taken within219a radius of 3 m. In these rapidly accreting sys-220tems, the upper 2 cm of sediments represent less221than 10 years of deposition (Boothroyd et al.,2221985). Sediments are characterized as ¢ne sand,223silt and mud. All 24 samples were stored frozen224prior to sectioning and further analysis.

2253.2. Sample preparation

226Sediment samples of known volume were ¢rst227dried at room temperature, then treated with cold22810% hydrochloric acid (HCl) to remove calcium229carbonate particles. Material was then rinsed

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230 twice with distilled water and sieved through 125-231 Wm and retained on 10-Wm nylon mesh to elimi-232 nate coarse and ¢ne material. To dissolve siliceous233 particles, samples were placed in a water bath234 with 40% hydro£uoric acid (HF) for 20 min,235 then treated for 10 min with cold HCl (10%).236 The residue was rinsed twice with distilled water,237 sonicated for 1^2 min and ¢nally collected on a238 10-Wm mesh. Calibrated tablets of Lycopodium239 spores (13 911 spores per tablet), added during240 processing (Stockmarr, 1977), allowed for calcu-

241lation of dino£agellate cyst concentrations based242on the volume of sediments. Aliquots of residue243were mounted in glycerine jelly, and dino£agellate244cysts were studied under a light microscope (63U245and 100U objectives).

2463.3. Dino£agellate cyst analysis

247Identi¢cation of dino£agellate cysts was made248on the basis of published descriptions in accor-249dance with taxonomy given in Lentin and Wil-

Table 2Taxonomic citation of dino£agellate cysts used in this study

Cyst species (paleontological name) Dino£agellate thecate name or a⁄nity (biological name)1

Ataxiodinium choane Gonyaulax spinifera complex2Alexandrium tamarense3

Brigantedinium cariacoens Protoperidinium avellanum4Brigantedinium simplex Protoperidinium conicoides5Brigantedinium spp. ? Protoperidinium spp.6Dubridinium spp. Diplopsalid group7

Gymnodinium spp.8Impagidinium spp. ? Gonyaulax sp. indet.9Islandinium brevispinosum Protoperidinium sp. indet.10Islandinium minutum Protoperidinium sp. indet.11Islandinium ? cezare Protoperidinium sp. indet.12Lejeunecysta oliva Protoperidinium sp. indet.13Lejeunecysta sabrina Protoperidinium leonis14Lingulodinium machaerophorum Lingulodinium polyedrum15Nematosphaeropsis spp. Gonyaulax spinifera complex16Operculodinium centrocarpum sensu Wall and Dale, 1966 Protoceratium reticulatum17Operculodinium israelianum ? Protoceratium reticulatum18

Pentapharsodinium dalei19Peridinium limbatum20Pheopolykrikos hartmannii21Polykrikos kofoidii22Polykrikos schwartzii23Protoperidinium americanum24Protoperidinium minutum25Protoperidinium nudum26

Protoperidinium spp. indet Protoperidinium group27Quinquecuspis concreta Protoperidinium leonis28Selenopemphix nephroides Protoperidinium subinerme29Selenopemphix quanta Protoperidinium conicum ; P. nudum30Spiniferites elongatus Gonyaulax spinifera complex31Spiniferites spp. Gonyaulax spinifera complex32Stelladinium stellatum Protoperidinium stellatum33Tectatodinium pellitum Gonyaulax spinifera complex34Trinovantedinium applanatum Protoperidinium pentagonum35Tuberculodinium vancampoae Pyrophacus steinii36Votadinium calvum Protoperidinium oblongum37Votadinium spinosum Protoperidinium claudicans38

Thecal equivalents are taken from Head (1996), Rochon et al. (1999) Head et al. (2001), Pospelova and Head (2002).39

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Table 3Relative abundance (%) of dino£agellate cyst taxa in our samples. Asterisks denote taxa not counted for cyst richness, including the freshwater Protoperidinium wis-consinense

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250 liams (1993). When species-level identi¢cation was251 not possible, identi¢cation was done at the genus252 level. The dino£agellate cyst nomenclature con-253 forms to Head (1996), Rochon et al. (1999),254 Head et al. (2001) and Pospelova and Head255 (2002). A list of counted dino£agellate cysts and256 their known thecal equivalent is provided in Table257 2. From 33 to 1448 cysts were counted in each258 sample (Table 3), averaging 300 cysts. Card’s259 Pond was excluded from statistical analysis be-260 cause of the low cyst count in this sample.261 More than 40 dino£agellate cyst taxa were262 identi¢ed in the sediment samples. For statistical263 treatment some taxa were grouped together on264 the basis of morphological similarities. In partic-265 ular, species of the genus Brigantedinium (B. car-266 iacoense and B. simplex) were grouped together267 because cyst folding or orientation sometimes ob-268 scured the archeopyle characteristics, thus pre-269 venting identi¢cation to the species level. Since270 the distinction between Protoperidinium nudum271 and Selenopemphix quanta is debatable (Head,272 1996; Rochon et al., 1999) we also grouped these273 species together. Because of great morphological274 variability among the species of the genus Spini-275 ferites, all taxa excluding S. elongatus were276 grouped as Spiniferites spp.277 Prior to statistical treatment, dino£agellate cyst278 data were transformed as described by de Vernal279 et al. (2001). A natural log (ln) transformation280 was applied to percentage data to increase the281 weight of less represented taxa as these species282 often have more narrow ecological a⁄nities and283 are likely to be most diagnostic of environmental284 conditions (de Vernal et al., 2001). In order to285 deal with whole numbers and to avoid decimals,286 which yield negative values when they are loga-287 rithmically transformed, we expressed relative288 abundance per thousand, instead of per cent. An-289 other minor modi¢cation was to replace zero val-290 ues with one (1) in order to deal with values great-291 er than zero. Thus, the relative abundances of292 dino£agellate cyst taxa range from 1 to 1000 be-293 fore logarithmic transformation.

294 3.4. Hydrological data

295 Water quality conditions in the lagoons were

296monitored over a period of years (3^9 yr) by vol-297unteer ‘Pondwatchers’ (Lee et al., 1997), sta¡ of298the Waquoit Bay National Estuarine Research299Reserve (WBNRR) and a group of researchers300lead by Dr. I. Valiela (Boston University, MA).301These groups measured temperature, salinity, ni-302trates, phosphates, and chlorophyll a on a303monthly or weekly basis. Measurements were tak-304en at a depth of approximately 30 cm below the305water surface. Water clarity was measured as sec-306chi depth. However, the shallowness of most of307the sites limits the usefulness of this parameter308and rather determines water depth at the site.309Compilation of mean water depth (D), tempera-310ture (T), salinity (S), nitrates (N), phosphates (P)311and chlorophyll a (Chl) for winter (w; December^312January^February), summer (s; June^July^Au-313gust), and September (st) for each sampling sta-314tion are summarized in Table 4.315To reduce bias in interpretation of the multi-316variate results, environmental variables of high317inter-collinearity were eliminated with the excep-318tion of one representative variable. Thus, mean319monthly measurements for individual months320(June, July and August) were dropped from the321environmental data because of collinearity, and322mean summer values were used. Data on winter323water parameters, including temperature, are in-324complete, but we are aware that the lagoons325sampled can become ice-covered in cold winters.326We selected the entire summer season and Sep-327tember values for statistical analysis, although328values for August and February are commonly329used to explain dino£agellate cyst distribution in330high latitudes (Rochon et al., 1999). Studies of331temporal distribution of phytoplankton in tem-332perate North American estuaries indicate that di-333no£agellates are most abundant during the entire334summer period and at the beginning of the fall335(Smayda, 1980).

3363.5. Statistical methods

337Relationship between environmental data and338dino£agellate cyst species abundances were as-339sessed with Canonical Correspondence Analysis340(CCA), a widely used method for direct gradient341analysis. It is a constrained correspondence anal-

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Table 4Compilation of the mean water quality parameters and the water depth for each individual sample site

Winter Summer September1

Lagoon Station D T S N P Chl T S N P Chl T S N P Chl2

Green Hill 9 1.3 2.2 11.9 26.6 0.6 0.7 21.9 20.3 0.7 0.4 3.3 18.5 20.3 0.8 0.4 2.23Green Hill 10 1.5 3.1 21.0 14.6 0.2 1.9 22.6 18.9 3.8 0.6 5.1 20.2 21.6 2.0 0.5 3.84Green Hill 11 0.9 N/A N/A N/A N/A N/A 22.4 20.0 5.1 0.6 4.9 19.8 19.4 4.1 0.4 6.95Ninigret 12 2.7 4.1 24.5 0.8 0.2 8.3 22.0 23.4 0.4 0.6 7.4 19.7 24.4 0.8 0.7 10.36Ninigret 13 1.5 5.0 31.0 6.0 1.1 2.4 20.4 26.2 2.4 0.8 5.5 18.6 25.4 3.2 0.6 3.57Ninigret 14 1.2 N/A N/A N/A N/A N/A 23.3 21.1 1.8 0.5 6.9 20.1 21.2 2.4 0.4 11.18Point Judith 1 1.7 5.3 30.3 1.7 0.3 1.0 19.6 28.1 0.3 0.5 1.8 18.0 28.2 1.1 0.4 2.49Point Judith 4 5.3 N/A N/A N/A N/A N/A 19.1 28.5 0.3 0.4 2.2 19.8 30.8 0.4 0.3 2.610Potter 5 0.7 3.0 28.7 4.0 0.7 0.7 19.7 26.8 0.7 0.8 4.7 17.2 25.5 0.7 0.7 4.411Potter 6 1.4 N/A N/A N/A N/A N/A 21.6 26.3 1.7 0.8 13.0 18.8 26.8 3.3 0.5 16.412Potter 7 1.8 N/A N/A N/A N/A N/A 22.8 25.7 0.9 0.9 6.6 20.5 26.6 0.8 0.7 8.113Potter 8 1.1 N/A N/A N/A N/A N/A 22.7 26.5 1.1 0.4 5.6 18.8 27.1 1.2 0.3 5.414Quonochontaug 16 1.9 N/A N/A N/A N/A N/A 20.5 28.0 0.5 0.9 3.8 18.7 27.5 0.3 0.6 3.815Quonochontaug 16A 2.0 3.1 29.2 2.3 0.5 4.6 20.5 28.7 0.7 0.8 2.9 17.3 29.1 0.8 0.7 3.116Quonochontaug 18 3.0 N/A N/A N/A N/A N/A 19.6 29.0 0.4 0.6 2.9 17.5 30.1 0.4 0.6 2.717Trustom 60 2.3 N/A N/A N/A N/A N/A 23.0 4.0 0.3 0.2 2.2 19.0 3.0 0.0 0.4 25.418Trustom 61 2.0 N/A N/A N/A N/A N/A 23.0 4.0 0.3 0.2 2.2 19.0 3.0 0.0 0.4 25.419Winnapaug 19 0.9 5.0 30.0 1.7 2.2 5.5 22.9 27.6 1.2 0.7 6.2 20.9 28.2 1.6 0.4 7.820Winnapaug 19A 0.8 1.0 26.0 8.2 0.6 1.0 22.1 26.7 1.6 1.0 20.4 18.6 27.0 3.7 0.9 9.321Winnapaug 21 1.6 N/A N/A N/A N/A N/A 20.3 28.1 0.6 0.5 6.3 18.9 28.7 1.0 0.7 3.722Waquoit 65 2.3 4.4 29.4 N/A N/A N/A 24.6 27.9 0.7 0.8 5.5 21.3 27.8 0.2 0.6 3.223Jehu 66 2.8 3.4 27.9 N/A N/A N/A 23.7 28.8 0.7 N/A 7.5 20.4 28.8 0.1 N/A N/A24Machaug 30 1.6 N/A 10.0 0.6 0.1 N/A 23.2 7.2 0.2 0.2 13.6 19.3 6.0 0.3 0.3 4.925Card’s 33 1.2 2.5 0.0 43.6 1.1 2.5 24.4 3.6 6.2 1.1 11.0 19.8 4.0 4.4 0.6 20.926Mean values all 1.8 3.5 23.1 10.0 0.7 2.9 21.9 22.3 1.4 0.6 6.3 19.2 22.5 1.4 0.5 8.127

Environmental parameters selected for CCA are in bold.D, depth (m); T, temperature (‡C); S, salinity; N, nitrates (WM l31) ; P, phosphates (WM l31) ; Chl, chlorophyll a (Wg l31).

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F342 ysis with selected environmental variables (ter343 Braak, 1995, 1996). The analysis is an eigenanal-344 ysis method applied to a matrix of dino£agellate345 cyst data (samples-by-taxa) and, simultaneously,346 to a matrix of environmental data (samples-by-347 water quality measurements) to identify patterns348 of distribution and in£uence among species and349 environmental variables. CCA was performed us-350 ing the CANOCO program (CANOCO Version351 4.02, Agricultural Mathematics Group, Wagenin-352 gen, The Netherlands).353 The relationship between dino£agellate cyst dis-354 tribution and environmental parameters was iden-355 ti¢ed by species scores and their ordination pat-356 terns. Forward selection was used to identify the357 variables that could e¡ectively explain the greatest358 amount of variance in the species data sets. The359 signi¢cance of each environmental variable was360 determined by testing the signi¢cance of the ¢rst361 canonical axis using Monte Carlo testing (based362 on 999 unrestricted permutations). On the CCA363 biplot, environmental variables are represented by364 arrows, which extend in both directions from the365 center although only the positive direction is366 shown. The arrows point in the direction of max-367 imum variation and length of the arrows demon-368 strates the relative importance of each environ-369 mental variable. The center of the ordination370 diagram indicates the mean value for each envi-371 ronmental variable. The greater the angle between372 two environmental arrows, the less likely that they373 are related to one another. The projection of spe-

374cies scores against these arrows allows for infer-375ences to be made about the dominant environ-376mental factors a¡ecting species composition (ter377Braak and Prentice, 1988).

3784. Results

379Dino£agellate cysts were recovered from all the380sediment samples. Total cyst concentrations range381from 102 to 103 cysts cm33 (Table 3). The lowest382concentrations (6 300 cysts cm33) are from sta-383tions in Trustom and Maschaug Ponds, as well as384Green Hill station 9. However, even these low385numbers probably re£ect high productivity, as386sedimentation rates in these lagoons are relatively387high (V0.2 cm yr31 ; Boothroyd et al., 1985). The388highest concentrations of dino£agellate cysts389(s 5000 cysts cm33) occur at Potter 7 and Nini-390gret 12.391The ratio between cysts produced by autotro-392phic and heterotrophic dino£agellates, commonly393considered an indication of the dominant trophic394mode and the level of primary productivity (Mu-395die and Rochon, 2001), ranges from 0.5 to 93.0396with a mean of 11 (Table 3). Cysts of heterotro-397phic dino£agellates usually comprise less then39833% of the assemblages (Fig. 2), with the excep-399tion of Waquoit Bay (61%), Quonochontaug 16400(57%) and Green Hill 9 (52%). Both stations in401Trustom Pond (60 and 61) are characterized by402the highest proportion of Spiniferites spp.403(s 97%), cysts produced by autotrophic dino£a-404gellates (Figs. 2 and 7).405The dino£agellate cyst assemblages from the406lagoons are generally diverse. A total of 40 taxa407were found (Table 3). Species richness of samples408ranges from 4 to 26, with an average of 15 (Table4093). There is a signi¢cant (P6 0.001) correlation410(R=0.82) between species richness and mean411summer salinity (Fig. 3). Dino£agellate cyst as-412semblages with the lowest cyst diversity (4^8413taxa) are found in low salinity (4.0^7.2) lagoons,414e.g. Trustom and Maschaug.

4154.1. Distribution of dino£agellate cyst taxa

416The distribution patterns of the relative abun-

0 5 10 15 20 25 300

5

10

15

20

25

30

11 Fig. 2. Relationship between species richness of dino£agellate2 cyst and mean summer salinity (S) at lagoon sample stations.

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417 dances of selected dino£agellate cyst taxa (those418 that comprise v 5% of at least one cyst assem-419 blage) are shown in Figs. 4^9. The following420 classes have been applied: present (s 0^1%);421 rare (1^5); common (5^30%); abundant (30^50);422 dominant (s 50%).

4234.1.1. Alexandrium tamarense (Fig. 4; Plate I, 1)424Remarks : the elongate to cylindrical cysts (V30425Wm) contain an orange accumulation body. A mu-426cilaginous substance with incorporated detrital427particles often covers the smooth cell wall.428Occurrence : cysts of A. tamarense were observed

11 Fig. 3. The relative abundance (%) of cysts of heterotrophic and autotrophic dino£agellates in assemblages from southern New2 England lagoons.

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429 at eight stations. The abundance of Alexandrium430 tamarense varies from 4.4% in Green Hill 10 to431 V0.5% in Waquoit Bay, Quonochontaug 18 and432 Potter 5, with values of V1% in Ninigret 12,433 Quonochontaug 16 and 16A and Winnapaug434 19A.

4354.1.2. Lingulodinium machaerophorum (Fig. 5;436Plate I, 4)437Remarks : folding of the cysts prevented deter-438mination of the exact number of precingular439plates involved in archeopyle formation. Cysts440bear characteristic processes, striated at their441bases with grana on the distal ends. Most showed

Fig. 4. Abundance (%) of cysts of Alexandrium tamarense and Spiniferites elongatus at each sample station.1

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442 fully developed processes reaching V1/4 of the443 cyst diameter.444 Occurrence : this species reaches a maximum445 abundance of 17.5% in Potter 8 and 11.2% in446 Potter 6. Its occurrence is rare in Potter 5, Green447 Hill 10 and Ninigret 12 and it is absent from

448Point Judith, Quonochontaug, Trustom, Ma-449schaug and Card’s.

4504.1.3. Nematosphaeropsis spp. (Fig. 5; Plate I,4512,3)452Remarks : most of the observed cysts have an

0

20

40 %

Fig. 5. Abundance (%) of Lingulodinium machaerophorum and Nematosphaeropsis spp. at each sample station.1

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453 ovoid to elongated body with slight apical protub-454 erance. The cyst wall is relatively thick and can be455 smooth to microgranulate. Most of the observed456 cysts have central bodies within the range of 31^457 52 Wm and a maximum process length from 9^14458 Wm (13 specimens measured). Despite the fact that

459the paratabulation is not expressed, processes ap-460pear to be exclusively gonal in distribution. Rod-461shaped processes are solid at the base and have462distal trifurcations. Trabecules are solid and463threadlike.464Occurrence : Nematosphaeropsis spp. constitute

0

20

40 %

11 Fig. 6. Abundance (%) of Operculodinium centrocarpum sensu Wall and Dale (1966), Operculodinium israelianum and cysts of Pen-2 tapharsodinium dalei at each sample station.

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465 0.4^4.2% of the assemblages at 3/4 of the stations466 and it is abundant (44.5%) at Potter station 7.467 Thusfar Nematosphaeropsis species had not been468 reported in such abundances in shallow estuarine469 and coastal waters (Wall et al., 1977; Rochon et470 al., 1999).

4714.1.4. Operculodinium centrocarpum sensu Wall472and Dale 1966 (Fig. 6; Plate I, 7)473Remarks : most processes of Operculodinium474centrocarpum are well developed, being V9 Wm475long. Specimens similar to O. centrocarpum but476having very short processes (up to 2 Wm) were477identi¢ed as O. centrocarpum var. truncatum.

020406080

100 %

Fig. 7. Abundance (%) of Spiniferites spp. at each sample station.1

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478 Occurrence : Operculodinium centrocarpum appar-479 ently has a wide distribution. It is a common480 component of most of the dino£agellate cyst as-481 semblages with an average abundance of 7.0%.482 Operculodinium centrocarpum is absent only

483from Potter 6, whereas it has the maximum abun-484dance in the same lagoon, at station 5 (35%).

4854.1.5. Operculodinium israelianum (Fig. 6; Plate486I, 5,6)487Remarks : Cysts are quite fragile and whole

0

10

20

30 %

11 Fig. 8. Abundance (%) of Brigantedinium spp., Dubridinium spp. and Protoperidinium spp. indet. at each sample station.2

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488 specimens with clearly visible archeopyles are489 rare.490 Occurrence : Operculodinium israelianum is found491 in 2/3 of all samples, but it is rare in most of the492 assemblages. However, it comprises up to 23.6%493 and 16.5% of cyst assemblages in Maschaug and

494Jehu Ponds, respectively, and occurs at its highest495abundance (38.3%) at Potter 8.

4964.1.6. Pentapharsodinium dalei (Fig. 6; Plate I,4978)498Remarks : these small spherical colorless cysts

11 Fig. 9. Abundance (%) of cysts of Polykrikos schwartzii and P. kofoidii, Islandinium brevispinosum and Islandinium minutum at2 each sample station.

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499 can be easily overlooked in slides containing large500 quantities of terrigenous organic material and re-501 quire counting at high magni¢cation or interfer-502 ence contrast microscopy.503 Occurrence : cysts of Pentapharsodinium dalei504 comprise 0.4^32.1% of the assemblages, averaging505 8.8%, and reach their maximum of 44.2% at Ni-506 nigret 13. This species is absent at Green Hill 9507 and 10, Winnapaug 19A, Trustom and Card’s508 Ponds.

509 4.1.7. Spiniferites group (Fig. 7; Plate I, 9^12)510 Remarks : Spiniferites species show a great deal511 of variation in the size, process length and devel-512 opment as well as the presence and absence of513 paratabulation. Because of the great morpholog-514 ical variations, the Spiniferites species were515 grouped as Spiniferites spp. Spiniferites elongatus516 (Plate II, 1) was easy to identify and it was not517 grouped in Spiniferites spp.518 Occurrence : Spiniferites spp. is the most abundant519 group and it is the only taxa found at all sites.520 The relative abundance of Spiniferites spp. varies521 from 12.6 to 98.4%, reaching its maximum in the522 Trustom 60 and 61 assemblages. Spiniferites elon-523 gatus occurs only in seven samples, with a max-524 imum abundance of V3.5% in Point Judith 4 and525 Winnapaug 21 (Fig. 4).

526 4.1.8. Brigantedinium group (Fig. 8)527 Remarks : this species group includes Brigante-528 dinium simplex, B. cariacoense and all spherical529 brown cysts having a smooth wall surface. Where530 species identi¢cation was possible, B. simplex was

531more abundant than B. cariacoense in the assem-532blages.533Occurrence : the genus Brigantedinium often dom-534inates assemblages in coastal and estuarine waters535(Wall et al., 1977; de Vernal and Giroux, 1991;536Rochon et al., 1999), but it is never abundant in537our samples. However, it occurs in all samples538except Trustom 61, varying in abundance from5395.1 to 29.2%. It reaches a maximum at Quono-540chontaug 16.

5414.1.9. Dubridinium spp. (Fig. 8; Plate II, 3)542Remarks : this group includes brown subspher-543ical to somewhat lenticular cysts with well-devel-544oped cingular lists. A theropylic archeopyle is545rarely observed. Phragma typically consists of546two layers; a thick smooth endophragm and a547thin granular periphragm. The apical pore com-548plex is clearly seen.549Occurrence : Dubridinium spp. is only common in550Ninigret 12, Point Judith 4, Quonochontaug 16551and Waquoit Bay with a maximum abundance552of 17.2% in Potter 7. Elsewhere it is at best only553a rare component in the assemblages.

5544.1.10. Islandinium brevispinosum (Fig. 9; Plate555II556Remarks : the characteristic small size, brown557color, spherical shape, smooth wall surface and558numerous solid spines prevent confusion with oth-559er species.560Occurrence : Islandinium brevispinosum occurs561only in four samples, with a maximum abundance562of 4.7% in Waquoit Bay.

Plate I. Photomicrographs are bright ¢eld images. Scale bar= 20 Wm

1. Cyst of Alexandrium tamarense, Potter Pond 5, MGU 982, slide 1, K44/3, optical section, mid focus showing protoplasmwithin cysts.2

1

2,3. Nematosphaeropsis spp., Point Judith Pond 1, MGU 1247, slide 1, D41/1, ventral view, upper (2) and mid (3) focus.34. Lingulodinium machaerophorum, Potter Pond 5, MGU 982, slide 1, P44/3, orientation unknown, mid focus showing

protoplasm within cysts.54

5,6. Operculodinium israelianum, Potter Pond 8, MGU 985, slide 1, R31/3, lateral view, upper (5) and low (6) foci.67. Operculodinium centrocarpum sensu Wall and Dale 1966, Potter Pond 7, UQAM 1300-5, slide 1, T38/3, orientation

unknown, low focus.87

8. Cyst of Protoperidinium dale, Potter Pond 7, MGU 1300-5, slide 1, V43/2, orientation unknown, upper focus.99^12. Cysts of Spiniferites group: (9) Quonochontaug Pond 16A, MGG 1235, slide 1, lateral view, upper focus; (10) Trustom

Pond 60, MGU 1300-6, slide 2, lateral view, upper focus; (11) Ninigret Pond 14, MGU 1246, slide 3, lateral view, upperfocus; (12) Trustom Pond 61, MGU 1091, slide 1, optical section.12

1110

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563 4.1.11. Islandinium minutum (Fig. 9; Plate II, 5)564 Remarks : these spherical, brownish cysts are565 characterized by a granulate wall surface, and nu-566 merous randomly dispersed processes terminating567 distally in ¢ne acuminate tips. No cysts with568 clearly visible archeopyles were found.569 Occurrence : this species is rare or absent in 3/4 of570 all samples. It is, however, a common component571 of the assemblages from Quonochontaug 16 and572 16A, Point Judith Pond, and Waquoit Bay, and573 reaches a maximum of 7.5% at Winnapaug 19A.

574 4.1.12. Polykrikos schwartzii (Fig. 9; Plate II, 6)575 and Polykrikos kofoidii576 Remarks : cysts of Polykrikos schwartzii and P.577 kofoidii are characterized by a reticulate surface578 structure. Cysts vary widely in shape, from elon-579 gated to ovoid, and in length from 60 to 120 Wm.580 Occurrence : cysts of Polykrikos schwartzii and P.581 kofoidii were found in 17 of 24 samples with an582 abundance ranging from 0.4% to a maximum of583 7.3% in Ninigret 14 (7.3%).

584 4.1.13. Protoperidinium type (Fig. 8)585 Remarks : this group includes all dark brown586 spherical to ovoid cysts that have neither process-587 es nor archeopyle features visible. Cysts have a588 granular to micro granular wall surface and range589 in size from 30 to 60 Wm.590 Occurrence : cysts occur at all stations except591 Trustom 61. The average abundance of Protoper-592 idinium type is V7%, with a maximum of 33.6%593 in Green Hill 9.

5944.1.14. Rare cysts595Rare cysts Tectatodinium pellitum, Gymnodi-596nium spp., Islandinium? cezare, Lejeunacysta sab-597rina, Quinquecuspis concreta, Selenopemphix quan-598ta and Stelladinium stellatum were found in less599than 1/2 of all samples. Cysts of the freshwater600dino£agellate Peridinium limbatum were recorded601at eight stations and in low numbers, with a max-602imum of 3% in Card’s Pond. Occasional cysts of603Ataxiodinium choane, Impagidinium spp., Tubercu-604lodinium vancampoae, Lejeunecysta oliva, Pheopo-605lykrikos hartmannii, Protoperidinium americanum,606P. oblongum, P. minutum, P. nudum, Trinovante-607dinium applanatum, Votadinium calvum and V. spi-608nosum were noted only in the assemblages.

6094.2. Relationship between the assemblages and610environmental parameters

611CCA produced an ordination in which the ¢rst612four axes (Table 5) are statistically signi¢cant613(P=0.03). These probabilities indicate that the614relationship between the species and the environ-615mental variables is signi¢cant. Moreover, the616probability for the ¢rst CCA axis is signi¢cant617at the 0.5% level. The eigenvalues measure the618importance of each of the CCA axes. The ¢rst619eigenvalue is 0.044, the second 0.024, the third6200.017 and the fourth 0.016. A triplot of samples,621species and environmental variables based on the622¢rst two axes explains 28% of the variance in the623species data, 50.8% of the variance in the ¢tted624species data, and the same percentage (50.8%) of

Plate II. Photomicrographs are bright ¢eld images. Scale bar= 20 Wm

1. Spiniferites elongatus, Winnapaug Pond 19, MGU 1300-4, slide 2, R30/0, ventral view, upper focus.12. Tuberculodinium vancampoae, Point Judith Pond 4, MGU 1300-2, slide 2, antapical surface, low focus.23. Dubridinium spp., Potter Pond 7, MGU 1300-5, slide 1, O37/1, apical view, upper focus.34. Islandinium brevispinosum, Winnapaug Pond 19A, MGU 1228, slide 1, P27/0, orientation unknown, upper focus.45. Islandinium minutum, Green Hill Pond 10, MGU 1030, slide 2, L43/3, orientation unknown, upper surface.56. Cyst of Polykrikos schwartzii, Potter Pond 7, MGU 1300-5, slide 1, F52/1, equatorial view, low focus.67. Selenopemphix quanta, Trustom Pond 60, MGU 1090, slide 1, R25/3, apical view, mid focus.78. Quinquecuspis concreta, Potter Pond 7, MGU 1300-5, slide 1, S41/3, ventral surface, upper focus.89. Lejeunacysta oliva, Potter Pond 7, MGU 1300-5, slide 1, T31/3, dorsal surface, upper view.910. Peridinium limbatum, Potter Pond 7, MGU 1300-5, slide 1, B43/0, optical section.1011. Votadinium calvum, Point Judith Pond 4, MGU 1300-2, slide 1, dorsal surface, upper focus.1112. Votadinium spinosum, Point Judith Pond 4, MGU 1300-2, slide 1, dorsal surface, low focus.12

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Table 5Eigenvalues for CCA axes 1^4, P values for the signi¢cance tests of the ¢rst and all four CCA axes, speciesênvironment (spp.ênv.) correlations and cumulative percent speciesênvironment variation

CCA CCA axes1

Axis 1 Axis 2 Axis 3 Axis 4 Total2

Eigenvalues 0.044 0.024 0.017 0.0163P-value 0.005 0.0304Speciesênvironment correlations 0.972 0.936 0.799 0.8615Cumulative % spp. data 18.1 28 34.9 41.56Cumulative % spp.ênv. variation 32.9 50.8 63.5 75.47

-1.0

+1.0-1.0

+1.

0

11 Fig. 10. Ordination diagram generated from CCA, showing results for axes 1 (horizontal) and 2 (vertical). The length of arrows2 (which represent environmental variables) indicates the importance of that variable in explaining the dino£agellate cyst distribu-3 tion. Solid arrows represent forward-selected variables and dashed arrows represent non-signi¢cant environmental variables. The4 direction of the arrows shows approximate correlation to the ordination axes. Abbreviations of the environmental variables: T,5 mean summer temperature; S, mean summer salinity; N, mean summer nitrates; P, mean summer phosphates; Chl a, mean6 summer chlorophyll a ; D, depth.

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625 the variance in the weighted averages and the626 class totals of the species with respect to the en-627 vironmental variables (Table 5). However, only628 two of the 11 environmental variables were signif-629 icantly correlated (P9 0.01) with the CCA axes,630 mean summer temperature and salinity (Fig. 10).631 The mean summer temperature (T) has a strong632 negative correlation (30.735) with axis 1, whereas633 mean summer salinity (S) is positively correlated634 with axis 2 (0.668).635 Table 6 shows each species cumulative ¢t in a636 CCA. The ¢t of Pentapharsodinium dalei in a637 CCA ordination diagram of the ¢rst axes, corre-638 lated with mean summer temperature, is the high-639 est (72%), followed by Spiniferites elongatus (39%)640 and Operculodinium israelianum (29%). The ¢rst641 two species are known to indicate cool marine642 waters (Dale, 1996; Rochon et al., 1999), whereas643 Operculodinium israelianum is most abundant in644 warm lagoonal waters (Wall et al., 1977; Morza-645 dec-Kerfourn, 1989). The species with the highest646 ¢t for the second axis, representing summer salin-647 ity, are Spiniferites spp., Dubridinium spp., Islan-

648dinium brevispinosum and Peridinium limbatum.649The percentage ¢t by all environmental variables650together, given in the last column of Table 6,651shows that given environmental factors can ex-652plain s 50% of the distribution of Spiniferites653spp., P. dalei, I. brevispinosum, Dubridinium spp.654and O. israelianum. Environmental range (mean655summer temperature, salinity, nitrates and phos-656phates) for individual cyst taxa is summarized in657Table 7.658Nematosphaeropsis spp. has the lowest cumula-659tive ¢t (14%) by all environmental variables to-660gether (Table 6). The unusually high proportion661(44.5%) Nematosphaeropsis spp. in the assemblag-662es is found in Potter 7. We assume that this ab-663normal abundance of Nematosphaeropsis spp. in664Potter 7 indicates bloom event and is caused by665abrupt environmental change not detected in our666environmental measurements. Indeed, when this667site is removed from the CCA analyses the ¢t of668Nematosphaeropsis spp. in a CCA ordination in-669creases up to 37%.

Table 6Cumulative ¢t per dino£agellate cyst species (selected taxa) as fraction of variance of species

Cyst taxa CCA axes1

Axis 1 Axis 2 Axis 3 Axis 4 % expl2

Alexandrium tamarense 0.00 0.01 0.31 0.32 483Brigantedinium spp. 0.01 0.02 0.04 0.05 414Dubridinium spp. 0.18 0.52 0.52 0.54 655Islandinium brevispinosum 0.20 0.51 0.60 0.64 736Islandinium ? cezare 0.19 0.20 0.21 0.22 487Islandinium minutum 0.00 0.23 0.23 0.24 338Gymnodinium spp. 0.16 0.17 0.31 0.32 549Lejeunecysta spp. 0.02 0.06 0.26 0.39 5310Lingulodinium machaerophorum 0.18 0.19 0.23 0.29 4611Nematosphaeropsis spp. 0.02 0.02 0.02 0.04 1412Operculodinium centrocarpum 0.20 0.30 0.31 0.32 4713Operculodinium israelianum 0.29 0.30 0.42 0.53 6114Pentapharsodinium dale 0.72 0.72 0.73 0.86 9015Polykrikos kofoidii and P. schwartzii 0.02 0.04 0.05 0.12 2716Protoperidinium spp. Indet 0.03 0.04 0.09 0.10 3617Peridinium limbatum 0.25 0.37 0.37 0.39 5318Quinquecuspis concreta 0.12 0.27 0.30 0.38 5319Selenopemphix quanta 0.04 0.13 0.16 0.37 4720Spiniferites elongatus 0.39 0.50 0.65 0.65 7621Spiniferites spp. 0.12 0.60 0.60 0.79 9022Tectatodinium pellitum 0.07 0.33 0.36 0.36 6023Cyst type E 0.03 0.13 0.31 0.37 4524

% expl, the percentage ¢t by all environmental variables together.25

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670 5. Discussion and conclusions

671 There are few published works focussed on di-672 no£agellate cysts in estuarine environments. We673 can ¢nd no studies of variability in cyst distribu-674 tion on similar scales on the temperate coasts of675 the western Atlantic with which to compare our676 results. Our study shows that dino£agellates are677 generally abundant (an average of 1660 cysts678 cm33) and diverse (an average of 15 dino£agellate679 cyst taxa) in back-barrier lagoons. Previous stud-680 ies of spatial distribution of dino£agellate cysts in681 the St. Lawrence Estuary (de Vernal and Giroux,682 1991), Ba⁄n Bay (Mudie and Short, 1985), Aus-683 tralian (McMinn, 1989, 1990, 1991), Japanese684 (Matsuoka, 1992) and Spanish (Blanco, 1995) es-685 tuaries as well as the global surveys by Wall et al.686 (1977) and Harland (1983) show cyst concentra-687 tions of the same order of magnitude and species688 richness comparable to our study.689 We have found that relatively low cyst concen-690 trations (6 430 cysts cm33) characterize lagoons691 with salinities below 10. Such low concentrations692 can be explained by low dino£agellate production693 in these environments, as few species tolerate sa-694 linity below 20 (Dale, 1996). However, sediment695 samples from low salinity sites often contain696 abundant organic detritus that would dilute dino-697 £agellate cyst concentrations.698 Some investigators (Wall et al., 1977; Dale,699 1996; Ellegaard, 2000; Mudie et al., 2001) also700 have noted that oligohaline environments are701 characterized by low species diversity (9 8 taxa)702 and cyst assemblages mainly dominated by the703 Spiniferites group, similar to our results. Spinifer-704 ites spp., which are dominant in most of our sam-705 ples, occur throughout a wide range of salinity706 reaching maxima at low salinity sites. In addition,707 dino£agellate cyst assemblages at low salinity sta-708 tions contain 9 8 taxa, approximately half that709 found in the lagoons with s 10 waters. The latter710 are characterized by generally abundant and di-711 verse (v 10 taxa) cyst assemblages.712 The novelty of our results is in the quantitative713 analysis of the environmental factors controlling714 the composition and distribution of dino£agellate715 cyst assemblages in the lagoons. With the help of716 CCA, we identify temperature and salinity as the

717main environmental factors a¡ecting the distribu-718tion of dino£agellate cysts in the New England719lagoons. The CCA reveals that the variation in720temperature has the largest impact on the compo-721sition of the dino£agellate cyst assemblages, but722the concentration of nutrients shows no clear cor-723relation with dino£agellate cyst assemblages.724Nitrogen is generally considered to be a limiting725nutrient for phytoplankton production in estua-726rine waters (Boynton et al., 1982) and an impor-727tant factor for dino£agellate development (Tay-728lor, 1987), yet nitrates are not found as a729signi¢cant factor in the composition of dino£agel-730late assemblages in our lagoons. This may be be-731cause nitrate measurements do not re£ect the total732nitrogen availability. Marine phytoplankton pref-733erentially takes up ammonium over nitrate (Valie-734la, 1995). Thus, various nitrogen compounds need735to be measured for future evaluation of the rela-736tion between dino£agellate cysts and environmen-737tal factors in estuarine systems. In £uvially dom-738inated estuaries covariance between nutrients and739salinity is always a problem. In our lagoons these740two parameters are covariant, but not signi¢-741cantly. The major input of nitrogen to the lagoons742is domestic sewage discharged to groundwater,743the latter being the main source of freshwater to744the lagoons. Indeed, the CCA points the mean745summer salinity (S) and the mean summer nitrates746(N) in the opposite directions (Fig. 10) indicating747that they are negatively but not signi¢cantly cor-748related. An extension of this data set would pro-749vide an opportunity to examine separate impacts750of these parameters on dino£agellate cyst distri-751bution without the complication of covariance.752The CCA re£ects the environmental ‘preferen-753ces’ of dino£agellate cyst taxa deduced from stud-754ies of dino£agellate cyst distributions in marine755and oceanic environments (Wall et al., 1977;756Morzadec-Kerfourn, 1989; Edwards and Andrle,7571992; Dale, 1996; Rochon et al., 1999). In partic-758ular, Operculodinium israelianum, Islandinium bre-759vispinosum, and Dubridinium spp. have a positive760relationship to temperature, whereas Pentapharso-761dinium dalei, Spiniferites elongatus, and Operculo-762dinium centrocarpum have a negative relationship.763The CCA also shows a negative relation between764salinity and Peridinium limbatum and Spiniferites

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Table 7Tolerance limits (mean summer temperature, salinity, nitrates, phosphates) for individual cyst taxa in New England lagoons and worldwide

Temperature (‡C) Salinity Nitrates Phosphates1

Lagoons Worldwide** Lagoons Worldwide** Lagoons Worldwide**Lagoons Worldwide**2

Cyst taxa min max min max min max min max min max min max min max min max3

Alexandrium tamarense 19.6 24.6 30.5 27.0 18.9 29.0 20.5 35.5 0.4 3.8 0.1 7.50 0.6 0.9 0.2 0.84Brigantedinium spp. 19.1 24.6 32.0 29.5 3.6 29.0 17.0 37.0 0.2 6.2 0.1 23.50 0.2 1.1 0.1 1.85Dubridinium spp. 19.1 24.6 N/A N/A 18.9 29.0 N/A N/A 0.3 3.8 N/A N/A 0.4 1.0 N/A N/A6Islandinium brevispinosum** 21.6 24.6 23.0 25.0 27.0 28.8 27.0 31.0 0.7 1.7 N/A 2.00 0.7 0.8 N/A 1.77Islandinium? cezare 19.6 22.0 32.0 19.0 23.4 28.7 21.5 35.5 0.3 0.7 0.1 7.00 0.5 0.9 0.1 1.18Islandinium minutum 19.1 24.6 32.0 27.5 4.0 29.0 21.5 35.5 0.3 3.8 0.1 21.00 0.2 1.0 0.1 1.59Gymnodinium spp. 19.1 23.7 N/A N/A 21.1 28.8 N/A N/A 0.3 1.8 N/A N/A 0.4 0.8 N/A N/A10Lejeunecysta spp. 19.1 24.6 N/A N/A 18.9 29.0 N/A N/A 0.3 3.8 N/A N/A 0.4 1.0 N/A N/A11Lingulodinium machaerophorum 19.7 24.6 31.5 29.0 18.9 28.8 17.0 37.0 0.4 3.8 0.2 8.0 0.4 1.0 0.2 0.712Nematosphaeropsis spp. 19.1 23.7 32.0 29.5 7.2 29.0 16.5 37.0 0.2 5.1 0.1 23.0 0.2 1.0 0.1 1.713Operculodinium centrocarpum 19.1 24.6 32.0 29.5 3.6 29.0 16.0 37.0 0.2 6.2 0.1 23.0 0.2 1.1 0.1 1.614Operculodinium israelianum 19.1 23.7 1.5 29.0 7.2 29.0 26.0 37.0 0.2 5.1 0.1 20.0 0.2 1.0 0.1 1.715Pentapharsodinium dalei 19.1 24.6 32.0 29.5 7.2 29.0 21.5 36.7 0.2 5.1 0.1 23.0 0.2 1.0 0.1 1.416Polykrikos kofoidii and P. schwartzii 19.1 24.6 31.0 27.5 7.2 29.0 28.5 37.0 0.2 5.1 0.5 7.5 0.2 1.0 0.1 0.717Protoperidinium spp. indet. 19.1 24.6 N/A N/A 3.6 29.0 N/A N/A 0.2 6.2 N/A N/A 0.2 1.1 N/A N/A18Peridinium limbatum 19.6 24.4 N/A N/A 3.6 28.8 N/A N/A 0.2 6.2 N/A N/A 0.2 1.1 N/A N/A19Quinquecuspis concreta 19.1 24.6 N/A N/A 21.1 28.8 N/A N/A 0.3 1.8 N/A N/A 0.4 0.9 N/A N/A20Selenopemphix quanta 19.1 24.6 32.0 29.5 4.0 29.0 17.0 37.0 0.3 5.1 0.1 13.5 0.2 1.0 0.1 1.221Spiniferites elongatus 19.1 22.4 32.0 26.7 20.0 28.5 21.5 36.5 0.3 5.1 0.1 7.5 0.4 1.0 0.1 1.222Spiniferites spp. 19.1 24.6 N/A N/A 3.6 29.0 N/A N/A 0.2 6.2 N/A N/A 0.2 1.0 N/A N/A23Tectatodinium pellitum 19.1 24.6 14.5 29.5 23.4 29.0 33.0 37.0 0.3 2.4 0.2 7.6 0.4 0.8 0.1 0.724

Bold indicates the extension of the tolerance limits.*Worldwide data based on Marret and Zonneveld (in press).**From Pospelova and Head (2002).

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765 spp., as expected from their predominance in766 Trustom, Maschaug and Card’s Ponds, all low767 salinity lagoons. Peridinium limbatum is a fresh-768 water species (Evitt and Wall, 1968) and Spinifer-769 ites spp. is the most abundant taxon in temperate770 low salinity environments (Wall et al., 1977). In771 addition, other dino£agellate cysts encountered in772 lagoons with low salinity are Brigantedinium spp.,773 Protoperidinium spp., and O. israelianum. Dubri-774 dinium spp. and I. brevispinosum were found at775 the sites with the highest salinity. A salinity of776 V27 is the lowest tolerance limit for I. brevispi-777 nosum (Pospelova and Head, 2002).778 More important than statistical con¢rmation of779 species preferences, our results demonstrate that780 variability in temperature and salinity is re£ected781 even at the small spatial scales that characterize782 lagoons. Thus, dino£agellate cyst assemblages can783 be used for the paleoreconstruction of water tem-784 perature and salinity on scales relevant to estua-785 ries, as well as marine systems. However, in con-786 trast to marine environments reconstruction of787 environmental parameters cannot be used directly788 for paleoclimatic interpretations in lagoons. This789 is because both temperature and salinity in la-790 goons are primarily controlled by the £ushing791 rate, which in turn depends on the nature of the792 inlets connecting lagoons to the ocean. Waters in793 lagoons without permanent inlets have longer res-794 idence time resulting in lower salinity and higher795 temperature, exempli¢ed by Trustom, Maschaug796 and Card’s Ponds (Table 4). Lagoons with perma-797 nent, large, stabilized inlets such as Point Judith798 and Quonochontaug Ponds have a dominating799 marine in£uence thus high salinities and the low800 temperatures (Table 4).801 Changes in the inlet characteristics should a¡ect802 the dino£agellate population as well as the phy-803 toplankton population in general. Temporal var-804 iations in the dino£agellate cyst assemblages from805 shallow estuarine systems may primarily re£ect806 changes in local hydrodynamics that cause (pos-807 sibly large) £uctuations in water temperature and808 salinity, rather than climatic changes. To this end,809 it will be useful to investigate past dino£agellate810 cyst records in some lagoons such as Point Judith811 or Potter Pond prior to the construction of per-

812manent inlets to see if such a change is indeed813re£ected in the assemblages.814Our conclusion that dino£agellate cyst distribu-815tions in the lagoons are correlated with water con-816ditions are further supported by the patterns of817variability within the same estuary. In addition to818the di¡erences in hydrological characteristics be-819tween the lagoons there is a substantial spatial820variability in water quality parameters within821each particular system. Water temperatures in822the peripheral parts of the lagoons are generally823higher during the summer and most likely are824lower during the winter. For example, the envi-825ronmental parameters in Potter Pond vary among826stations; notably the mean summer temperature827varies by as much as 3.1‡C, with the coolest828waters near the inlet. This variability of water829quality is commonly observed in estuarine waters,830and deemed responsible for the heterogeneous dis-831tribution of estuarine phytoplankton (Smayda,8321980), and dino£agellates in particular. Our study833shows that even within the same lagoon the dino-834£agellate cyst assemblages can widely vary be-835tween di¡erent stations. In Potter Pond Operculo-836dinium centrocarpum constitutes (35%)837dino£agellate cyst assemblage at station 5, Spini-838ferites spp. (71%) at station 6, Nematosphaeropsis839spp. (45%) at station 7 and Operculodinium israel-840ianum (38%) at station 8. On the other hand, di-841no£agellate cyst assemblages are relatively homo-842genous between the stations in Trustom and Point843Judith Ponds, where the environmental parame-844ters such as temperature and salinity vary little845between the stations. Our observation of hetero-846geneous pattern of dino£agellate cyst distribution847is consistent with the results of a similar study848along the Spanish coast (Blanco, 1995) but di¡ers849from the conclusion drawn by McMinn (1990,8501991) who studied Australian estuaries. Although851McMinn (1991) stated that cyst distribution was852homogeneous within a single system, careful in-853spection of his assemblage data indicates that854some of the lagoons are characterized by a high855degree of heterogeneity. For example, the relative856abundance of O. centrocarpum ranges 0^100%, O.857israelianum 0^20%, Selenopemphix quanta 0^14%858and Lejeunacysta sabrina 0^25% in the assemblag-859es collected from Lake Macquarie, a lagoon in

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860 New South Wales. On the other hand, dino£agel-861 late cyst assemblages in Tuggerah Lakes are more862 similar between the sites. Unfortunately, it is not863 possible to tie the heterogeneous pattern of dino-864 £agellate cyst distribution in Lake Macquarie and865 the homogeneous pattern in Tuggerah Lakes to866 the water quality parameters, as these measure-867 ments are not provided in the paper.868 In marine and oceanic studies the proportion of869 cysts of heterotrophic dino£agellates has been870 suggested as an indicator of nutrient availability871 due to increasing shore proximity or presence of872 upwelling zones (Wall et al., 1977; Bujak, 1984;873 Mudie, 1992; Harland et al., 1998, Dale, 1996;874 Mudie and Rochon, 2001). Mudie and Rochon875 (2001) consider this is an indication of the domi-876 nant trophic mode and the level of primary pro-877 ductivity. The proportion of heterotrophic dino-878 £agellates is correlated with the availability of879 preferred prey such as diatoms and micro£agel-880 lates, in turn in£uenced by environmental factors.881 Generally, the proportion of the cysts of hetero-882 trophic dino£agellates in the assemblages within883 each lagoon tends to increase with the distance884 from the inlet (Fig. 3), except in lagoons without885 permanent inlets. The distance from sample sta-886 tions to the inlets is an important parameter re-887 £ecting the degree of the lagoonal water exchange888 with the ocean, whereas lagoons without perma-889 nent inlets have no such a gradient. We suspect890 that the variance in the proportion of cyst of het-891 erotrophic dino£agellates may be related to the892 di¡erences in the water residence time. However,893 the ecology of heterotrophic dino£agellates in es-894 tuarine systems is complex and needs further stud-895 ies.

896 6. Uncited references

897 Valiela et al., 1992

898 Acknowledgements

899 We are grateful to M.J. Head and A. de Vernal900 for discussions on the taxonomy of dino£agellate901 cysts and technical support. Special thanks are

902due to R. Crawford, I. Valiela, C. Weidman, V.903Lee, the Waquoit Bay National Estuarine Re-904search Reserve and the Pondwatchers of Rhode905Island for their dedication to estuarine research906and for sharing with us their data on water qual-907ity conditions. Fieldwork was partially funded908through a Geological Society of America student909fellowship. We gratefully acknowledge the sup-910port of the Natural Sciences and Engineering Re-911search Council of Canada (NSERC) and the912Fonds pour la Formation de Chercheurs et l’aide913a' la Recherche (FCAR) of Quebec. This is Con-914tribution No. AED-03-027 of the USEPA O⁄ce915of Research and Development, National Health916and Environmental E¡ects Research Laboratory,917Atlantic Ecology Division. The research described918in this paper has not been subject to agency level919review. Mention of trade names or commercial920products does not constitute endorsement or rec-921ommendation for use by USEPA.

922References

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1000 Association of Stratigraphic Palynologists Foundation, Dal-1001 las, TX, pp. 1197^248.1002 Head, M.J., Harland, R., Matthiessen, J., 2001. Cold marine1003 indicators of the late Quaternary: The new dino£agellate1004 cyst genus Islandinium and related morphotypes. J. Quat.1005 Sci. 16, 621^636.1006 Hoare, R., 1996. World Climate, USA Climate Normals. But-1007 tle and Tuttle (http://www.worldclimate.com).

1008Lee, V., 1980. An Elusive Compromise: Rhode Island Coastal1009Ponds and Their People. Coastal Resources Center, Univer-1010sity of Rhode Island Marine Technical Report 73, RI.1011Lee, V., Olsen, S., 1985. Eutrophication and management ini-1012tiatives for the control of nutrient inputs to Rhode Island1013coastal lagoons. Estuaries 8, 191^202.1014Lee, V., Ernst, L., Marino J., 1997. Rhode Island Salt Pond1015Water Quality, Salt Pond Watchers Monitoring Data 1985^10161994, Well and Stream Monitoring Data 1994. Rhode Island1017Sea Grant Publication P1470, RI.1018Lentin, J.K., Williams, G.L., 1993. Fossil Dino£agellates: In-1019dex to Genera and Species, 1993 ed. American Association1020of Stratigraphic Palynologists, Contribution Series 28, Dal-1021las, TX.1022Marret, F., Zonneveld, K., in press. Atlas of the Modern Or-1023ganic-Walled Dino£agellate Cyst Distribution. Rev. Palaeo-1024bot. Palynol.1025Matsuoka, K., 1992. Species diversity of modern dino£agellate1026cysts in surface sediments around the Japanese Islands. In:1027Head, M.J., Wrenn, J.H. (Eds.), Neogene and Quaternary1028Dino£agellate Cysts and Acritarchs. American Association1029of Stratigraphic Palynologists Foundation, Dallas, TX, pp.103033^53.1031McMinn, A., 1989. Late Pleistocene dino£agellate cysts from1032Botany Bay, New South Wales, Australia. Micropaleontol-1033ogy 35, 1^9.1034McMinn, A., 1990. Recent dino£agellate cyst distribution in1035eastern Australia. Rev. Palaeobot. Palynol. 65, 305^310.1036McMinn, A., 1991. Recent dino£agellate cysts from estuaries1037on the central coast of New South Wales, Australia. Micro-1038paleontology 37, 269^287.1039Morzadec-Kerfourn, M.-T., 1989. Autochthonous and al-1040lochthonous dino£agellate cysts in Pleistocine marine sedi-1041ments from the West African margin and their paleoenvi-1042ronmental signi¢cance. Program and Abstracts of the1043Fourth International Conference on Modern and Fossil Di-1044no£agellates, Woods Hole, MA, p. 81.1045Mudie, P.J., 1992. Circum-Arctic Quaternary and Neogene1046marine palyno£oras: Paleoecology and statistical analysis.1047In Head, M.J., Wrenn, J.H. (Eds.), Neogene and Quaternary1048Dino£agellate Cysts and Acritarchs. American Association1049of Stratigraphic Palynologists Foundation, Dallas, TX, pp.1050347^390.1051Mudie, P.J., Rochon, A., 2001. Distribution of dino£agellate1052cysts in the Canadian Arctic marine region. J. Quat. Sci. 16,1053603^620.1054Mudie, P.J., Short, S.K., 1985. Marine palynology of Ba⁄n1055Bay. In: Andrews, J.T. (Ed.), Quaternary Studies of Ba⁄n1056Island, West Greenland and Ba⁄n Bay. Allen and Unwin,1057London, pp. 263^308.1058Mudie, P.J., Aksu, A.J., Yasar, D., 2001. Late Quaternary1059dino£agellate cysts from the Black, Marmara and Aegean1060seas: Variations in assemblages, morphology and paleosalin-1061ity. Mar. Micropaleontol. 43, 155^175.1062Nixon, S.W., 1982. Nutrient dynamics, primary production1063and ¢sheries yields of lagoons. Oceanol. Acta, 357^371.1064Pospelova, V., Head, M.J., 2002. Islandinium brevispinosum sp.

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1065 nov. (Dino£agellata), a new organic-walled dino£agellate1066 cyst from modern estuarine sediments of New England1067 (USA). J. Phycol. 38, 593^601.1068 Rochon, A., de Vernal, A., Turon, J.-L., Matthiessen, J.,1069 Head, M. J., 1999. Distribution of Recent dino£agellate1070 cysts in surface sediments from the North Atlantic Ocean1071 and adjacent seas in relation to sea-surface parameters.1072 American Association of Stratigraphic Palynologists Foun-1073 dation, Contribution Series 35, Dallas, TX.1074 Sheath, R.G., Harlin, M.M., 1988. Physical and chemical char-1075 acteristics of freshwater and marine habitats. In: Sheath,1076 R.G., Harlin, M.M. (Eds.), Freshwater and Marine Plants1077 of Rhode Island. Kendall/Hunt, RI, pp. 7^19.1078 Smayda, T.J., 1980. Phytoplankton species succession. In:1079 Morris, I. (Ed.), The Physiological Ecology of Phytoplank-1080 ton. Blackwell, Oxford, pp. 483^570.1081 Stockmarr, J., 1977. Tablets with spores used in absolute pol-1082 len analysis. Pollen Spores 13, 615^621.1083 Taylor, F.J.R. (Ed.), 1987. The Biology of Dino£agellates. Bo-1084 tanical Monographs 21, Blackwell Scienti¢c Publications,1085 Oxford.1086 ter Braak, C.J.F., 1995. Ordination. In: Jongman, R.H.G., ter1087 Braak, C.J.F., van Tongeren O.F.R. (Eds.), Data Analysis

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Environmental factors influencing the spatial distribution of dinoflagellate cyst assemblages in shallow lagoons of southe...IntroductionStudy areaPhysical characteristicsEnvironmental characteristics

Materials and methodsStation locations and sediment collectionSample preparationDinoflagellate cyst analysisHydrological dataStatistical methods

ResultsDistribution of dinoflagellate cyst taxaAlexandrium tamarense (Fig. 4; Plate IPlate IPhotomicrographs are bright field images. Scale bar=20 mum1.Cyst of Alexandri...Lingulodinium machaerophorum (Fig. 5; Plate I, 4)Nematosphaeropsis spp. (Fig. 5; Plate I, 2,3)Operculodinium centrocarpum sensu Wall and Dale 1966 (Fig. 6; Plate I, 7)Operculodinium israelianum (Fig. 6; Plate I, 5,6)Pentapharsodinium dalei (Fig. 6; Plate I, 8)Spiniferites group (Fig. 7; Plate I, 9-12)Brigantedinium group (Fig. 8)Dubridinium spp. (Fig. 8; Plate II, 3)Islandinium brevispinosum (Fig. 9; Plate IIIslandinium minutum (Fig. 9; Plate II, 5)Polykrikos schwartzii (Fig. 9; Plate II, 6) and Polykrikos kofoidiiProtoperidinium type (Fig. 8)Rare cysts

Relationship between the assemblages and environmental parameters

Discussion and conclusionsUncited referencesReferences

Documents

ARTICLE IN PRESS · 2003. 10. 6. · ARTICLE IN PRESS UNCORRECTED PROOF 140 and August are the warmest months of the year, 141 while January and February are the coldest with 142