Foraminiferal assemblages in Biscayne Bay, Florida, USA: Responses to urban and agricultural influence in a subtropical estuary

Marine Pollution Bulletin 59 (2009) 221–233

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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

Foraminiferal assemblages in Biscayne Bay, Florida, USA: Responses to urban and agricultural influence in a subtropical estuary E.A. Carnahan a, A.M. Hoare a, P. Hallock a,*, B.H. Lidz b, C.D. Reich b a b

College of Marine Science, University of South Florida, 140 7th Avenue South, St. Petersburg, FL 33701, USA US Geological Survey, 600 4th St. South, St. Petersburg, FL 33701, USA

a r t i c l e Keywords: Ammonia Archaias Heavy metals Eutrophication Hypoxia FORAM Index

i n f o

a b s t r a c t This study assessed foraminiferal assemblages in Biscayne Bay, Florida, a heavily utilized estuary, interpreting changes over the past 65 years and providing a baseline for future comparisons. Analyses of foraminiferal data at the genus level revealed three distinct biotopes. The assemblage from the northern bay was characterized by stress-tolerant taxa, especially Ammonia, present in low abundances (2.0  103 foraminifers/gram) though relatively high diversity (19 genera/sample). The southwestern margin of the bay was dominated by Ammonia and Quinqueloculina, an assemblage characterized by the lowest diversities (12 genera/sample) and highest abundances (1.1  104 foraminifers/gram), influenced by both reduced salinity and elevated organic-carbon concentrations. A diverse assemblage of smaller miliolids and rotaliids (26 genera/sample) characterized the open-bay assemblage, which also had a significant component (10%) of taxa that host algal endosymbionts. In the past 65 years, populations of symbiont-bearing taxa, which are indicators of normal-marine conditions, have decreased while stress-tolerant taxa, especially Ammonia spp., have increased in predominance. Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction Increasing human populations and their activities are rapidly degrading nearshore ecosystems. Anthropogenic stressors include contamination from urban, industrial and agricultural sources; sedimentation associated with land clearing; and altered hydrology. Effective, low cost bioindicators can be used to evaluate the status of estuarine and other nearshore ecosystems, as well as to determine the need for more expensive chemical or molecular assessments for specific stressors (e.g., Hallock et al., 2004). Studies using benthic foraminifers as proxy indicators of anthropogenic contamination were initiated in the early 1960s, although effects on these protists were recognized even earlier (see reviews by Alve (1995), Schafer (2000) and Yanko et al. (1999)). Benthic foraminifers have exceptional utility as bioindicators of coastal contamination because: (1) they have short life spans and specific niches, and therefore respond quickly to environmental change; (2) they are commonly well preserved in the sedimentary record; (3) they are widely distributed yet generally regarded as relatively immobile; (4) they are diverse; (5) they are small, abundant and easily sampled, and therefore their use can be cost effective; (6) their collection has minimal impact on environmental resources (Yanko et al., 1994), and (7) the most * Corresponding author. Tel.: +1 727 553 1567; fax: +1 727 553 1189. E-mail address: [email protected] (P. Hallock). 0025-326X/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2009.08.008

stress-tolerant representatives are often among the last eukaryotes to disappear completely from heavily contaminated sites (Schafer, 2000). Studies that have utilized foraminiferal assemblages have assessed the consequences of organic-waste discharges from sewage outfalls and paper and pulp mills, as well as oil, thermal, and various types of chemical contamination including the effects of heavy-metals on foraminifers (e.g., Alve, 1995; Samir and El-Din, 2001; Schafer, 2000; Seiglie, 1971; Yanko et al., 1999). In reef environments, some enrichment of nutrients and therefore organic matter tends to increase abundances of small, heterotrophic taxa at the expense of the mixotrophic larger foraminifers that host algal endosymbionts (Cockey et al., 1996; Hallock et al., 2003). Alve (1995) published a very useful conceptual model predicting such increase in abundance of some species at intermediate distance from a point source, while reduced abundance and species richness are typical responses to acute contamination at or near a source. Multivariate statistical analyses are the most common strategies in environmental studies that utilize foraminiferal assemblages. In addition, resource management has called for single-metric indicators of the condition of the resource of interest (e.g., Jackson et al., 2000). Sen Gupta et al. (1996), in recognition of the greater tolerance of Ammonia spp. to hypoxia as compared with Elphidium spp., used an Ammonia-Elphidium Index (AEI) as an indicator of oxygen depletion in cores from the Mississippi delta region. Hallock et al. (2003) developed the Foraminifera in Reef

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Assessment and Monitoring (FORAM) Index (FI) to provide a simple, non-invasive measure to determine whether water quality in the environment is sufficient to support coral-reef growth or recovery. The FI is based on foraminiferal-assemblage data from surficial sediments and observations that symbiont-bearing foraminifers and zooxanthellate, reef-building corals require similar high water quality. While neither the AEI nor the FI was specifically developed for use in estuaries, a logical question is, ‘‘Can either index be useful in assessments of subtropical/tropical estuaries?”

1.1. Research objectives The goals of the research reported in this paper were fourfold: 1. to describe total foraminiferal assemblages and their distributions in sediments from Biscayne Bay; 2. to determine if a modified Ammonia-Elphidium Index, which was developed to indicate hypoxia (Sen Gupta et al., 1996), or the FORAM Index, designed to indicate nutrification in coral-reef environments (Hallock et al., 2003), can be useful assessment tools in subtropical estuaries; 3. to compare foraminiferal distributions with available environmental data, and 4. to compare foraminiferal assemblages with assemblages reported from samples from Biscayne Bay collected as much as 65 years earlier.

2. Materials and methods 2.1. Study location Our research focused on Biscayne Bay (Fig. 1), a shallow, subtropical marine estuary off southeast Florida, USA. The bay is bordered on the west by Miami-Dade County, including urban Miami to the northwest, and on the east by two barrier islands, five major carbonate keys, and a series of lesser keys (VanArman, 1984). As a consequence of its proximity to urban Miami, the bay is a site of much recreational and commercial activity, including several marinas, a major cruise-ship port, and a US Coast Guard port. Southward along the western margin of the bay, urbanization decreases where agricultural fields and wetlands remain prevalent. The Black Point Landfill is located roughly midway down the western shore and the Turkey Point Power Plant is near the south end of the western shore of the bay (Fig. 1). Historically, Biscayne Bay was influenced by widespread and continuous submarine groundwater discharge and overland sheetflow (Langevin, 2003). However, during the past century, the natural flow of freshwater into the bay has been radically altered by the urbanization of southeast Florida and human manipulation of drainage from Lake Okeechobee. In the late 1940s, a massive flood-control project was initiated throughout central and south Florida (DeGrove, 1984). By draining more than 200,000 hectares south of Lake Okeechobee and diverting freshwater flow for urban development and for agricultural, industrial, and municipal water supplies, the resultant levees and canals irreversibly damaged wetlands and associated ecosystems (Douglas, 1978). Today, freshwater enters Biscayne Bay from the Miami, Little, and Oleta Rivers in the northern bay, as well as through the Biscayne Aquifer and many man-made canals (Fig. 1; VanArman, 1984). The altered hydrology has substantially affected salinity and nutrient flux into Biscayne Bay, while urban and agricultural development has influenced air, land, and water quality.

Numerous studies have examined some aspect of foraminiferal assemblages in Biscayne Bay and vicinity over the past 65 years (Almasi, 1978; Andersen, 1975; Bush, 1949, 1958; Cole, 1974; Goldstein 1976; Ishman et al., 1997; Stubbs, 1940; Tisserand Delclos, 1979). As a consequence, the taxa common in the bay are well known. The most extensive sample set was described and reported by Bush (1958). It provides an excellent dataset for comparisons with our data to assess how foraminiferal assemblages have changed in Biscayne Bay over the past 50–60 years. 2.2. Sample collection Sediment samples were collected from Biscayne Bay by US Geological Survey (USGS) personnel during December 2000 by free diving and in July 2001 and April 2002 using a Petite Ponar Grab. Samples were frozen until processed. Coordinates for the full dataset can be found in Carnahan (2005). Samples were thawed overnight prior to processing. Each sample was mixed thoroughly and a subsample of approximately 10 g was processed for geochemical analysis of the bulk sediment (Carnahan et al., 2008). A second subsample was wet sieved using deionized water over a 63-lm mesh nylon sieve. Samples, separated into mud fraction (<63 lm) and sand fraction (>63 lm), were dried in an oven (<50 °C). The mud fraction was weighed using an electronic balance and retained for geochemical analysis (Carnahan, 2005; Carnahan et al., 2008). The sand fraction was weighed, split, and half was dry sieved according to methods described by Folk (1980) to determine grain-size distribution. Weighed splits of the other sand-size portion were examined microscopically and picked to yield 150–200 foraminiferal shells (total assemblage), as described by Hallock et al. (2003). The total assemblages integrate information about the general conditions over a longer time period (Alve and Nagy, 1986), whereas the composition of living assemblages solely reflects environmental conditions at that microhabitat at the time of sample collection (Buzas et al., 2002). 2.3. Data analyses The raw weights for each grain-size class were converted to weight percents for each sample. Median grain size for each sample was also calculated and reported in phi units. Data are summarized as medians and ranges because most of the parameters are not normally distributed. Using the statistical software package, PRIMER-e v.5 (Plymouth Routines in Multivariate Ecological Research) (Clarke and Warwick, 2001), similarity matrices were constructed for sites (Q-mode) and foraminiferal genera (R-mode) using log (1 + X) transformed relative abundance data with Euclidean distance (0-infinity) chosen as the similarity measure. Cluster analyses and non-metric multidimensional scaling (MDS) plots were derived from the similarity matrices. Similarity measures based on Euclidean distance are sensitive to differences in sample magnitude (Parker and Arnold, 1999), though transforming the data reduces that sensitivity. MDS constructs a configuration of samples or variables, in this case two-dimensional, which attempts to satisfy all conditions imposed by the rank-similarity matrix. The stress coefficient, ranging from 0 to 1, measures the success of the MDS plot. A stress coefficient < 0.05 is excellent, <0.1 is good, and <0.2 still gives a potentially useful two-dimensional picture (Clarke and Warwick, 2001). The PRIMER-e v.5 SIMPER routine (similarity percentages) examines the contributions of individual genera to the separation of the sample groups determined by cluster analysis (Clarke and Warwick, 2001). The SIMPER analysis provides several statistical parameters (average abundance, average similarity, a ratio of similarity to standard deviation, percent contribution, and cumulative

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Fig. 1. Study area, Biscayne Bay, off the southeast coast of Florida, USA.

percent contribution) for each genus contributing to > 90% similarity within each group of samples. The Ammonia-Elphidium Index (AEI) described by Sen Gupta et al. (1996) was calculated as

AEI ¼ ½Na =ðN a þ Ne Þ  100; where Na and Ne were the numbers of Ammonia and Elphidium, respectively. When neither Ammonia nor Elphidium was present,

we used a zero as the best-numeric substitute for the undefined values. While Sen Gupta et al. (1996) used specific data, we calculated the AEI with generic-level data, including Cribroelphidium with Elphidium, due to the uncertainty of the taxonomy of this group. The FORAM Index (FI) enumerates foraminiferal taxa into functional groups as defined by Hallock et al. (2003) and was calculated as follows:

FI ¼ ð10  P s Þ þ ðPo Þ þ ð2  Ph Þ

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where Ps = Ns/T; Po = No/T; Ph = Nh/T; and T = total number of specimens counted; Ns = number of specimens of symbiont-bearing taxa; No = number of specimens of opportunistic taxa; Nh = number of specimens of small, heterotrophic taxa. We subsequently refer to taxa considered ‘‘opportunistic” by Hallock et al. (2003) as being ‘‘stress tolerant,” a term more consistent with that of Yanko et al. (1999), and those referred to previously as ‘‘small, heterotrophic” as ‘‘other smaller” foraminifers, since the stress-tolerant taxa are also small and heterotrophic. Pearson’s correlation matrices were constructed using STATISTICA v.5.5 (2000) to elucidate relationships among and between metals (log (1 + X) transformed), abundances of foraminiferal taxa (square-root transformed), and indices of diversity. Analyses were based upon the assumption that all samples were independent. These analyses produce Pearson’s correlation coefficients (1.0 to 1.0), which are relatively insensitive to differences in numerical size of the entities being clustered (Parker and Arnold, 1999). Environmental data were acquired from Southeast Environmental Research Center (SERC) Water Quality Monitoring Network, which collected data monthly over an 11-year time period (sites 101–125: 1993–2004; sites 126–135: 1996–2004) at sites throughout Biscayne Bay (http://serc.fiu.edu/wqmnetwork/2005) (SERC, 2005). The means and standard errors of selected waterquality parameters at each site for its entire sampling period were computed. Contour plots were made for total organic carbon (TOC), salinity, and chlorophyll a (chl a) using SURFER v.8 (Golden, 2002). These variables were chosen for their potential to influence the foraminiferal community. Total organic carbon indicates food availability for heterotrophic foraminifers (Crevison, 2001). Several taxa, including some agglutinates, Ammonia, and Elphidium, are known to be euryhaline (Sen Gupta, 1999). Laws and Redalje (1979) found chlorophyll a to be the most sensitive indicator of nutrient enrichment in a subtropical estuary. PRIMER’s BIO-ENV procedure examines the extent to which physio-chemical data are related to observed biological assemblages (Clarke and Warwick, 2001). The approach is to analyze

the biotic data first and then test how well the information on environmental variables, in combination, matched the community structure. We modified the procedure, creating a BIO–BIO procedure, to determine which subset of foraminiferal genera best described the total assemblage.

3. Results 3.1. Foraminiferal assemblages and sample distribution Sixty-three genera of foraminifers were identified from 137 sites in Biscayne Bay. Raw counts, indices of diversity (number of genera, Fisher Index, and Shannon Index), FORAM Index, and density (foraminiferal shells per gram) for each sample are reported in Carnahan (2005). Cluster analysis performed on foraminiferalassemblage data grouped sample sites (n = 137) into three major groups (A, B, and C), which exhibited > 53% similarity. Group B consisted of three subgroups that were > 60% similar (Table 1). Sample III-1 was an outlier (O) to group B at 57% similarity. The results for all 137 sample sites are graphically represented in an MDS plot (stress value = 0.16) (Fig. 2). The contributions of individual genera to the characterization of the groups A, B-1, B-2, B-3, and C were elucidated with SIMPER analysis (Table 1). The cluster analysis, MDS plot (Fig. 2), and the SIMPER output (Table 1) consistently showed that groups B-3 and C were most dissimilar (59%). Fig. 3 shows sample locations throughout the bay, characterizing each sample by its cluster group. Group A consisted of 20 samples predominantly from the southwestern margin of Biscayne Bay (Fig. 3). This group was characterized by the highest abundances and lowest diversities of any group (Table 2). Seven genera contributed to almost 92% of the within-sample variability (Table 1). Miliolids made up 60% of the assemblage, and the stress-tolerant taxa, Ammonia, Cribroelphidium, and Haynesina, were 32%.

Table 1 Sample groups and subgroups (see Fig. 2), showing average within-group similarity, the genera that together contribute to 90% similarity within each group/subgroup, and the average abundances of those genera within each group.

Average similarity

* **

Group A

Group B-1

Group B-2

Group B-3

Group C

71.4

69.3

67.8

70.9

63.1

Average abundance

Average abundance

Genus

F.I.*

Average abundance

Average abundance

Ammonia Bolivina Brizalina Cribroelphidium Elphidium Haynesina Nonion Discorbis Neoeponides Rosalina Valvulineria Affinetrina Articulina Miliolinella Quinqueloculina Triloculina Androsina Archaias JSBM** Laevipeneroplis Clavulina Siphonaperta Valvulina

ST ST ST ST ST ST ST OSR OSR OSR OSR OSM OSM OSM OSM OSM SB SB SB SB AG AG AG

17.7

4.37

6.21 1.92

6.08 3.78 37.8 20.0

1.27 4.60 1.94 3.15 4.68 1.62 3.55 2.48 5.45 4.76 3.70 4.81 34.0 10.8

1.48 2.18 1.45 2.19 1.19 5.96 2.07 4.96 2.94 4.38 7.43 35.8 7.99 1.86 2.49 2.10 1.70 0.76 1.49 1.30

1.27 1.65 1.77 2.80 4.36 8.86 2.25 20.7 32.9 8.08

Average abundance 20.0 1.12 3.64 12.7 2.21 7.17 11.6 1.52 1.61 3.11

20.6 5.70

2.57 2.50

1.29 1.85

FORAM Index (FI) categories, SB = algal symbiont-bearing, OSM = other smaller miliolid, OSR = other smaller rotaliid, ST = stress-tolerant, AG = agglutinated. JSBM = juvenile symbiont-bearing miliods.

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Fig. 2. Multi-dimensional scaling (MDS) plot of sample sites by groups identified using cluster analysis and characterized in Table 1. Interpretations of trends are overlain on the plot.

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The B group of samples was characterized by higher diversities, dominance by smaller miliolids, and moderate contribution by stress-tolerant taxa (20%). The 27 samples that made up subgroup B-1 came from the north-central part of the bay (Fig. 3). Fifteen genera made up 92% of this relatively diverse assemblage; five smaller miliolid genera made up nearly half. Six stress-tolerant genera were another quarter of the assemblage. Four other small rotaliid genera contributed 18% to the group. Median abundance of foraminiferal shells (984 forams/gm) was the lowest in this subgroup (Table 2). Twenty open-bay samples comprised subgroup B-2 (Fig. 3), with the highest diversities of any group or subgroup (Tables 1 and 2). Again, smaller miliolid genera made up nearly half the assemblage, and other smaller rotaliids composed 20% (Table 1). Stress-tolerant taxa made up only 11%. Four categories of symbiont-bearing taxa accounted for 10% of the assemblage, and two agglutinated genera also were present in this sample subgroup. Subgroup B-3 was the largest subgroup of samples, collected from 44 sites that dominated the southern, open bay (Fig. 3). Smaller miliolids dominated (63%), with smaller rotaliids composing

Fig. 3. Sample sites in Biscayne Bay labeled by sample group as identified in Fig. 2 and characterized in Table 1.

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Table 2 Statistics (median and range) for each sample group (defined in Fig. 1 and Table 1): abundance (forams per gm), measures of diversity (number of genera, Fisher Index, Shannon Index), grain-size data (*5 was substituted for median phi > 4 to calculate overall median), and bioindicator metrics [FORAM Index and modified Ammonia-Elphidium Index (Mod. AEI)]. Group

Forams per gm Median(min.– max.)

A B-1 B-2 B-3 C

10,883 (186– 26,258) 984 (171–4708) 1775 (258– 14,762) 2718 (47– 17,780) 1199 (130–6495)

Number of genera Median(min.– max.)

Fisher Index

Shannon Index

% Mud

*Median U

FORAM Index

Mod. AEI

Median (min.– max.)

Median (min.– max.)

Median (min.– max.)

Median (min.– max.)

Median (min.– max.)

Median (min.– max.)

12 (7–18)

2.7 (1.6–4.9)

0.74 (0.50–0.84)

17 (2–58)

2 (1 to 5)

1.8 (1.4–2.5)

75 (57–91)

23 (13–30) 26 (18–36)

7.4 (3.4–10.8) 8.7 (5.5–10.6)

1.03 (0.74–1.20) 1.06 (0.84–1.20)

9 (0–69) 28 (5–72)

3 (1–5) 2 (1 to 5)

2.0 (1.6–2.9) 2.6 (2.0–5.1)

38 (0–73) 0 (0–50)

18 (12–27)

5.1 (2.8–7.8)

0.93 (0.50–1.09)

11 (1–77)

2 (1–5)

2.6 (2.0–3.8)

0 (0–100)

19 (7–28)

5.5 (1.6–9.7)

0.96 (0.54–1.14)

24 (3–94)

3 (1–5)

1.6 (1.0–1.9)

58 (19–78)

16% of the assemblage and symbiont-bearing taxa 7% (Table 1). Only one stress-tolerant genus, Nonion, was identified at 2.6%. Abundance was the highest and diversity lowest of the ‘‘B” subgroups (Table 2). Group C sites were mostly located in the northern portion of the bay (Fig. 3), closest to urban-Miami influence. One sample, III-72, was collected nearest the Black Point Landfill. Group C was dominated by stress-tolerant taxa (61%) and the ubiquitous miliolids, Quinqueloculina and Triloculina (Table 1). Other stress-tolerant genera included Cribroelphidium, Nonion, Haynesina, Brizalina, Elphidium, and Bolivina. Despite the predominance of finer sediments at Group C sites, abundances of foraminiferal shells were generally low (Table 2).

3.2. Key genera Foraminiferal genera that occurred in at least 5% of the samples (n = 23) separated into three distinct assemblages (Fig. 4; see also Fig. 4 in Carnahan et al., 2008). One assemblage was composed of characteristic stress-tolerant foraminifers: Ammonia, Cribroelphidium, Nonion, Haynesina, Bolivina, and Brizalina. A second assemblage consisted of symbiont-bearing foraminifers, from the order Miliolida (Archaias, Androsina, Laevipeneroplis, and the juvenile symbi-

ont-bearing miliolids), a true agglutinated foraminifer (Valvulina), and an agglutinated miliolid (Siphonaperta). The third assemblage, which multi-dimensional scaling placed between the previous two (Fig. 4), included most of the taxa considered as other smaller foraminifers belonging to the orders Rotaliida and Miliolida, including Discorbis, Quinqueloculina, Triloculina, Rosalina, Affinetrina, Miliolinella, Articulina, Neoeponides, and Valvulineria. Interestingly, Elphidium occurred with this assemblage rather than with the stresstolerant taxa, though in Fig. 4, it occurs on the far left of its assemblage, closest to the other stress-tolerant taxa. One genus, Sorites, was an outlier, exhibiting less than 10% similarity of occurrence with any other foraminiferal genus. Genera from the assemblages of symbiont-bearing and other smaller foraminifers tended to correlate positively (n = 137, p < 0.05) to one another and negatively with stress-tolerant taxa (Carnahan, 2005). Ammonia and Cribroelphidium showed the strongest correlation at 0.77. Ammonia and Miliolinella displayed the strongest, negative correlation (0.70). There were no strong correlations with percent mud in the sediments, though Affinetrina, Siphonaperta, Triloculina, Androsina, Archaias, and Valvulina each showed a negative correlation to median phi (i.e., greater abundance in coarser sediments), while Ammonia, Cribroelphidium, Haynesina, Nonion, Bolivina, and Brizalina correlated positively with median phi, indicating prevalence in finer sediments (Table 3). Miliolinella was the genus whose presence and abundance best reflected the total foraminiferal assemblage (BIO–BIO analysis = 0.57). Although Ammonia had one of the lowest correlations of any single genus (0.15), together Ammonia and Miliolinella best characterized (0.72) the total foraminiferal assemblage in Biscayne Bay (see further details in Carnahan, 2005).

3.3. Ammonia-Elphidium and FORAM indices

Fig. 4. MDS plot by genera that occurred in at least 5% of the samples, circling each group of genera identified using cluster analysis. The stress-tolerant taxa cluster to the left of the figure, the symbiont-bearing taxa (JSBM: juvenile symbiont-bearing miliolids) cluster to the right, with two smaller taxa, Valvulina and Siphonaperta, clustering with them, and Sorites occurring as an outlier. The other smaller taxa cluster between these two extremes, with Elphidium, which is typically considered stress tolerant, on the left side of the ‘‘other smaller” cluster. The two genera that best represent the data set, Miliolinella and Ammonia, are noted by arrows.

Values for the modified AEI in Biscayne Bay exhibited the full range from 0 to 100. The highest values occurred in the north and along the western margin, and the lowest values were found in the open bay (Fig. 5a). Subgroups B-2 and B-3 had median modified AEI = 0, indicating that Ammonia were uncommon at those sites, while group A had the highest median (75), indicating that hypoxia was influencing the assemblage at these sites (Table 2). Samples from the northern and southwestern bay showed the lowest FI values (Fig. 5b). The FI in the open bay ranged from the low-mid range to the highest, with only one sample P 4. FORAM Index values are contoured in Fig. 5b, and median FI values for sample groups are reported in Table 2. Subgroup B-3 had the highest median FI (2.6), while group C had the lowest (1.6).

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Table 3 Correlations of selected heavy metals and median phi versus key foraminiferal taxa and measures of density and diversity (N = 137; bolded correlations are significant at p < 0.05).

Affinetrina Articulina Miliolinella Quinqueloculina Siphonaperta Triloculina Juv symb-mil Androsina Archaias Laevipeneroplis Sorites Ammonia Cribroelphidium Elphidium Haynesina Nonion Discorbis Neoeponides Rosalina Valvulineria Bolivina Brizalina Valvulina Forams/gram # Genera Fisher Index Shannon Index FORAM Index

Cu

Ni

Pb

Zn

Cr

Hg

% Mud

Med U

0.30 0.16 0.43 0.23 0.22 0.04 0.39 0.18 0.27 0.19 0.09 0.39 0.42 0.02 0.33 0.18 0.04 0.22 0.14 0.24 0.43 0.42 0.16 0.15 0.17 0.14 0.04 0.31

0.08 0.20 0.36 0.04 0.28 0.10 0.47 0.28 0.32 0.19 0.18 0.30 0.28 0.10 0.30 0.04 0.04 0.14 0.13 0.13 0.40 0.26 0.23 0.03 0.11 0.17 0.14 0.33

0.30 0.13 0.41 0.20 0.15 0.10 0.35 0.23 0.23 0.15 0.03 0.37 0.36 0.02 0.33 0.25 0.02 0.03 0.14 0.08 0.34 0.35 0.15 0.17 0.09 0.06 0.05 0.30

0.19 0.34 0.51 0.16 0.40 0.18 0.57 0.24 0.43 0.34 0.16 0.49 0.42 0.12 0.32 0.09 0.01 0.36 0.27 0.32 0.38 0.32 0.21 0.09 0.35 0.35 0.26 0.42

0.19 0.25 0.38 0.12 0.21 0.06 0.44 0.25 0.33 0.35 0.15 0.39 0.39 0.12 0.44 0.22 0.04 0.25 0.11 0.22 0.45 0.35 0.23 0.09 0.13 0.15 0.08 0.40

0.36 0.27 0.65 0.24 0.41 0.04 0.56 0.34 0.51 0.37 0.14 0.64 0.66 0.03 0.47 0.23 0.12 0.34 0.27 0.30 0.47 0.41 0.32 0.00 0.25 0.23 0.12 0.56

0.27 0.05 0.14 0.06 0.12 0.19 0.10 0.31 0.22 0.13 0.10 0.08 0.05 0.12 0.19 0.23 0.12 0.07 0.06 0.14 0.01 0.17 0.19 0.01 0.11 0.09 0.04 0.26

0.46 0.01 0.47 0.11 0.31 0.30 0.07 0.44 0.41 0.23 0.06 0.30 0.32 0.19 0.42 0.43 0.02 0.14 0.05 0.06 0.35 0.35 0.52 0.04 0.15 0.12 0.05 0.42

Fig. 5. Biscayne Bay, with sites indicated by sample groups identified in Fig. 2 and Table 1, showing contours of (a) modified Ammonia-Elphidium Index (AEI) values with darker shading indicates predominance by Ammonia and (b) FORAM Index (FI) with darker shading indicating predominance of stress-tolerant taxa.

3.4. Environmental data Correlations between key foraminiferal genera and heavy metals in the bulk sediments were reported previously in Carnahan et al. (2008), with copper being the geochemical parameter that showed the strongest influence on foraminiferal assemblage distributions in Biscayne Bay. Heavy metals in the mud fractions of our samples (Carnahan, 2005; Hoare, 2002), as well as in the bulk sediments as reported by Carnahan et al. (2008), correlated negatively

with symbiont-bearing foraminifers and positively with stress-tolerant genera (Table 3). All heavy metals in the mud fraction correlated negatively to the FORAM Index, with the strongest negative correlation (0.56) with mercury. Chlorophyll a (chl a), total organic carbon (TOC), and salinity averages, calculated from data collected by the Southeast Environmental Research Center (SERC) Water Quality Monitoring Network (http://serc.fiu.edu/wqmnetwork/2005) at sites 101–125 (1993– 2004) and sites 126–135 (1996–2004) were contoured (Fig. 6) for

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Fig. 6. Biscayne Bay showing (a) collection sites for environmental data obtained from the Southeast Environmental Research Center (2005), (b) chlorophyll (chl) a, (c) total organic carbon (TOC), and (d) salinity (our sites are indicated by sample group in b, c and d).

comparison with our data. Chlorophyll a averages were highest in the northern portion of the bay, between Miami and Key Biscayne. The open bay showed the lowest concentration of chl a. Average salinity was lowest along the coast near Black Creek Canal. Nearshore areas to the north and south of the Black Point Landfill exhibited salinities closer to normal-marine conditions. The contours for total organic carbon in the bay provide nearly a perfect inverse image of salinity, showing a maximum off Black Creek Canal and decreasing in the north, south, and offshore directions.

4. Discussion 4.1. Foraminiferal distributions throughout Biscayne Bay Foraminiferal-assemblage data revealed strong environmental gradients in Biscayne Bay. The end members included a near-pristine estuarine assemblage, an open-marine assemblage, an urban/ industrial-impacted assemblage, and a hyposaline/hypoxia-influenced assemblage.

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Sites characterized by the group A assemblage had median foraminiferal abundances more than four times higher than any other group (Table 2), though taxonomic diversities at these sites were relatively low. This group primarily occurred at sites between Black Creek Canal and Turkey Point, where salinity was lowest and TOC was highest (Fig. 6c and d). Thus, variable salinity likely reduced diversity, although abundant food was available to support high densities of species that tolerated salinity stress. Together, Ammonia and Quinqueloculina made up 46% of the assemblage, resulting in a median FI = 1.8 (Table 2), reflecting those stresses. The modified AEI values (Table 2) were the highest for this group (median = 75, minimum = 57), indicating that intermittent hypoxia also influences these sites (Sen Gupta et al., 1996). Group C sites, which occurred mostly in the northern portion of the bay closest to urban-Miami influence, were dominated by Ammonia and other stress-tolerant taxa. The median modified AEI was 58 (Table 2). This dominance by Ammonia and other stress-tolerant taxa resulted in the lowest median FI (1.6) of any group. The C group exhibited some of the lowest shell densities, despite occurrence primarily in fine sands and mud. Although Long et al. (1999) found sediments from this area of the bay to exhibit relatively low toxicity, the stressors apparently are chronic, as indicated by the low densities of foraminifers, dominance by stresstolerant taxa, and the low abundances of ubiquitous miliolids. This enigmatic combination may indicate that in situ production of shells by stress-tolerant taxa is suppressed by unfavorable conditions, although mixing processes (e.g., waves, currents, boat traffic) possibly dilute toxicity. Mixing processes also may transport small numbers of dead shells and probably live embryons (e.g., Alve and Goldstein, 2003) or juveniles of diverse smaller taxa into the area, thereby anomalously elevating diversity. Group B sites were dominated by smaller miliolid foraminifers (Table 1). The sites characterized by subgroup B-1 were distributed throughout the north-central part of the bay (Fig. 3). This subgroup exhibited the lowest median shell density (Table 2), minimal contribution from symbiont-bearing foraminifers, and the greatest similarity to group C. The intermediate/intermittent stress occurring at these sites is further reflected in both median modified AEI (38) and FI (2.0). Thus, subgroup B-1 appears to represent the transition between the heavily impacted northern bay and more open-bay conditions. The subgroup B-2 assemblage occurred at sites farthest from anthropogenic influence, showed the greatest diversity, had the highest contribution from symbiont-bearing miliolids, and reflected the most open-marine influence. Subgroup B-3 assemblages, with intermediate values of diversity and density, dominated sites in the southern and south-central bay. Both modified AEI and FI values indicate the relatively good water quality at subgroup B-2 and B-3 sites (Table 2). Median modified AEI values were zero for both subgroups, reflecting the absence of Ammonia at most sites. Median FI values were 2.6 for both B-2 and B-3. The only sites with FI > 3 occurred in these subgroups. Three endpoints appear to influence distributions of foraminifers strongly throughout Biscayne Bay – freshwater, urban contamination, and oceanic waters. While several researchers have noted that, in practice, it is often difficult to separate effects caused by chemical contaminants from those caused by organic material and consequent hypoxia (Alve, 1995; Banerji, 1992; Cearreta et al., 2002; Debenay et al., 2001), Biscayne Bay illustrates different organic carbon and heavy metal gradients with distinct associated assemblages. Freshwater, carrying nutrients from agricultural activities, has the strongest influence on group A along the southwest margin of the bay, which is represented by reduced and variable salinity, increased TOC, and frequent hypoxia (Fig. 6). The influences of urbanization, including heavy-metal contamination (Carnahan et al., 2008), are reflected by group C in the northern

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sector. Oceanic influence characterized subgroup B-2, found in the east-central sector nearest the passes to the ocean. Subgroup B-3, found in the southern sector of the bay, was the least affected by any one influence and was a typical subtropical estuarine foraminiferal assemblage. When these interpretations were placed on the MDS plot (Fig. 2), subgroup B-1 was evident not only as intermediate between freshwater (group A) and oceanic (subgroup B-2) influences, but also as an intermediate between impacted (group C) and relatively unimpacted (subgroup B-3) subtropical estuarine foraminifers. Alve (1995) previously noted that as organic contamination increases, populations of tolerant species increase at the expense of more sensitive taxa (e.g., characteristic of our group A) until the contamination reaches toxic concentrations. In a study of a fjord in western Norway, Alve (1991) found that increased heavy-metal contamination corresponded with impoverished foraminiferal abundance (e.g., analogous to our group C). Miliolinella best described the foraminiferal assemblage throughout Biscayne Bay and, in combination with Ammonia, accounted for more than 70% of the variability among sites. Whereas Ammonia was nearly absent throughout the open bay, the genus was predominant in the northern portion of the bay, between the mainland and Key Biscayne, and nearshore in the southern bay close to canal sites (Fig. 5a). Miliolinella was rare in the northern bay, increased in abundance in the central bay, and reached maximum abundance in the southern bay, offshore (Carnahan, 2005). 4.2. Comparisons with earlier studies Bush (1958) identified Ammonia (which he called Streblus) in his 1948 collection (n = 63) as the 12th most common foraminiferal genus in the bay, characteristic of areas directly affected by dilution by freshwater and weak currents. He described a nearshore biotope affected by surface-water runoff from nearby land and drainage canals characterized by the presence of Ammonia. Ammonia was present in nearly all, and predominant (>10%) in five out of 16, of Bush’s (1958) northern bay sites and at its maximum, 30%, south of Black Creek Canal (Fig. 7a). Andersen (1975) reported that Ammonia dominated the western margin of the bay. The distribution of Ammonia in our study was consistent with that of Bush (1958). However, the areas of dominance have expanded (Fig. 7b). In our samples, the relative abundance of Ammonia in the northern bay was approximately double that reported by Bush and extended farther south and east than in Bush’s samples. In our samples, high proportions of Ammonia also extended farther south along the southern margin of the bay. In both studies, Ammonia was nearly absent throughout the open bay. Ishman et al. (1997) identified three distinct assemblages in Biscayne Bay: an Ammonia-Elphidium assemblage, an Archaias-miliolid assemblage, and a bolivinid assemblage. The AmmoniaElphidium assemblage was predominant in restricted environments (salinities < 35) in northern Biscayne Bay, Barnes Sound, and in adjacent freshwater-discharge points. The Archaias-miliolid assemblage was predominant at sites situated in unrestricted, open-marine central and southern Biscayne Bay. The bolivinid assemblage occurred in the northernmost Biscayne Bay, associated with diatomaceous muds that are rich in organic matter, indicating high productivity (Ishman et al., 1997). Samples were not collected from the northernmost sector of the bay for our study. Bolivinids tend to be tolerant of hypoxia and can dominate where organic carbon is abundant at normal marine salinities (Ishman et al., 1997). In our analysis, Elphidium clustered with the ‘‘other smaller” taxa rather than with the stress-tolerant taxa (Fig. 4). However, when Hoare (2002) analyzed the first set of samples collected for

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Fig. 7. Distribution of relative abundance of Ammonia (a) this study and (b) Bush.

our study, she found that Elphidium clustered with the stress-tolerant genera. This is not surprising, since Elphidium has been shown to withstand low-oxygen levels (Bernhard and Sen Gupta, 1999), environmental contamination (Yanko et al., 1999), and other stress, although the genus is clearly not as tolerant of oxygen depletion as is Ammonia (Sen Gupta et al., 1996). Elphidium, as well as Haynesina, Nonion, Nonionella, Bulimina, Fursenkoina, and Reophax, have been shown to sequester chloroplasts (e.g., Bernhard and Bowser, 1999; Cedhagen, 1991; Lopez, 1979). This relationship may provide these taxa with the potential to utilize chloroplast photosynthate when food supplies are limited, while not limiting their potential for rapid population increase when food is plentiful (e.g., Stoecker, 1998). Sorites was present in only 12% of our samples and never accounted for more than 5% of the assemblage in any sample. This dinoflagellate-endosymbiont-bearing miliolid was absent from all samples collected in December 2000 and was an outlier in samples from the other collections. Fujita and Hallock (1999) reported that Sorites appears to favor primary phytal substrates, particularity Thalassia blades, over epiphytized substrates, and predicted that Sorites populations would decline when increased nutrient input stimulated epiphytic growth on seagrass. Bush (1958) observed Sorites to be representative of the northeast portion of Biscayne Bay, an area influenced by the open ocean, and present in up to 10% abundance. In our study, Sorites never accounted for more than 2% of any sample in northeast Biscayne Bay. This disparity also indicated a displacement of Sorites from northeastern Biscayne Bay in the past 50 years. Archaias, the most abundant symbiont-bearing foraminifer that we identified, accounted for 16% of one sample and never more than 11% of the assemblage at any other site. In contrast, Bush (1958), reporting on samples collected in 1948, showed Archaias to be abundant (average > 18%) throughout central and southern Biscayne Bay. Even Ishman et al. (1997), working with samples collected in 1996, found Archaias sufficiently common to characterize one of their assemblages. This disparity is consistent with data pre-

sented by Fisher (2007) and Fisher et al. (2007), indicating that stressors affecting corals near a major pass that carries Biscayne Bay waters to the reef tract are relatively recent in onset. Archaias has consistently been rare in the northern bay (Bush, 1958; present work). Present distributions of both Archaias and Sorites elsewhere in the bay show quantifiable decline, reflecting decline in water and sediment quality in the central and southern bay over the past half century. Archaias tolerates strong salinity and temperature variability (Fujita and Hallock, 1999), but not organic loading and hypoxia (Hallock and Peebles, 1993). In our dataset, symbiont-bearing miliolids show a positive correlation to salinity that cannot be distinguished from a possible negative correlation with TOC, whose contoured data are a mirror image of salinity. Some agglutinated foraminifers, such as Reophax (Scott et al., 2005) and Trochammina (Tsujimoto et al., 2006; Zalensky, 1959) can be indicators of stressed environments. However, the most common agglutinates identified in this study, Valvulina and Siphonaperta, cluster with symbiont-bearing foraminifers that are indicative of more pristine environments (Hallock et al., 2003). These two genera secrete calcite cements (Loeblich and Tappan, 1988) and therefore likely require near-normal marine salinities. Bolivina and Brizalina were strongly correlated with each other and less strongly with other stress-tolerant taxa. These genera and other buliminids [e.g., Fursenkoina (Alve, 2003)] have been shown to tolerate high TOC and low-oxygen conditions (Bernhard and Sen Gupta, 1999). We recommend that foraminifers belonging to the order Buliminida be grouped with other stress-tolerant taxa in calculating the FORAM Index. 4.3. Ammonia-Elphidium and FORAM indices Hallock et al. (2003) proposed the FI as a simple, single-metric tool to determine if the quality of the environment is sufficient to support coral-reef growth or recovery. Based on our research in Biscayne Bay, we anticipate that the FI can also be a useful tool

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in subtropical estuarine assessment. The initial premise upon which the formula for the FI was based is that 100% other smaller taxa gives an FI = 2. Any addition of symbiont-bearing taxa raises the FI, any addition of stress-tolerant taxa lowers the FI from that reference value. An assemblage totally dominated by other smaller foraminifers says there is too much food for symbiont-bearing foraminifers to occur in any abundance (i.e., autotrophic and heterotrophic processes predominate), but not so much (or there is sufficient circulation) that biological oxygen demand in the upper sediments does not become limiting. Where oxygen becomes limiting, stress-tolerant forms would be prevalent. The more scarce nutrients and organic matter are, the more prevalent the mixotrophic symbiont-bearing taxa become. Calcifying mixotrophs (symbiont-bearing foraminifers and zooxanthellate corals) also tend to be longer lived and slower growing than their autotrophic/heterotrophic competitors for space, and more sensitive to highly variable oxygen because they have such high respiratory needs at night and produce excess oxygen during the daylight. The symbiont-bearing taxa and stress-tolerant taxa tend to be strongly negatively correlated. To have an FI > 2, there must be some symbiont-bearing taxa, and for FI > 4, symbiont-bearing taxa must make up at least 25% of the assemblage. Given the faster turnover rates of smaller taxa, water quality must be sufficiently nutrient poor on average for the shells of symbiont-bearing taxa to be relatively abundant. This is the basis for the assumption that if FI > 4, the environment consistently supports calcifying mixotrophs. Comparison of the FI values from our sample groups with FI values that we calculated from data reported by Bush (1958) provides valuable insight into FI variability and trends (Fig. 8). The data distribution for our subgroups B-2 and B-3, which are from the least impacted part of the bay, are essentially identical to the FI distribution for Bush’s data. In Bush’s data, approximately 10% of the samples had FI values that exceeded four; our dataset had only two out of 137, less than 2%. About 40% of Bush’s samples had FI values of three or higher, compared with only about 10% of the FI values for our sites, all from subgroups B-2 and B-3. The ‘‘baseline” FI for Bush’s data and for our groups B-2 and B-3 is 2; less than 10% of Bush’s samples had FI values < 2. FI values were less than two for about 40% of our samples, including roughly half of our subgroup B-1, most of group A, and all of group C (Fig. 8). Thus, the FI as a single-metric index can express what is shown graphically by comparing Fig. 7a and b, that stress-tolerant taxa are much more prevalent in the sediments of Biscayne Bay now than 50–60 years ago. One can legitimately ask what taxa should be included in the FI categories. Clearly, Ammonia was by far the most important stresstolerant genus in our dataset. MDS analysis by genus (Fig. 4) quite effectively differentiated the stress-tolerant taxa from the bulk of the other smaller miliolids and rotaliids, with only Elphidium

Fig. 8. Plot of FORAM Index values by site groups defined in Fig. 2 and Table 1, compared with data from Bush.

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occurring with the ‘‘other” taxa. Interestingly, together the FI and modified AEI further characterized the groups of sites. Group A sites had higher FI and higher modified AEI values, indicting organic loading and hypoxia, whereas both indices for group C sites were lower, indicating that other stressors, possibly chemicals from urban, industrial, or maritime sources, were more important than hypoxia in proximity to urban Miami. 4.4. Data limitations Samples analyzed in this study were collected in December 2000, July 2001, and April 2002. The first collection targeted sites in northern Biscayne Bay, including suspected areas of contamination in the upper part of the bay, along a transect projecting eastward of Black Point in southern Biscayne Bay, and several open-bay sites (Hoare, 2002). The second collection included mostly openbay sites with minimal terrestrial influence, and the third collection included 68 sites bay-wide. Thus, there is the possibility that temporal variations in measured parameters influenced the data. However, because total assemblages represent shell accumulations integrated through time, the assemblages are less susceptible to temporal perturbations than live assemblages and are therefore more directly comparable. Local blooms can potentially influence results, but that variability is equally likely within a sampling episode as between them (e.g., Buzas et al., 2002). Within the community of foraminiferal researchers, there is a controversy regarding analysis strategies. Murray and Alve (1999) and Murray (2000) argued eloquently for analyses of live assemblages only. However, Buzas et al. (2002) observed longterm stability in foraminiferal assemblages of a subtropical estuary despite substantial short-term variability in live assemblages in space and time, a phenomenon they called ‘‘pulsating patches.” Patchiness of live foraminifers in soft-bottom sediments is compounded when the dominant habitats are phytal (macroalgae and seagrass) and hard substrates (e.g., rocky seafloor outcrops, reef, or shell rubble), not the soft sediments themselves. Other researchers have argued that assessment of the accumulation of foraminiferal shells in the sediments (i.e., total assemblages) integrates information about the general conditions more effectively than that of living assemblages (e.g., Hallock et al., 2003; Scott and Medioli, 1980). In developing indicator guidelines for Gulf of Mexico estuaries, (Engle, 2000, p. 3–1) noted: ‘‘An ideal indicator of the response of benthic organisms to perturbations in the environment would not only quantify their present condition in ecosystems but would also integrate the effects of anthropogenic and natural stressors on the organisms over time. . ..” Hallock et al. (2003) argued that this information is precisely what the total assemblage of foraminiferal shells in the sediments can provide. Additionally, the research objectives, time frame being addressed, and resources available for the study should inform the investigator as to whether total assemblage will yield satisfactory results, or whether the much more labor-intensive sampling designs required for meaningful assessment of live assemblages must be employed. As part of the program for which the current analyses were conducted, heavy-metal concentrations were analyzed from the same samples (Carnahan, 2005; Carnahan et al., 2008; Hoare 2002). Copper, zinc, chromium, and lead all exhibited some degree of enrichment relative to background levels for Florida estuaries. Most of the samples analyzed indicated enrichment with respect to lead; roughly half were enriched with respect to copper and zinc (Carnahan et al., 2008). Chromium was only enriched in sediments collected immediately off Miami and near one drainage canal. Other anthropogenic contaminants known to enter south Florida estuaries, including polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), pesticides, herbicides, insecticides, and fungicides (Corcoran et al., 1984; Long and Morgan, 1990; Miles

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and Pfeuffer, 1997; Scott et al., 2002; Strom et al., 1992), were not measured and therefore their influence on assemblages remains unknown.

manuscript. Any use of trade names is for descriptive purposes only and does not imply endorsement by the U.S. Government. Acknowledgment does not imply endorsement of results by any of the funding or permitting agencies.

5. Conclusions References (1) The foraminiferal assemblages in Biscayne Bay indicate four major influences: (a) the northern sector of the bay is characterized by a low-density assemblage dominated by Ammonia and other stress-tolerant genera that reflect the combined influences of urban-sourced contamination and freshwater flux (19 genera/sample, FI 1.8, modified AEI 58); (b) the southwestern shoreline is characterized by a high density, low diversity, mixed assemblage dominated by Ammonia and Quinqueloculina that reflects flux of freshwater and organic matter (12 genera/sample, FI 1.8, modified AEI 75); (c) the eastern margin of the bay is characterized by oceanic influence, and is dominated by a diversity of smaller miliolid and rotalid foraminifers, with a small but significant contribution by symbiont-bearing taxa (26 genera/sample, FI 2.6, modified AEI 0); (d) the southern sector of the bay approximates natural estuarine conditions and is characterized overwhelmingly by smaller miliolid foraminifers (18 genera/ sample, FI 2.6, modified median AEI 0). (2) Two genera characterize the foraminiferal assemblages of Biscayne Bay: abundant Miliolinella indicate near-natural subtropical estuarine conditions, while domination by Ammonia reflects freshwater and/or contaminant-influenced areas of the bay. (3) The FORAM Index, which reflects water quality, and the modified Ammonia-Elphidium Index, as an indicator of hypoxia, in conjunction with diversity and abundance data, elucidated interpretation of environmental influences on a subtropical estuary. (4) Comparison of our data with foraminiferal-assemblage data published by Bush (1958) for Biscayne Bay indicates substantial expansion of areas dominated by Ammonia and a substantial decline in areas suitable for foraminifers that host algal endosymnbionts. These changes indicate longterm decline in water quality and benthic habitats in the bay.

Acknowledgments Funding for this work was provided by the University of South Florida/US Geological Survey Cooperative Agreement 99HQAG0004, the National Oceanic and Atmospheric Administration through the Florida Hurricane Alliance, and the US Environmental Protection Agency Gulf Ecology Division Grant No. X796465607-0. Water quality data were provided by the SERCFIU Water Quality Monitoring Network which is supported by SFWMD/SERC Cooperative Agreements #C-10244 and #C-13178 as well as EPA Agreement #X994621-94-0. We thank Eugene A. Shinn (USGS) and Randolph P. Steinen (University of Connecticut, Storrs, retired) for sample collection. We also thank Richard Z. Poore (USGS), Benjamin P. Flower (University of South Florida, College of Marine Science), Barun Sen Gupta (Louisiana State University), and an anonymous reviewer for critical comments on this

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