Impact of Late Holocene climate variability and anthropogenic activities on Biscayne Bay (Florida, U.S.A.): Evidence from diatoms

Palaeogeography, Palaeoclimatology, Palaeoecology 371 (2013) 80–92

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Palaeogeography, Palaeoclimatology, Palaeoecology journal homepage: www.elsevier.com/locate/palaeo

Impact of Late Holocene climate variability and anthropogenic activities on Biscayne Bay (Florida, U.S.A.): Evidence from diatoms Anna Wachnicka a, b,⁎, Evelyn Gaiser b, c, Lynn Wingard d, Henry Briceño b, Peter Harlem b a

Department of Earth and Environment, Florida International University, Miami, FL 33199, USA Southeast Environmental Research Center, Florida International University, Miami, FL 33199, USA Department of Biological Sciences, Florida International University, Miami, FL 33199, USA d U.S. Geological Survey, Reston, VA 20192, USA b c

a r t i c l e

i n f o

Article history: Received 16 July 2012 Received in revised form 7 December 2012 Accepted 12 December 2012 Available online 28 December 2012 Keywords: Diatoms Biscayne Bay Climate oscillation patterns Salinity changes Paleoecology

a b s t r a c t Shallow marine ecosystems are experiencing significant environmental alterations as a result of changing climate and increasing human activities along coasts. Intensive urbanization of the southeast Florida coast and intensification of climate change over the last few centuries changed the character of coastal ecosystems in the semi-enclosed Biscayne Bay, Florida. In order to develop management policies for the Bay, it is vital to obtain reliable scientific evidence of past ecological conditions. The long-term records of subfossil diatoms obtained from No Name Bank and Featherbed Bank in the Central Biscayne Bay, and from the Card Sound Bank in the neighboring Card Sound, were used to study the magnitude of the environmental change caused by climate variability and water management over the last ~ 600 yr. Analyses of these records revealed that the major shifts in the diatom assemblage structures at No Name Bank occurred in 1956, at Featherbed Bank in 1966, and at Card Sound Bank in 1957. Smaller magnitude shifts were also recorded at Featherbed Bank in 1893, 1942, 1974 and 1983. Most of these changes coincided with severe drought periods that developed during the cold phases of El Niño Southern Oscillation (ENSO), Atlantic Multidecadal Oscillation (AMO) and Pacific Decadal Oscillation (PDO), or when AMO was in warm phase and PDO was in the cold phase. Only the 1983 change coincided with an unusually wet period that developed during the warm phases of ENSO and PDO. Quantitative reconstructions of salinity using the weighted averaging partial least squares (WA-PLS) diatom-based salinity model revealed a gradual increase in salinity at the three coring locations over the last ~600 yr, which was primarily caused by continuously rising sea level and in the last several decades also by the reduction of the amount of freshwater inflow from the mainland. Concentration of sediment total nitrogen (TN), total phosphorus (TP) and total organic carbon (TOC) increased in the second half of the 20th century, which coincided with the construction of canals, landfills, marinas and water treatment plants along the western margin of Biscayne Bay. Increased magnitude and rate of the diatom assemblage restructuring in the mid- and late-1900s, suggest that large environmental changes are occurring more rapidly now than in the past. © 2012 Elsevier B.V. All rights reserved.

1. Introduction Shallow marine ecosystems are dynamic environments that support diverse life (Done and Jones, 2006). These ecosystems are under an enormous pressure from growing human population along coasts, and natural and human-induced climate variability (Ottersen et al., 2004; Nicholls et al., 2007; Doney, 2010; Hoegh-Guldberg and Bruno, 2010; Doney et al., 2012). Increasing loads of suspended

⁎ Corresponding author at: Southeast Environmental Research Center, Florida International University, University Park, OE 148, 11200 SW 8th Street, Miami, FL, USA. Tel.: +1 305 348 1876; fax: +1 305 348 4096. E-mail addresses: wachnick@fiu.edu (A. Wachnicka), gaisere@fiu.edu (E. Gaiser), [email protected] (L. Wingard), bricenoh@fiu.edu (H. Briceño), harlemp@fiu.edu (P. Harlem). 0031-0182/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.palaeo.2012.12.020

sediment, nutrients and industrial pollutants cause eutrophication of coastal waters and increase water turbidity (Ralph et al., 2006; Schaffelke et al., 2011). Concurrently, rising global air and sea surface temperatures change the intensity, frequency of occurrence and persistence of global climate phenomena such as El Niño Southern Oscillation (ENSO), Atlantic Multidecadal Oscillation (AMO) and North Atlantic Oscillation (NAO), which shape global precipitation and temperature patterns (Najjar et al., 2000; Walther et al., 2002; Doney et al., 2012). Consequently, changes in global precipitation and temperature patterns affect water quality conditions, which in turn affect marine biodiversity (Tunberg and Nelson, 1998; Stenseth et al., 2002; Briceño and Boyer, 2010; Wachnicka et al., 2011a, 2011b). These large-scale climate oscillation patterns (ENSO, AMO, and NAO) are well known sources of climatologically driven variations in marine populations (Stenseth et al., 2003;

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Hallett et al., 2004; Cloern and Jassby, 2010; Menge et al., 2011) and they often seem to be better predictors of ecological processes than the local climate (Hallett et al., 2004). However, distinguishing between changes in the community structure caused by anthropogenic activities and long-term natural variations that are attributable to natural causes is not an easy task in coastal marine ecosystems. In these ecosystems, changes associated with climate variability are often masked by changes caused by anthropogenic factors, and only careful analyses of ecological and climatological data, and knowledge of local development history, can help to disentangle the ecological consequences of these two factors. Florida has 36 times more residents today than it had in 1900 (18,538,000 vs. 528,542, respectively), and more than 13% of that population (2,496,435 residents) lives in Miami-Dade County, along the western shore of Biscayne Bay (U.S. Census, 2010). This rapid population growth has prompted development of a regional drainage and flood control system along the Biscayne Bay coast in the 1940s, 1950s and 1960s. Development led to a significant reduction of natural surface and ground freshwater flows into Biscayne Bay and caused water pollution. These transformations changed the character of the Bay from an estuary fed by coastal rivers, tidal creeks, and groundwater discharge, to a coastal lagoon with water deliveries constrained to point-source pulsed freshwater discharges through canals, especially pronounced in the subtropical wet season (Browder et al., 2005; Caccia and Boyer, 2005; Graves et al., 2005; McVoy et al., 2011). Additionally, construction of deep-water channels and cuts (e.g., Government Cut) in the northern part of the Bay destroyed seagrass beds, increased turbidity, prompted algae blooms, and changed the salinity and water circulation patterns across the Bay (Alleman et al., 1995; Meeder and Boyer, 2001; Browder et al., 2005; Renken et al., 2005). Previous paleoenvironmental studies in Biscayne Bay based on foraminifera, mollusks, ostracodes, and geochemical data have focused on investigating the effects of anthropogenic activities on the mainland on water quality in the Bay (e.g., salinity, nutrient concentrations; Ishman, 1997; Stone et al., 2000; Wingard et al., 2003, 2004, 2007), but no quantitative reconstructions of the past water quality conditions have been performed yet. Additionally, the impact of long-term climate variability on benthic communities in the Bay has not been fully investigated. The main objectives of this study were to: 1) quantitatively reconstruct past salinity conditions based on subfossil diatom records in 3 sediment cores retrieved from No Name Bank, Featherbed Bank and Card Sound Bank; 2) determine the timing and magnitude of significant shifts in diatom community structure; and 3) determine what the most plausible mechanisms for these shifts were by comparing the timing of the shifts to the well documented historic data of the major climatic and anthropogenic events that occurred in South Florida over the last several hundred years.

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Bank in south-central Bay (25°31.850′ N, 80°15.575′ W; Fig. 1). The third core was collected from the bank in the eastern part of the Card Sound (25°19.295′ N, 80°21.362′ W; Fig. 1). General areas of investigation were selected based on South Florida Water Management District research priorities to characterize pre-drainage conditions (prior to 1900) and to identify trends beginning in the 1960s and 1970s as a diversion of water caused changes in the freshwater distribution and influx into the Bay. Within these general areas, core sites were collected that had greater than 1 m of sediment cover, little human disturbance, and relatively low incidence of bioturbation. The No Name Bank core (GLW402-NNA) was extracted from ~0.5 m water depth on the bank, and was composed of calcareous sand deposits covered by dense seagrass beds of Thalassia testudinum mixed with Syringodium filiforme (Wingard et al., 2003, 2004). The Featherbed Bank core (GLW402-FBA) was retrieved from ~0.6 m water depth, in an area that was characterized by a series of carbonate sand “stringer shoals” that were densely vegetated by the T. testudinum, S. filiforme and Halodule wrightii seagrasses and Laurencia sp. green macroalgae (Wanless, 1976; Wingard et al., 2004). The Card Sound Bank core (GLW402-CBA) was retrieved from 0.76 m water depth in an area composed of carbonate sand sediments, and vegetated by patchy T. testudinum (Wingard et al., 2003, 2004). The bank is characterized by restricted water circulation due to its geographic isolation, and residence time of its waters can be up to 2–3 months (Lee, 1975). 3. Methods 3.1. Core collection Duplicate cores, A and B, were collected side by side (10–20 cm apart) from a pontoon barge equipped with a mounted tripod winch and an 11.4 cm in diameter polycarbonate tube, with a piston positioned at the bottom of the tube at the start of coring (Wingard et al., 2003). The cores were retrieved by pushing the tubes into the sediment until bedrock was reached or the tube could no longer be pushed. The cores were then recovered from the sediment by using the tripod winch, and the top and bottom of the tubes were capped to prevent sediment loss. All cores were X-rayed to determine the presence of bedding and lamination and to evaluate the extent of sediment disturbance (e.g., bioturbation), and examined for type of deposits. They were later sectioned into 2-cm slices and subjected to different paleontological and geochemical analyses (Wingard et al., 2003, 2004, 2007). Only cores marked with letter A were used for diatom analyses, while cores marked with letter B were used for other geochemical and biological analyses (Wingard et al., 2003, 2004, 2007). 3.2. Core dating

2. Study area and coring locations 2

Biscayne Bay is a relatively large (~ 700 km ), shallow (~ 1.8 m average depth), subtropical lagoonal estuary adjacent to the Miami metropolitan area of southeast Florida (Fig. 1). The Bay formed between ~ 5000–2400 yr ago, when rising sea level flooded the depression in the limestone bedrock (Wanless, 1976). The sediments of Biscayne Bay consist mostly of autochthonous calcareous and siliceous skeletal benthic organisms, although the northern part of the Bay receives detrital sediment and a quartz–carbonate sand influx from the southern Appalachian Mountains and pure quartz Pleistocene Pamlico Sand of the mainland Atlantic Coastal Ridge (Wanless, 1976). Three sediment cores, collected by the United States Geological Survey (USGS) in April 2002 were analyzed in this study. Two of the cores were retrieved from Biscayne Bay — one from an unnamed bank in the north-central part of the bay (25°34.484′ N, 80°16.320′ W) locally referred to as “No Name Bank”, and the second from the Featherbed

Age models for the cores were developed by using Lead 210 ( 210Pb; for sediments younger than 150 yr) and Carbon 14 (14C; for sediments older than 150 yr) radiometric methods, and pollen biostratigraphy (Wingard et al., 2007; Fig. 2). Two cores collected side by side (A and B) contributed to the development of the age models (Fig. 2). The 210 Pb method and the first stratigraphic appearance of Casuarina equisetiforma (Australian pine) pollen, introduced into South Florida ~1900, were used to determine the age of the last century deposits and to mark the beginning of the 20th century, while shell and wood fragments found in the sediments were dated by using 14C method to determine the age of older deposits (Wingard et al., 2007). The activity of 210Pb was measured by alpha spectroscopy following the method described by Flynn (1968) in the USGS Center for Coastal and Watershed Studies in St. Petersburg, Florida. The chronologic model used in this study was a simple first-order model developed by Robbins et al. (2000). In this model the flux of the atmospheric 210Pb

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Fig. 1. Map showing coring locations of No Name Bank (GLW402-NNA), Featherbed Bank (GLW402-FBA) and Card Sound Bank (GLW402-CBA) cores in Biscayne Bay and Card Sound (Florida, U.S.A.).

and sediment accumulation rate are assumed to be constant, and any variability in the 210Pb concentration (except for the decay-related variations) was averaged by sedimentological processes (Robbins et al.,

2000). The age models have been used to quantify sediment accumulation rates based on 210Pb decay profiles that take into account the variables of atmospheric flux, sediment supply, and mixing (Wingard et al.,

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Fig. 2. Age models for three cores: (a) No Name Bank (GLW402-NNA and NNB); (b) Featherbed Bank (GLW402-FBA and FBB); (c) Card Bank (GLW402-CBA and CBB). Age depth models were developed by using CAgeDepth function within the R software (Heegaard, 2003). LOI, loss on ignition, indicates organic material in core. Refer to Wingard et al. (2007) for all data and analyses associated with the age models and to Wingard et al. (2003) for complete lithologic descriptions.

2007). The 14C dating of sediments was conducted with the accelerator mass spectrometry (AMS) by Beta Analytical Inc. in Miami, Florida and by the USGS Radiocarbon Lab in Reston, Virginia. Radiocarbon 2-sigma age ranges were calibrated to calendar years by using Calib 5.0 (Stuiver and Reimer, 1993) and either a marine or terrestrial carbon correction factor was applied (Wingard et al., 2007).

3.3. Laboratory methods Approximately 1 g of sediment was removed from every 2-cm slice in the top 20 cm of each core and every 2 or 4 cm below that level. The subsamples were prepared for diatom analyses by removing organic and minerogenic matter, and salts with nitric acid, and settling and

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decanting them several times with deionized water until the mixture became neutral. Permanent diatom slides were made by placing 1 ml of the final suspension on No. 1 coverslips, air drying them and mounting them onto glass slides by using the Naphrax® mounting medium. Approximately 500 diatom valves were counted on each slide on random transects. Identification and enumeration of diatoms were made by using a Zeiss light microscope at 1008× magnification (N.A. = 1.4). The identification of species was based on the local and standard diatom taxonomic literature (for a complete list see Wachnicka, 2009). Total carbon (TC) and total nitrogen (TN) contents of sediments were determined by using a Leco 932 CNS Analyzer (Leco Corp., St. Joseph, MI, USA). Total organic carbon (TOC) was determined on the Leco analyzer after removal of inorganic carbon (IC, mostly carbonates) by an acid vapor method (Wingard et al., 2004). 3.4. Data sources and data analysis The abundance of each taxon was expressed as relative to the total and was arcsine squareroot transformed to more closely approximate a normal distribution (McCune and Grace, 2002). The average historic salinity levels at each of the study sites were estimated by applying a two-component weighted averaging partial least squares (WA-PLS) prediction model for salinity (Wachnicka et al., 2011a) to subfossil diatom assemblages preserved in the sediment cores. This prediction model was developed based on information about the relationships between modern diatom assemblages and salinity obtained from 58 sites across Biscayne Bay in April (dry season) and October (wet season) 2005 (Wachnicka et al., 2011a). This model (r 2apparent = 0.92 and r 2jackknife = 0.85) is capable of predicting salinity with a very small prediction error (RMSEP = 1.86 ppt). One thousand cycles of a bootstrapping resampling procedure was used to provide a sample-specific root mean square error of prediction for each sample in the core (Birks et al., 1990). A cumulative sum of standardized deviations technique (Z-Cusum), which is based on deviations from the mean, was used to identify changes in the percent diatom assemblage similarity, species richness, salinity, and concentration of total phosphorus (TP), total nitrogen (TN) and total organic carbon (TOC) in sediments, between consecutive samples in each core. The Z-Cusum analyses are very sensitive to small departures from the average values, and the increasing trends are displayed as concave curves, while the declining trends as convex curves (Briceño et al., 2010). Segments with negative slopes indicate below average values, while those with positive slopes indicate above average values (Briceño et al., 2010). The inflection point of the curves corresponds to the major shifts from below- to above-average values and vice versa (Briceño et al., 2010). Additionally, a parametric method based on sequential t-test analyses of regime shifts (STARS; Rodionov, 2004; Rodionov and Overland, 2005), was used to identify periods of time during which significant changes in a diatom assemblage structure (species composition and abundance) occurred and to determine if all the changes in the percent diatom assemblage similarity, species richness, salinity, and nutrients and organic matter concentration identified by using Z-Cusum analyses were statistically significant. The same method was used to detect regime shifts in the AMO, NAO, Pacific Decadal Oscillation (PDO), and Extended Multivariate ENSO (ENSO) indices, Palmer Drought Severity Index (PDSI), average annual air temperature in Miami (MIAT), total annual rainfall in Miami (MIAR), sea level in Key West, and average maximum water flow from major canals along the Biscayne Bay coast. The above mentioned data were obtained from the National Oceanic and Atmospheric Administration's (NOAA) Earth System Research Laboratory climate index database (NOAA, 2012), the South Florida Water Management District's (SFWMD) DBHYDRO environmental database (SFWMD, 2012) and the University of Anglia's Climate Research Unit climate database (CRUUEA, 2012) The advantage of the STARS

method is that it provides a probability level for the identified year of a regime shift, based on Student's t-test. When a new observation is included, a check is performed to determine whether it represents a statistically significant deviation from the mean value of the current regime (Rodionov, 2004; Rodionov and Overland, 2005). This method allows for the calculation of a Regime Shift Index (RSI), which represents a cumulative sum of normalized anomalies relative to a critical value (Rodionov, 2004; Rodionov and Overland, 2005). In this method the minimum length of the regimes, for which the magnitude of the shift remains intact, can be controlled by the cut-off length (year interval in the time series; Rodionov, 2004; Rodionov and Overland, 2005). A longer cut-off length allows for the identification of the strongest signal, while a shorter length allows for the identification of smaller events (Rodionov, 2004; Rodionov and Overland, 2005). Cut-off lengths of 10 calendar years and probability level 0.05 were chosen for regime shift detection to filter out all the shifts with a magnitude of one standard deviation or less if they lasted less than 10 yr.

4. Results 4.1. Lithostratigraphy and chronology The initial length of the cores collected from No Name Bank, Featherbed Bank, and Card Sound Bank were 150 cm, 195.5 cm, and 157.5 cm, respectively, but due to the compaction of sediments during transport the lengths decreased to 144 cm, 188 cm and 149 cm, respectively (Wingard et al., 2003). X-radiographs and visual inspection of the cores revealed that sediments in the upper portion of the cores were mostly composed of soft mud mixed with plant material and abundant mollusk shells, while the middle and bottom portions of the cores were composed of more cohesive mud to clay deposits mixed with scattered shells and plant material (Wingard et al., 2003; Fig. 2). 210 Pb and pollen biostratigraphy revealed that the upper 60 cm of sediments in GLW402-NNA, the upper 70–80 cm of sediments in core GLW402-FBA and the upper 30–46 cm in core GLW402CBAwere deposited during the 20th century (Wingard et al., 2007). The average sedimentation rates at the locations for the 20th century period were ~ 0.6 cm yr − 1, ~ 0.7 cm yr − 1, and 0.3–0.5 cm yr − 1, respectively (Wingard et al., 2007). The age model for GLW402-NNA was based on the basal 210Pb date at 60 cm depth and two radiocarbon dates obtained on the shells of a gastropod Turbo castanea (114–336 YBP at 89 cm) and a bivalve Chione cancellata (272–453 YBP at 139 cm) from GLW402-NNB (Wingard et al., 2007). The basal radiocarbon date indicated deposition of sediments within the core since ~ 1600 AD, with an average sedimentation rate of ~ 0.3 cm yr − 1 in the pre-20th century period (Wingard et al., 2007). The age model for GLW402-FBA was based on three radiocarbon dates obtained on the shells of a gastropod T. castanea (52–201 YBP at 109 cm, 52–285 YBP at 137 cm and 95–296 YBP at 187 cm) from GLW402-FBB (Wingard et al., 2007). The pre-20th century sedimentation rate at this location was ~ 1.4 cm yr − 1 (Wingard et al., 2007). Examination of X-radiographs and stratigraphy of the paired cores (A and B) indicated comparable deposition patterns between A and B cores at No Name Bank and Featherbed Bank, which justified the construction of a single age model for the pair of cores at each location (Wingard et al., 2007). An age model could not be developed for the Card Sound Bank cores due to a partial offset between the A and B cores (Wingard et al., 2007). Radiocarbon dating was conducted on shells of C. cancellata (bivalve) (378–553 YBP at 123 cm) in core GLW402-CBA and two shells of Bittiolum varium (gastropod) (174–390 YBP and at 41 cm and 359–534 YBP at 105 cm) in core GLW402-CBB (Wingard et al., 2007).

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4.2. Historical changes in diatom assemblage structure, salinity and sediment geochemistry

Diploneis didyma, Grammatophora oceanica, Synedra fulgens and Tryblionella granulata significantly decreased in abundance, while Actinocyclus ehrenbergii significantly increased (Fig. 4a). After ~1956, Amphora corpulenta var. capitata, Amphora ostrearia var. vitrea, Cyclotella litoralis, D. didyma, Diploneis suborbicularis, Grammatophora angulosa, Mastogloia sp. 13, Nitzschia graeffii, Nitzschia marginulata var. didyma and Parlibellus panduriformis significantly decreased in abundance, while Amphora sp. 07 and Cocconeis britanica significantly increased (Fig. 4a). The shift from below- to above-average salinity conditions occurred ~1909 (Fig. 3c). The earliest significant shift in average salinity, from 30.7 ppt to 34.3 ppt, occurred ~1827, and it was followed by the shift to 37.9 ppt ~1909 (Fig. 4a). Significant shifts towards higher TN, TP and TOC concentrations occurred ~1969 (Fig. 3d; Orem data from Wingard et al., 2004). After that time, the average TN, TP and TOC concentrations increased from 0.2% to 0.6%, 0.0070% to 0.0197%, and 1.9% to 4.6%, respectively (Fig. 4a). The 1956 major shifts in the diatom assemblage structure occurred when South Florida was experiencing major drought conditions (PDSI = −3.19; MIAT= 24 °C; MIAR= 67.9 cm/yr; Fig. 5). In 1956, ENSO, PDO, AMO and NAO were in cold phases (although the last two were not strong; Fig. 5). 164 166 168 170 172 174 176 178 180 182 184 186 188 190 192 194 196 198 200

1640 1660 1680 1700 1720 1740 1760 1780 1800 1820 1840 1860 1880 1900 1920 1940 1960 1980 2000

4.2.1. No Name Bank A total of 186 diatom taxa were identified in the core (Appendix 5.1 in Wachnicka, 2009), with Grammatophora oceanica, Mastogloia bahamensis, Mastogloia corsicana, Mastogloia cribrosa, Campylodiscus ecclesianus, Dimeregramma dubium and Synedra fulgens occurring most frequently in the samples. Z-Cusum analysis revealed an overall declining trend in assemblage similarity between the consecutive samples moving up in the core (Fig. 3a). The main shift from aboveto below-average similarity values occurred ~ 1956 (Fig. 3a). In the post-1956 period, the magnitude and rate of assemblage restructuring increased and the average similarity fell to 52.7% from 67.9% (Fig. 4a). The main shift from below- to above-average species richness occurred ~ 1827 (Fig. 3b). In the post-1827 period, the average richness increased from 37 to 45 taxa per sample, and in the post-1993 period it increased again to an average of 52 taxa per sample (Fig. 4a). The most significant shift in the assemblage structure occurred ~1956 (RSI = 4.91; Figs. 4a and 5) and was preceded by a smaller shift ~1720 (RSI= 2.98; Fig. 4a). In the post-1720 period, taxa such as

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Fig. 3. Cumulative sums of standardize anomalies (Z-Cusum) of the diatom assemblage compositional similarities between consecutive samples (a), species richness (b) and diatom-inferred salinity (c) in the No Name Bank (GLW402-NNA), Featherbed Bank (GLW402-FBA) and Card Sound Bank (GLW402-CBA) cores, and sediment total phosphorus (TP), total nitrogen (TN) and total organic carbon (TOC) in the GLW402-NNA (d), GLW402-FBA (e) and GLW402-CBA (f) cores. Negative slopes indicate below average values, while positive slopes indicate above average values. Inflection points of the curves correspond to the main shifts from below- to above-average values and vice versa.

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poor below the 120 cm level. Among the taxa, Paralia sulcata var. genuina f. coronata, G. oceanica, P. sulcata var. genuina f. radiata and C. ecclesianus were the most frequently occurring in the samples.

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Fig. 4. Significant changes in species composition and abundance of taxa, % similarity between consecutive samples in the core, species richness, diatom-inferred salinity, TP, TN and TOC in GLW402-NNA (a), GLW402-FBA (b) and GLW402-CBA (c) cores. Gray lines indicate significant changes in the values of the abovementioned variables determined by the STAR method.

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Fig. 4 (continued).

Assemblage similarity between the consecutive samples in the core experienced its main change ~ 1932 (Fig. 3a). After that time, the average similarity decreased significantly from 68.9% to 29.8%, and then increased to 56.1% after ~ 1974 (Fig. 4b). The main shift in species richness also occurred ~ 1932 (Fig. 3b). After that time, the average richness increased from 28 to 47 taxa per sample (Fig. 4b). The largest shift in the assemblage structure, which involved the largest changes in abundance of the highest number of species, occurred in the post-1966 period (RSI =6.3; Figs. 4b and 5). This shift involved Amphora coffeiformis, Mastogloia angulata, Mastogloia cruticula, Mastogloia cyclops, Mastogloia lacrimata, Mastogloia punctifera and Mastogloia emarginata which significantly increased in abundance, and G. oceanica which significantly decreased. The second largest shift occurred ~1942 (RSI = 6.1), and it involved Trachyneis aspera, M. cribrosa, Diploneis crabro, C. ecclesianus, Campyllodiscus limbatus and A. ehrenbergii, which significantly decreased in abundance (Figs. 4b and 5). Another large shift during which the average abundance of Toxarium undulatum, Mastogloia fimbriata, G. angulosa, D. dubium, Cymatosira lorenziana and C. britanica significantly increased occurred ~1974 (RSI = 5.2; Figs. 4b and 5), and this was followed by the post-1983 shift, which involved Rhopalodia cf. acuminata, Hyalosynedra laevigata, Cocconeis scutellum and Cocconeis cf. neothumensis, which significantly increased in abundance. Less significant shifts, which also involved several taxa, occurred in the post-1861 and post-1893 periods (RSI=3.7 and RSI =2.4, respectively; Figs. 4b and 5). During the former shift, the abundance of Surirella fastuosa, Nitzschia marginulata var. didyma, Mastogloia splendida, and Mastogloia bahamensis significantly increased, while G. oceanica, C. limbatus and C. ecclesianus decreased (Fig. 4b). During the later shift, the abundance of T. aspera and D. dubium significantly increased, while M. splendida, M. fimbriata and H. laevigata decreased (Fig. 4b). The major change in average salinity occurred ~1822 (Fig. 3c) when it shifted from 25.8 ppt to 37 ppt (Figs. 3c and 4b). The main change from below- to above-average TN, TP and TOC concentrations occurred

~1966, ~1937 and ~1942, respectively (Fig. 3e; Orem data from Wingard et al., 2004). In the post-1966 period, the average TP concentration increased from 0.008% to 0.015% (Figs. 3e and 4b). The first significant increase in average TN concentration from 0.194% to 0.296% occurred in the post-1896, and then the second to 0.473% in the post-1947 period (Figs. 3e and 4b). The average TOC concentration increased at first from 2.2% to 2.6% after ~1896, and then again to 3.5% after ~1947 (Figs. 3e and 4b). The 1966 restructuring of diatom assemblages coincided with exceptionally low average air temperatures (MIAT = 23.5 °C) during the cool phases of PDO and NAO, and the initiation of the cool phase of ENSO (Fig. 5). Additionally, this shift was preceded by the 1964 and 1965 Hurricanes Cleo (Cat. 2) and Betsy (Cat. 3), which also possibly contributed to assemblage restructuring. The 1942 restructuring coincided with the acceleration of sea level rise and very dry conditions (MIAR =31.9 cm/yr) that occurred during a positive phase of AMO and when PDO was switching to a negative phase (Fig. 5). The 1974 change also coincided with a sharp increase in the mean sea level, and an exceptionally dry and hot time period (PDSI = −1.87; MIAT = 25.2 °C; MIAR = 119.6 cm/yr), which developed during the cold phases of ENSO, AMO and PDO (Fig. 5). During that time the flow from canals increased, but not significantly (Fig. 5). The latest change ~1983 coincided with a wet period that occurred during the warm phases of PDO, NAO and ENSO (Fig. 5). During that time the flow from canals was very low (Fig. 5). 4.2.3. Card Sound Bank A total of 191 diatom taxa were identified in the CBA core (Appendix 5.3 in Wachnicka, 2009) and the preservation of the diatom valves was excellent between 122 and 0 cm depth (from ~1480 to 2002) (Appendix 5.3 in Wachnicka, 2009). The most frequently occurring taxa in the core were G. oceanica, A. corpulenta var. capitata, Cyclotella distinguenda and Synedra bacilaris. The main shift in assemblage similarity between the consecutive samples in the core occurred ~1905 (Fig. 3a). The

A. Wachnicka et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 371 (2013) 80–92

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Fig. 5. Links between historical changes in large-scale climate oscillation patterns, local precipitation and air temperature patterns, sea level and maximum water flow from major canals along the Biscayne Bay coast, and major shifts in diatom assemblage structure at No Name Bank (black bars and line), Featherbed Bank (gray bars and lines), and Card Sound Bank (stripped bars and dotted line). Vertical black lines indicate significant regime shifts in major climate indices, local climate variables and average water flow from major canals along the Biscayne Bay coast.

Assemblage similarity was on average 64.2% before ~1905 but decreased to average 52.8% after that period (Figs. 3a and 4c). An important shift from below- to above-average species richness occurred ~1957 (Fig. 3b). In the post-1957 period, average species richness increased significantly from 39 to 54 taxa per sample (Fig. 3b and 4c). The post-1957 period was also characterized by the largest restructuring of diatom assemblages, which involved 17 taxa (RSI= 4.9; Figs. 4c, 5). After that time, many Mastogloia spp. (M. biocellata, M. corsicana, M. discontinua, M. erythreae, M. lacrimata, M. ovalis, M. pisciculus, M. pusilla, M. punctifera, and M. rimosa), Amphora sp. 03, H. laevigata, N. longa var. irregularis and Rhopalodia cf. pacific significantly increased in abundance, while C. distinguenda, D. didyma and G. oceanica significantly decreased (Fig. 4c). The main change in average salinity occurred ~1538. In the following years, average salinity significantly increased to 36.7 ppt from 34.2 ppt before that time (Figs. 3c and 4c). The main shift in average TN, TP and TOC concentrations occurred ~1946, ~1900 and ~1887, respectively (Fig. 3f; Orem data from Wingard et al., 2004). The average TN and TOC concentrations increased significantly from 0.537% to 0.879% and from 5.1% to 7.3%, respectively after ~1887 (Fig. 4c). Additional significant increases in TN and TOC concentrations from 0.879% to 1.04% and 7.3% to 8.3%, respectively were also recorded after ~1997 (Fig. 4c). The first significant increase in average TP concentration (from 0.008% to 0.011%) occurred after ~1900, and the second one (to 0.020%) after ~1987 (Fig. 4c).

The major restructuring of the diatom assemblages ~1957 occurred during an exceptionally dry period (PDSI = −3.55; MIAT = 24.2 °C; MIAR = 89 cm/yr; Fig. 5). In 1957, ENSO, AMO and PDO were switching to positive phases, which resulted in wetter conditions in the following years (Fig. 5). 5. Discussion The structure (species composition and abundance) of the diatom assemblages at the three coring locations in Biscayne Bay changed significantly over the last few hundred years in response to changing environmental conditions caused by natural and anthropogenic factors. Analyses revealed that the rate and magnitude of the diatom assemblage restructuring, and the magnitude of the salinity variations, and nutrient and organic carbon concentrations in sediments increased during the second half of the 20th century. This is not surprising, since this period marks the beginning of the unprecedented global climate change (Levitus et al., 2001; Barnett et al., 2005; IPCC, 2007; Swanson and Tsonis, 2009), which is characterized by the occurrence of more extreme climate conditions to much of the United States, including South Florida (Easterling et al., 2000; NOAA, 2012). However, climate change cannot exclusively be blamed for the environmental changes in the Bay because even the occurrence of more severe climate conditions in this region during the Little Ice Age (Lund and Curry, 2006; Richey et al., 2009) did not result in large-scale restructuring of the

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diatom assemblages comparable to those that occurred during the 20th century. An intensive urbanization of the southeast Florida coast (Sklar et al., 2002; Renken et al., 2005; McVoy et al., 2011) caused by a surge of population growth after the World War II, resulted in major changes of the South Florida hydroscape (Renken et al., 2005; U.S. Census, 2010; MIAMI, 2012). Because the population of South Florida is largely confined to an elevated strip of land between the Atlantic Ocean and the Everglades (the Atlantic Coastal Ridge), the rapid urbanization of coastal areas along the southeastern coast of Florida put enormous pressure on nearshore habitats of the adjacent Biscayne Bay. Analyses showed that the combined effect of the intensification of climate change and rapid urbanization of the southeast Florida coast (Sklar et al., 2002; Renken et al., 2005; McVoy et al., 2011) significantly decreased the ability of the Biscayne Bay ecosystem to absorb and respond to changes in the driving variables, which led to a distinct ecological regime shift at the study locations in the late 1950s and the early 1960s. Similar shifts were also observed at the nearshore locations in the neighboring Florida Bay (Wachnicka et al., 2011b), which suggests that the changes had a regional character. Significant increase in the extraction of freshwater for drinking, farming and watering of lawns, and development of canals, levees and highways along the southeastern coast, caused significant reduction and in many cases an almost complete elimination of the overland freshwater flow from the Everglades through coastal wetlands and underwater springs to nearshore areas of Biscayne Bay (Sklar et al., 2002; Graves et al., 2005; Renken et al., 2005; McVoy et al., 2011). These ground freshwater discharges were once sufficient enough to allow mariners to collect drinkable water directly from the Bay (Munroe and Gilpin, 1930; Parker et al., 1955; Renken et al., 2005), which played an important role in the formation of distinct biological community zonation (Kohout and Kolipinski, 1967) and most likely helped to prevent the development of hypersaline conditions during severe droughts. This later statement is supported by the diatom-based salinity reconstructions, which revealed that salinity was above average at Card Sound Bank and No Name Bank during the mid-1970s' drought (when the hydroscape on the mainland was already significantly altered), but a similar situation did not occur during the earlier droughts (prior to and during the early stages of urbanization). Even though groundwater discharge into the nearshore areas of Biscayne Bay still occurs (Langevin, 2001; Reich et al., 2006), most of it is re-circulated seawater and only a small part is freshwater (Kohout and Kolipinski, 1967; Langevin, 2001). The water is also rich in nutrients, especially nitrogen, which originates in the agricultural and urban areas of Miami-Dade County (Alleman et al., 1995; Meeder et al., 1997; Meeder and Boyer, 2001; Caccia and Boyer, 2005; Graves et al., 2005; Renken et al., 2005; Carey et al., 2011a, 2011b). Earlier studies revealed that highly permeable soils under drainage canals result in nutrient leaching into groundwater, which eventually discharges into nearshore areas of the Bay together with water from the canals (Li and Zhang, 2002; Caccia and Boyer, 2005; Graves et al., 2005; Renken et al., 2005). Nitrogen and phosphorus concentrations in the water and sediments near the Black Creek, Princeton, Military and Mowry canals are much higher compared to any other location in the Bay (Caccia and Boyer, 2005; Wachnicka et al., 2011a, 2011b, 2011c). Additional sources of pollution include the South Dade Landfill and Treatment Plant (in operation since 1979) and the Old South Dade Dump (closed in 1968), which pollute the Bay waters via coastal groundwater discharges and surface water discharges from the Black Creek and Goulds Canals that drain the area (Church et al., 1980; Alleman et al., 1995; Meeder and Boyer, 2001; Caccia and Boyer, 2005). Runoff from the South Dade Agricultural basin also contributes to the problem (Alleman et al., 1995; Caccia and Boyer, 2005). The Snapper Creek and Coral Gables Waterway discharge nutrient-rich, heavy-metal-contaminated waters into the section of the Bay where the GLW402-NNA core was collected, causing a

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significant damage to nearshore coastal habitats (Alleman et al., 1995; Wachnicka (personal observation)). Concentration of phosphorus in the Biscayne Bay waters is relatively low (SERC, 2012) because it is quickly scavenged from the water by calcium carbonate-rich sediments and phytoplankton (Brand, 1988), while the nitrogen-rich water can affect an area up to 15 km from the point of discharge (Caccia and Boyer, 2005; Graves et al., 2005; SERC, 2012). Therefore it is not surprising that even the Featherbed Bank, which is located ~ 11.5 km away from the coast, experienced a significant increase in sediment nutrient concentration during the 20th century, even though this site has a much shorter water residence time compared to the other coring locations due to its proximity to the “Safety Valve”, where the exchange of water between the Bay and the Atlantic Ocean occurs. A similar temporal increase in sediment nutrient concentration was observed at Card Sound Bank, which had the highest concentration of nutrients in sediments, and at No Name Bank, where nutrient concentration levels were intermediate. On average, the highest concentration of nutrients at Card Sound Bank is most likely a result of poor water circulation and flushing, long water residence time and high evaporation rates (Alleman et al., 1995). These conditions are also responsible for the development of periodic hypersaline conditions and sudden salinity decreases at the site (Alleman et al., 1995). For example, above average salinity conditions developed at Card Sound Bank during severe droughts of the mid-1970s (average salinity 38.8 ppt), while a short-term drop in salinity occurred in the early 1980s (average salinity 32.2 ppt) when precipitation was high. The 1970s' temporal salinity increase was also recorded at No Name Bank and the 1980s' salinity drop was recorded at Featherbed Bank. The significant increase of organic carbon concentration in sediments, with the highest average concentration occurring in the cores retrieved from the nearshore areas and the lowest at the most distant coring site, are most likely a result of loading of the canals and groundwater in this zone (Alleman et al., 1995; Meeder and Boyer, 2001; Caccia and Boyer, 2005). Cultural eutrophication is a common problem facing coastal marine ecosystems around the world today (Kelly, 2008; Smith and Schindler, 2009). Addition of phosphorus and nitrogen to sediment in shallow estuaries can increase vegetation abundance and change the composition of microbenthic communities attached to them (Armitage et al., 2005; Frankovich et al., 2009). This situation occurred at Featherbed Bank and Card Sound Bank, and to a lesser extent at No Name Bank, where seagrass-associated taxa such as Mastogloia spp., Cocconeis spp. and H. laevigata (Frankovich et al., 2009; Wachnicka et al., 2010) significantly increased in abundance since the late 1950s. The presence of taxa belonging to the abovementioned genera in the lower parts of the cores indicates the presence of some type of vegetation at the banks throughout the time of deposition. This observation can be supported by the continuous presence of the vegetation-associated mollusk taxa at the same coring locations (Wingard et al., 2004). Additionally, lower abundance of vegetation-associated diatom taxa at Card Sound Bank during the 16th, the early 17th and the first part of the 20th century was accompanied by a low abundance of vegetationassociated mollusk taxa (Wingard et al., 2004), which suggests the presence of less dense sub-aquatic vegetation at the location during these time periods. Analyses revealed that there are strong links between major shifts in the diatom assemblage structures and large-scale climate oscillation patterns. Most of the largest shifts occurred when ENSO, AMO and PDO were in the cold phases, or when these climate oscillation patterns were switching from one phase to another (most often from warm to cold phase). Only the 1957 and 1983 assemblage restructuring occurred when ENSO and PDO were in the warm phases. In the case of the 1957 restructuring, AMO was also in a warm phase and in the case of the 1983 restructuring NAO was also in a warm phase. Computer simulations revealed that when cold PDO and AMO phases overlap, the

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South Florida region experiences extremely dry conditions (McCabe et al., 2004). Similar conditions develop, when cold PDO and ENSO overlap (Gershunov and Barnett, 1998). On the contrary, precipitation in South Florida increases during the positive phases of ENSO and AMO (Enfield et al., 2001; Childers et al., 2006). Although links between the large-scale climate oscillation patterns, and hydrology and biota have been poorly investigated in Florida, the existing studies showed that the inflow of water to Lake Okeechobee (Central Florida) and river flow in west-central Florida are indeed higher than average during warm ENSO and AMO years (Enfield et al., 2001; Kelly, 2004; Abtew and Trimble, 2010). Changes in precipitation and freshwater deliveries from the mainland result in significant inter- and intra-annual fluctuations of water quality in the South Florida estuaries. For example, salinity in shallow areas of the Biscayne Bay can rise to more than 40 ppt during dry periods and drop to less than 15 ppt during wet periods (SERC, 2012). Earlier studies showed that salinity, together with nutrient concentration and temperature, is the most influential variable structuring diatom assemblage in the South Florida estuaries and other shallow marine ecosystems around the world (Frankovich et al., 2006; Tibby et al., 2007; Frankovich et al., 2009; Saunders, 2010; Wachnicka et al., 2010, 2011a). Even though many estuarine diatom taxa can tolerate wide changes in water quality conditions, most of them cannot tolerate extreme and long-lasting alterations, which results in significant and often irreversible changes in the diatom assemblage structure (Saunders et al., 2007; Wachnicka et al., 2010, 2011a). Salinity reconstructions revealed that the average salinity levels at all the coring locations gradually increased, although the inferred values of salinity should be interpreted with caution since no evaluation of the influence of autocorrelation on the developed transfer function was performed (Telford and Birks, 2009). These results imply that the increase was primarily a result of a rising sea level. In this region sea level is rising at the rate of ~2.27 +/− 0.09 mm/yr based on 87 yr of data from the tide gauge stations in the Key West (Wanless, 1976; Maul and Martin, 1993; Zervas, 2001). The increasing trend in salinity can be additionally confirmed by the gradual decrease in abundance of taxa such as T. granulata, C. distinguenda, and D. suborbicularis (especially in the CBA and NNA cores), which flourish in average salinity conditions not exceeding ~35 ppt in nearshore and mangrove areas, and their abundance declines in hypersaline conditions (Gaiser et al., 2005; Wachnicka et al., 2010, 2011a). These taxa were replaced with species that are better adapted to hypersaline conditions, including C. britanica, D. dubium, and many Mastogloia spp. (Gaiser et al., 2005; Wachnicka et al., 2010, 2011a). These results support earlier findings of Wingard et al. (2003, 2004) based on the analyses of changes in the assemblage structure and the salinity preferences of foraminifera, mollusk, and ostracod taxa from the same locations. The average salinity increase was smallest at Card Sound Bank (~2 ppt in the last ~510 yr), followed by No Name Bank (~7 ppt in the last ~355 yr) and Featherbed Bank (~13 ppt in the last ~150 yr). Reconstruction of the historic salinity levels at Featherbed Bank exposed few time periods characterized by very low salinity conditions, the most recent of them occurring in 1953 (18.3 ppt), 1966 (19.5 ppt) and 1983 (7.8 ppt), when precipitation levels increased. However, these results are questionable and require further investigation because the site is located approximately 11.6 km away from the coast and close to the “Safety Valve”, where the intra- and interannual salinity variations are relatively small (SERC, 2012). It is possible that the increased abundance of fresh- and brackish water taxa in the core is a result of the transportation of sediment from the nearshore areas of the Bay toward the “Safety Valve” with currents and entrapment of that sediment by seagrass beds at the Featherbed Bank, or the migration of the bank, which was earlier suggested by Stone et al. (2000). The former hypothesis can be supported by Wang et al.'s (2003) modeling of the velocity and direction of the surface water movement in Biscayne Bay and the study of the origin of the carbonate mud banks in Biscayne Bay by Wanless et al. (1995). The former study indicated a general movement of water

from nearshore areas in the central part of the Bay toward Featherbed Bank, while the later study showed that Featherbed Bank appears to be a direct result of water circulation and storm sediment flow through the “Safety Valve”. Furthermore, studies of the modern diatom assemblages in Biscayne Bay did not encounter fresh- and brackish water taxa at Featherbed Bank (Wachnicka et al., 2011a), which further supports the theory of the allochthonous nature of the fresh- and brackish water taxa recorded in the GLW402-FBA core. The significant reduction in abundance and often complete disappearance of taxa with salinity optima below 30 ppt since the mid-1900s, when the major alterations of the South Florida hydrosphere began, strongly suggest that anthropogenic factors also played an important role in the transformation of the salinity patterns in Biscayne Bay. 6. Conclusions Analyses of the Late Holocene diatom records obtained from Biscayne Bay showed that the combined effects of climate change and anthropogenic drivers overwhelmed the resilience of the Biscayne Bay ecosystem, which resulted in a significant ecological shift during the second half of the 20th century. Additionally, data showed that severe, prolonged droughts associated with the cold phases of ENSO, AMO and PDO, and the warm phases of AMO and the cold phases of PDO, strongly influence microbenthic communities in the Bay, which was reflected in the significant restructuring of diatom assemblages during the intensification of these oscillation patterns. Furthermore, switching of these oscillation patterns from one phase to another (most often from warm to cold phase) and to a lesser extent development of wet conditions during the warm phases of ENSO and AMO, also caused significant restructuring of the assemblages. Obtaining multiproxy, higher resolution (e.g., inter-annual) data on changes in the microbenthic community structure would further help to expose links between major large-scale atmospheric and oceanic circulation patterns and microbenthic communities. This information would help to improve our ability to estimate future responses of shallow marine ecosystems to climate change. This is an extremely important task, since these ecosystems act as nursery grounds for countless numbers of marine organisms, and they will be affected by climate change much earlier compared to deeper parts of the ocean. Quantitative salinity reconstructions indicate that long-term salinity increase in the open-water areas of the Bay is primarily a result of rising sea level. However, intensive urbanization of the southeast Florida coast and related to that reduction of freshwater discharges into Biscayne Bay also contributed to salinity increase during the 20th century. Anthropogenic factors most likely played even a more important role in shaping salinity patterns in areas located closer to the coast, but to test this would require obtaining additional historical records from nearshore areas of the Bay known to have groundwater discharge in the past. The effect of urbanization of the coastal areas along the Biscayne Bay coast is also evident in the increased levels of sediment nutrients (increased flux is superimposed on natural diagenetic recycling of nutrients), and associated with that increase in magnitude and rate of diatom assemblage restructuring since the mid-1900s. Acknowledgments This study was financially supported by the United States Geological Survey (USGS; Cooperative Agreement) # 800000961. Funding for the initial collection and radiometric dating of the cores was provided by the USGS Greater Everglades Priority Ecosystems Science (GEPES) effort, G. Ronnie Best, Coordinator, and by South Florida Water Management District (Contract C-13400), and Richard Alleman and Trisha Stone, Project Managers. The Biscayne National Park provided access to the coring sites and the research was conducted as part of the NPS Study Number BISC-02027. The core collection and processing were done by James Murray (USGS), Rob Stamm (USGS), and Carlos Budet

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(former USGS contractor). Lead-210 analyses were conducted by Charles W. Holmes (USGS, retired) and Marci Marot (USGS), pollen biostratigraphy by Debra Willard and Christopher Bernhardt (USGS), and sediment geochemistry by William Orem (USGS). The GIS map (Fig. 1) was generated by Bethany Stackhouse (USGS). Any use of trade names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This is contribution number 588 from the Southeast Environmental Research Center at Florida International University. References Abtew, W., Trimble, P., 2010. El Niño–Southern Oscillation link to South Florida hydrology and water management applications. Water Resources Management 24 (15), 4255–4271. Alleman, R.W., Bellmund, S.A., Black, D.W., Formati, S.E., Gove, C.A., Gulick, L.K., 1995. An update of the surface water improvement and management plan for Biscayne Bay. Technical Supporting Document and Appendices. South Florida Water Management District, West Palm Beach, FL. Armitage, A.R., Frankovich, T.A., Heck, K.L., Fourqurean, J.W., 2005. Experimental nutrient enrichment causes complex changes in seagrass, microalgae, and macroalgae community structure in Florida Bay. Estuaries 28, 422–434. Barnett, T.P., Pierce, D.W., Achuta Rao, K.M., Gleckler, P.J., Santer, B.D., Gregory, J.M., Washington, W.M., 2005. Penetration of human-induced warming into the world's oceans. Science 309, 284–287. Birks, H.J.B., Line, J.M., Juggins, S., Stevenson, A.C., Ter Braak, C.J.F., 1990. Diatoms and pH reconstruction. Philosophical Transactions of the Royal Society of London, Series B 327, 263–278. Brand, L., 1988. Assessment of plankton resources and their environmental interaction in Biscayne Bay, Florida. Dade Environmental Resource Management Technical Report, p. 79. Briceño, H.O., Boyer, J.N., 2010. Climatic controls on phytoplankton biomass in a subtropical estuary, Florida Bay, USA. Estuaries and Coasts 33 (2), 541–553. Briceño, H., Boyer, J., Harlem, P., 2010. Proposed methodology for the assessment of protective numeric nutrient criteria for South Florida estuaries and coastal water. Technical Report of the Southeast Environmental Research Center, T-501. Browder, J.A., Alleman, R., Markley, S., Ortner, P., Pitts, P.A., 2005. Biscayne Bay conceptual ecological model. Wetlands 25, 854–869. Caccia, V.G., Boyer, J.N., 2005. Spatial patterning of water quality in Biscayne Bay, Florida as a function of land use and water management. Marine Pollution Bulletin 50, 1416–1429. Carey, R.O., Migliaccio, K.W., Li, Y.C., Schaffer, B., Kiker, G.A., Brown, M.T., 2011a. Land use disturbance indicators and water quality variability in the Biscayne Bay Watershed, Florida. Ecological Indicators 11, 1093–1104. Carey, R.O., Migliaccio, K.W., Brown, M.T., 2011b. Nutrient discharges to Biscayne Bay, Florida: water quality trends, loads, and a pollutant index. Science of the Total Environment 409, 530–539. Childers, D.L., Boyer, J.N., Davis, S.E., Madden, C.J., Rudnick, D.T., Sklar, F.H., 2006. Relating precipitation and water management to nutrient concentrations in the oligotrophic “upside-down” estuaries of the Florida Everglades. Limnology and Oceanography 51 (1), 602–616. Church, P., Donahue, K., Alleman, R., 1980. The Nitrate Monitoring Program. DERM, Miami, FL, p. 26. Cloern, J.E., Jassby, A.D., 2010. Patterns and scales of phytoplankton variability in estuarine–coastal ecosystems. Estuaries and Coasts 33, 230–241. CRUUEA, 2012. http://www.cru.uea.ac.uk/cru/. Done, T.J., Jones, R., 2006. Tropical coastal ecosystems and climate change prediction: global and local risks. In: Phinney, J.T., Hoegh-Guldberg, O., Kleypas, J., Skirving, W., Strong, A. (Eds.), Coral Reefs and Climate Change: Science and Management. : Coastal and Estuarine Studies, 61. American Geophysical Union, pp. 5–32. Doney, S.C., 2010. The growing human footprint on coastal and open-ocean biogeochemistry. Science 328, 1512–1516. Doney, S.C., Ruckelshaus, M.H., Duffy, J.E., et al., 2012. Climate change impacts on marine ecosystems. Annual Review of Marine Science 4, 11–37. Easterling, D.R., Evans, J.L., Groisman, P.Ya, Karl, T.R., Kunkel, K.E., Ambenje, P., 2000. Observed variability and trends in extreme climate events: a brief review. Bulletin of the American Meteorological Society 81, 417–425. Enfield, D.B., Mestas-Nuñez, A.M., Trimple, P.J., 2001. The Atlantic multidecadal oscillation and its relation to rainfall and river flows in the continental. U.S. Geophysical Research Letters 28 (10), 2077–2080. Flynn, W.W., 1968. The determination of low levels of polonium-210 in environmental materials. Analytica Chimica Acta 43, 221–227. Frankovich, T.A., Gaiser, E., Wachnicka, A., Zieman, J.C., 2006. Spatial and temporal distributions of epiphytic diatoms: relationships to salinity and nutrients in a subtropical ecosystem. Hydrobiologia 569, 259–271. Frankovich, T.A., Armitage, A.R., Wachnicka, A.H., Gaiser, E.E., Fourqurean, J.W., 2009. Nutrient effects on seagrass epiphyte community structure in Florida Bay. Journal of Phycology 45, 1010–1020. Gaiser, E.E., Wachnicka, A., Ruiz, P., Tobias, F.A., Ross, M.S., 2005. Diatom indicators of ecosystem change in coastal wetlands. In: Bortone, S. (Ed.), Estuarine Indicators. CRC Press, Boca Raton, FL, pp. 127–144. Gershunov, A., Barnett, T., 1998. Interdecadal modulation of ENSO teleconnections. Bulletin of the American Meteorological Society 79, 2715–2726.

91

Graves, G., Thompson, M., Schmitt, G., Fike, D., Kelly, C., Tyrrell, J., 2005. Using macroinvertebrates to document the effects of a storm water-induced nutrient gradient on a subtropical estuary. In: Bortone, S.A. (Ed.), Estuarine Indicators. CRC Press, Boca Raton, FL, pp. 333–349. Hallett, T.B., Coulson, T., Pilkington, J.G., Clutton-Brock, T.H., Pemberton, J.M., Grenfell, B.T., 2004. Why large-scale climate indices seem to predict ecological processes better than local weather. Nature 430, 71–75. Heegaard, E., 2003. Mixed Effect Age-depth Routine for R. Retrieved 8 November 2006 from http://www.uib.no/bot/qeprg/Age-depth.htm. Hoegh-Guldberg, O., Bruno, J.F., 2010. The impact of climate change on the world's marine ecosystems. Science 328, 1523–1528. IPCC, 2007. Climate Change 2007: The Physical Science Basis. Intergovernmental Panel on Climate Change, Cambridge University Press. Ishman, S.E., 1997. Ecosystem history of South Florida: Biscayne Bay sediment core descriptions. U.S. Geologic Survey Open-File Report 97-437. Kelly, K.A., 2004. Wind data: a promise in peril. Science 303, 962–963. Kelly, J.R., 2008. Nitrogen effects on coastal marine ecosystems, In: Hatfield, J.L., Follett, R.F. (Eds.), Nitrogen in the Environment: Sources, Problems, and Management, Second edition. Elsevier Inc., pp. 271–332. Kohout, F.A., Kolipinski, M.C., 1967. Biological zonation related to groundwater discharge along the shore of Biscayne Bay, Miami, Florida. Estuaries 83, 488–499. Langevin, C.D., 2001. Simulation of ground-water discharge to Biscayne Bay, Southeastern Florida. U.S. Geological Survey Water-Resources Investigations Report 00-4251, p. 127. Lee, T.N., 1975. Circulation and exchange processes in southeast Florida's coastal lagoons. Technical Report, 75-3. University of Miami, Miami, FL. Levitus, S., Antonov, J.I., Wang, J., Delworth, T.L., Dixon, K.W., Broccoli, A.J., 2001. Anthropogenic warming of earth's climate system. Science 292, 267–270. Li, Y., Zhang, M., 2002. Major problems affecting agriculture in Miami-Dade: natural resources and crop management (fertilizer). In: Degner, R.L., Stevens III, T.J., Morgan, K.L. (Eds.), Miami-Dade County Agricultural Land Retention Study: Final Report, Florida Department of Agricultural and Consumer Services Contract No. 5218. Florida Agricultural Market Research Center, Institute of Food and Agricultural Sciences, University of Florida, Gainesville. Lund, D.C., Curry, W., 2006. Florida current surface temperature and salinity variability during the last millennium. Paleoceanography 21. Maul, G.A., Martin, D.M., 1993. Sea level rise at Key West, Florida, 1846–1992; America's longest instrument record? Geophysical Research Letters 20 (18), 1955–1958. McCabe, G.J., Palecki, M.A., Betancourt, J.L., 2004. Pacific and Atlantic Ocean influences on multidecadal drought frequency in the United States. Proceedings of the National Academy of Sciences of the United States of America 101, 4136–4141. McCune, B., Grace, J.B., 2002. Analysis of Ecological Communities. MJM Software Design, Gleneden Beach, Oregon, U.S.A. McVoy, C.W., Said, W.P., Obeysekera, J., VanArman, J.A., Dreschel, T.W., 2011. Landscapes and Hydrology of the Predrainage Everglades. University Press of Florida, Gainesville, FL. Meeder, J., Boyer, J.N., 2001. Total ammonia concentrations in soil, sediments, surface water, and groundwater along the western shoreline of Biscayne Bay with the focus on Black Point and a reference mangrove site. Final Report to the National Park Service under NPS/FIU Cooperative Agreement No. CA5280-8-9038. Meeder, J.F., Alvord, J., Byrns, M., Ross, M.S., Renshaw, A., 1997. Distribution of benthic nearshore communities and their relationship to groundwater nutrient loading. Final Report to Biscayne National Park. SERP, FIU. Menge, B.A., Gouhier, T.C., Freidenburg, T., Lubchenco, J., 2011. Linking long-term, large-scale climatic and environmental variability to patterns of marine invertebrate recruitment: toward explaining unexplained variation. Journal of Experimental Marine Biology and Ecology 400, 236–249. MIAMI, 2012. http://www.historymiami.org. Munroe, R.M., Gilpin, V., 1930. The Commodore's Story. Ives Washburn, New York, p. 330. Najjar, R.G., Walker, H.A., Anderson, P.J., Barron, E.J., Bord, R.J., Gibson, J.R., Kennedy, V.S., Knight, C.G., Megonigal, J.P., O'Connor, R.E., Polsky, C.D., Psuty, N.P., Richards, B.A., Sorenson, L.G., Steele, E.M., Swanson, R.S., 2000. The potential impacts of climate change on the mid-Atlantic coastal region. Climate Research 14, 219–233. Nicholls, R.J., Wong, P.P., Burkett, V.R., Codignotto, J.O., Hay, J.E., McLean, R.F., Ragoonaden, S., Woodroffe, C.D., 2007. Coastal systems and low-lying areas. In: Parry, M.L., Canziani, O.F., Palutikof, J.P., van der Linden, P.J., Hanson, C.E. (Eds.), Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK, pp. 315–356. NOAA, 2012. http://www.esrl.noaa.gov/psd/data/climateindices/list/. Ottersen, G., Stenseth, N.C., Hurrell, J.H., 2004. Climatic fluctuations and marine systems: a general introduction to the ecological effects. In: Stenseth, N.C., Ottersen, G., Hurrell, J.H., Belgrano, A. (Eds.), Marine Ecosystems and Climate Variation. : The North Atlantic, A Comparative Perspective. Oxford University Press, Chippenham, pp. 3–14. Parker, G.G., Ferguson, G.E., Love, S.K., 1955. Water resources of southeastern Florida. U.S. Geol. Survey Water-Supply Paper, 1255, p. 965. Ralph, P.J., Tomasko, D., Moore, K., Seddon, S., Macinnis-Ng, C.M.O., 2006. Human impacts on seagrasses: eutrophication, sedimentation, and contamination. In: Larkum, A.W.D., Orth, R.J., Duarte, C.M. (Eds.), Seagrasses: Biology, Ecology and Conservation. Springer, the Netherlands, pp. 567–593. Reich, C., Halley, R.B., Hickey, T., Swarzenski, P., 2006. Groundwater characterization and assessment of contaminants in marine areas of Biscayne Bay National Park. Technical Report (NPS/NRWRD/NRTR-2006/356). Renken, R.A., Shapiro, A.M., Cunningham, K.J., Harvey, R.W., Metge, D.W., Zygnerski, M.R., Osborn, C.L., Wacker, M.A., Ryan, J.N., 2005. Assessing the vulnerability of a

92

A. Wachnicka et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 371 (2013) 80–92

municipal well field to contamination in a karst aquifer. Environmental and Engineering Geoscience 11, 341–354. Richey, J.N., Poore, R.Z., Flower, B.P., Quinn, T.M., Hollander, D.J., 2009. Regionally coherent Little Ice Age cooling in the Atlantic Warm Pool. Geophysical Research Letters 36, L21703. Robbins, J.S., Holmes, C.W., Halley, R., Bothner, M., Shinn, E., Graney, J., Keeler, G., ten Brink, M., Orlandini, K.A., Rudnick, D., 2000. Time-averaged fluxes of lead and fallout radionuclides to sediment of Florida Bay. Journal of Geophysical Research 105, 28805–28822. Rodionov, S., 2004. A sequential algorithm for testing climate regime shifts. Geophysical Research Letters 31, L09204. Rodionov, S.N., Overland, J.E., 2005. Application of a sequential regime shift detection method to the Bering Sea ecosystem. Journal of Marine Science 62, 328–332. Saunders, K.M., 2010. A diatom dataset and diatom–salinity inference model for southeast Australian estuaries and coastal lakes. Journal of Paleolimnology 4, 525–542. Saunders, K.M., Mcminn, A., Roberts, D., Hodgson, D.A., Heijnis, H., 2007. Recent humaninduced salinity changes in Ramsar-listed Orielton Lagoon, south-east Tasmania, Australia: a new approach for coastal lagoon conservation and management. Aquatic Conservation: Marine and Freshwater Ecosystems 17, 51–70. Schaffelke, B., Carleton, J., Skuza, M., Zagorskis, I., Furnas, M.J., 2011. Water Quality in the Inshore Great Barrier Reef Lagoon: Implications for Long-term Monitoring and Management. SERC, 2012. http://serc.fiu.edu/wqmnetwork/. SFWMD, 2012. http://www.sfwmd.gov/dbhydroplsql/show_dbkey_info.main_menu. Sklar, Fm, McVoy, C., VanZee, R., Gawlik, D.E., Tarboton, K., Rudnick, D., Miao, S., 2002. The effects of altered hydrology on the ecology of the Everglades. In: Porter, J.W., Porter, K.G. (Eds.), The Everglades, Florida Bay and Coral Reefs of the Florida Keys — An Ecosystem Sourcebook. CRC Press, Boca Raton, Florida, USA, pp. 39–82. Smith, V.H., Schindler, D.W., 2009. Eutrophication science: where do we go from here? Trends in Ecology & Evolution 24, 201–207. Stenseth, N.C., Mysterud, A., Ottersen, G., Hurrell, J.W., Chan, K.-S., Lima, M., 2002. Ecological effects of climate fluctuations. Science 297, 1292–1296. Stenseth, N.C., Ottersen, G., Hurrell, J.W., Mysterud, A., Lima, M., Chan, K.S., Yoccoz, N.G., Adlandsvik, B., 2003. Studying climate effects on ecology through the use of climate indices: the North Atlantic oscillation, El Niño southern oscillation and beyond. Proceedings of the Royal Society of London Series B 270, 2087–2096. Stone, J.R., Cronin, T.M., Brewster-Wingard, G.L., Ishman, S.E., Wardlaw, B.R., Holmes, C.W., 2000. A paleoecological reconstruction of the history of Featherbed Bank, Biscayne National Park, Biscayne Bay, Florida. USGS Open-File Report 00-191, p. 24. Stuiver, M., Reimer, P.J., 1993. Extended 14C data base and revised CALIB 3.0 14C age calibration program. Radiocarbon 35, 215–230. Swanson, K.L., Tsonis, A.A., 2009. Has the climate recently shifted? Geophysical Research Letters 36, L06711. Telford, R.J., Birks, H.J.B., 2009. Evaluation of transfer functions in spatially structured environments. Quaternary Science Reviews 28, 1309–1316. Tibby, J., Gell, P.A., Fluin, J., Sluiter, I.R.K., 2007. Diatom–salinity relationships in wetlands: assessing the influence of salinity variability on the development of inference models. Hydrobiologia 591, 207–218.

Tunberg, B., Nelson, W., 1998. Do climatic oscillations influence cyclical patterns of soft bottom macrobenthic communities on the Swedish west coast? Marine Ecology Progress Series 170, 85–94. U.S. Census, 2010. http://2010.census.gov/2010census/. Wachnicka, A., 2009. Quantitative diatom-based reconstruction of paleoenvironmental conditions in Florida Bay and Biscayne Bay, U.S.A. PhD dissertation, Florida International University, Miami, Florida, USA. http://etd.fiu.edu/ETD-db/available/etd-0506109-123854. Wachnicka, A., Gaiser, E., Collins, L., Frankovich, F., Boyer, J., 2010. Distribution of diatoms and development of diatom-based models for inferring salinity and nutrient concentrations in Florida Bay and adjacent coastal wetlands of South Florida (USA). Estuaries Coasts 33, 1080–1098. Wachnicka, A., Gaiser, E., Boyer, J., 2011a. Autecology and distribution of diatoms in Biscayne Bay, Florida: implications for bioassessment and paleoenvironmental studies. Ecological Indicators 11 (2), 622–632. Wachnicka, A., Collins, L., Gaiser, E., 2011b. Response of diatom assemblages to 130 years of environmental change in Florida Bay (U.S.A.). Journal of Paleolimnology (On line first: http://dx.doi.org/10.1007/s10933-011-9556-3). Wachnicka, A., Gaiser, E., Collins, L., 2011c. Correspondence of historic salinity fluctuations in Florida Bay, U.S.A., to atmospheric variability and anthropogenic changes. Journal of Paleolimnology (On line first: http://dx.doi.org/10.1007/s10933-011-9534-9). Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.M., Hoegh-Guldberg, O., Bairlein, F., 2002. Ecological responses to recent climate change. Nature 416, 389–395. Wang, J.D., Luo, J., Ault, J.S., 2003. Flows, salinity and some implications on larval transport in South Biscayne Bay, Florida. Bulletin of Marine Science 72 (3), 695–723. Wanless, H.R., 1976. Geological setting and recent sediments of the Biscayne Bay region. In: Thorhaug, A., Volker, A. (Eds.), Biscayne Bay: Past, Present and Future, Special Report, University of Miami Sea Grant, vol. 5, p. 32. Wanless, H.R., Tedesco, L.P., Risi, J.A., Bischof, B.G., Gelsanliter, S., 1995. the role of storm processes on the growth and evolution of coastal and shallow marine sedimentary environments in South Florida. Field Trip Guide, The 1st SEPM Congress on Sedimentary Geology, St. Petersburg, FL, USA. Wingard, G.L., Cronin, T.M., Dwyer, G.S., Ishman, S.E., Willard, D.A., Holmes, C.W., Bernhardt, C.E., Williams, C.P., Marot, M.E., Murray, J.B., Stamm, R.G., Murray, J.H., Budet, C., 2003. Ecosystem history of southern and central Biscayne Bay: summary report on sediment core analyses. U.S. Geological Survey Open File Report No. 03375. Wingard, G.L., Cronin, T.M., Holmes, C.W., Willard, D.A., Dwyer, G.S., Ishman, S.E., Orem, W., Williams, C.P., Albietz, J., Bernhardt, C.E., Budet, C., Landacre, B., Lerch, T., Marot, M.E., Ortiz, R., 2004. Ecosystem history of southern and central Biscayne Bay: summary report on sediment core analyses-year two. U.S. Geological Survey Open File Report No. 2004-1312. Wingard, G.L., Hudley, J.W., Holmes, C.W., Willard, D.A., Marot, M., 2007. Synthesis of age data and chronology for Florida Bay and Biscayne Bay cores collected for ecosystem history of South Florida's estuaries project. Open File Report 2007-1203. Zervas, C., 2001. Sea level variations of the United States 1854–1999. NOAA Technical Report NOS CO-OPS, 36 . (201 pp.).