SAV Communities of Western Biscayne Bay, Miami, Florida,USA: Human and Natural Drivers of Seagrass and MacroalgaeAbundance and Distribution Along a Continuous Shoreline

D. Lirman & T. Thyberg & R. Santos & S. Schopmeyer &

C. Drury & L. Collado-Vides & S. Bellmund & J. Serafy

Received: 14 March 2013 /Revised: 4 December 2013 /Accepted: 4 January 2014# Coastal and Estuarine Research Federation 2014

Abstract Nearshore benthic habitats of Biscayne Bay fit theprediction of communities at risk due to their location adjacentto a large metropolitan center (Miami) and being influencedby changes in hydrology through the activities of theComprehensive Everglades Restoration Plan (CERP). Weexamine whether the proposed programmatic expansion ofmesohaline salinities through the introduction of additionalfresh water would result in: (1) increases in seagrass cover; (2)expansion in the distribution and cover of Halodule; and (3) areduction in the dominance of Thalassia, as hypothesized byCERP. Seagrasses were present at 98 % of sites where theycovered 23 % of the bottom. Salinity was the only physicalvariable with a significant relationship to the occurrence of allSAV taxa. Occurrence of Thalassia, Halimeda, and Penicillusincreased significantly with increasing salinity, but Halodule,Syringodium, Laurencia, Udotea, Batophora, Caulerpa, andAcetabularia showed a significant negative relationship withsalinity. Mesohaline habitats had higher cover of seagrass andHalodule, and reduced dominance by Thalassia. Thus, weexpect increases in the extent of mesohaline habitats to

achieve the established CERP goals. We also examined thenutrient content of seagrass blades to evaluate whether: (1)nutrient availability is higher in areas close to canal dis-charges; and (2) tissue nutrient levels are related to seagrassabundance. The low abundance of Thalassia along the shore-line is not only due to its exclusion from low-salinity envi-ronments but also by higher nutrient availability that favorsHalodule. Percent N and P, and N:P ratios in seagrass tissuesuggest that Biscayne Bay receives high N inputs and is P-limited. Thus, increased P availability may facilitate an ex-pansion of Halodule. The data presented suggest that in-creasedmesohaline salinities will increase seagrass abundanceand support co-dominance by Halodule and Thalassia ashypothesized, but raise concerns that current high N availabil-ity and increases in P may prompt a shift away from seagrass-dominated to algal-dominated communities under scenariosof enhanced fresh water inputs.

Keywords SAV . Salinity . Nutrients . Evergladesrestoration . Biscayne Bay .Macroalgae

Introduction

Recent reviews of the global status of seagrass communitieshave highlighted significant declines in condition and extent,leading to declarations that these important coastal habitats are“at risk” (Short et al. 2011) or “in crisis” (Orth et al. 2006).The declines and vulnerability of seagrasses are especiallyevident in those habitats located adjacent to populated coast-lines exposed to eutrophication and other human impacts(Duarte 2002; Lotze et al. 2006; Short et al. 2006; Waycottet al. 2009). The submerged aquatic vegetation (SAV) com-munities of western Biscayne Bay (Florida, USA), whichinclude both seagrasses and macroalgae, would certainly fitthe prediction of communities at risk due to their location

Communicated by Nuria Marba

D. Lirman (*) : T. Thyberg : R. Santos : S. Schopmeyer :C. Drury : J. SerafyRosenstiel School ofMarine and Atmospheric Science, University ofMiami, 4600 Rickenbacker Cswy, Miami, FL 33149, USAe-mail: dlirman@rsmas.miami.edu

L. Collado-VidesDepartment of Biological Sciences, Florida International University,Miami, FL 33199, USA

S. BellmundBiscayne National Park, 9700 SW 328th St, Homestead,FL 33033, USA

J. SerafyNOAA/NMFS/SEFSC, 75 Virginia Beach Drive, Miami,FL 33149, USA

Estuaries and CoastsDOI 10.1007/s12237-014-9769-6

adjacent to Miami-Dade County and the city of Miami(population 2.5 million) and downstream of a FloridaEverglades system that has been significantly modified by alarge water management system in the past 50 years (Davisand Ogden 1994; Light and Dineen 1994; Steinman et al.2002). Moreover, the adjacency of this system to FloridaBay, an ecosystem influenced by similar human and naturaldrivers that underwent a major seagrass and sponge die-off inthe recent past (Robblee et al. 1991; Butler et al. 1995; Ziemanet al. 1999), raises concern over the status and fate of SAValong the littoral habitats of Biscayne Bay.

Seagrass habitats are essential to the ecology and economyof coastal communities in Florida and elsewhere (Costanzaet al. 1997; Orth et al. 2006). Healthy seagrass beds play a keyrole in maintaining water quality through sediment depositionand carbon and nutrient sequestration. Significant reductionsin seagrass biomass commonly prompt increases in turbiditythat can persist for prolonged periods (Boyer et al. 1999) andhinder recovery. Seagrass beds also provide essential habitatto endangered plants and animals. Biscayne Bay is home todepleted or endangered megafauna, which include species ofsea turtle, manatee, crocodile, dolphin, and several membersof the reef fish community such as groupers, snappers, andgrunts. One of the most important contributions of seagrasscommunities of Biscayne Bay to the local economy is theirrole as nursery habitat for recreational and commercial fisher-ies species (Ault et al. 1999a, b; Diaz 2001; Serafy et al. 1997,2003). These shallow (<2 m of depth) habitats also provideunique recreational opportunities to >5 million residents of SEFlorida that live within a short distance to the bay. Theseagrasses of Biscayne and other South Florida regions in-clude one of the largest expanses of seagrass communities inthe world (Fourqurean et al. 2002). Thus, the continued con-servation and enhanced restoration of these habitats is a localand regional priority.

In South Florida, conservation efforts have concentrated onrestoring the natural hydrology of the system that was modi-fied with the construction of the Central and Southern FloridaProject (CS&F) water-drainage system completed in the1960s (Browder and Ogden 1999; McIvor et al. 1994). Inaddition to reductions in the amount of fresh water reachingcoastal bays, the water management system reduced the pro-portion of flows derived from overland and ground watersources, directing the majority of the fresh water throughcanals that discharge directly into littoral environments.These discharge patterns have created environments that ex-hibit drastic reductions in salinity over short periods of time(Wang et al. 2003; Lirman et al. 2008a, b). Modifications inmean salinity and concentrated points of discharge have al-ready been associated with declines in seagrass abundance(Montague and Ley 1993; Zieman et al. 1999) and changes inspecies composition of seagrass communities (Herbert et al.2011). Designed in part to recover the natural and historical

hydrology of the Everglades and coastal lagoons of SouthFlorida, the Comprehensive Everglades Restoration Plan(CERP) includes specific goals to increase the amount of freshwater reaching Florida and Biscayne Bay, as well as to modifythe way the fresh water is delivered (Light and Dineen 1994;McIvor et al. 1994; Browder and Ogden 1999). Of specialconcern within the restoration framework are those nearshorehabitats that presently exhibit the widest fluctuations in salin-ity and where the impacts of restoration projects would beconcentrated.

Nearshore habitats of western Biscayne Bay became afocal point of monitoring starting in 2003. The long-termSAV monitoring program conducted by the State of Floridaand Miami-Dade County (Yarbro and Carlson Jr 2011), whileproviding excellent bay-wide information on status and trendsof SAV communities, did not include the habitats closest toshore due to the logistical constraints of accessing shallowenvironments. SAV surveys conducted prior to the presentstudy in nearshore western Biscayne Bay were limited inseasonal (only the wet season was examined in 2003) orspatial coverage (2003 and 2005 surveys only ranged fromRickenbacker Cswy. to Turkey Pt.) (Lirman et al. 2008a, b).Thus, the data and analyses included here represent a signif-icant expansion in both the period of record and the areasampled, as well as in the physical variables recorded (depth,light, salinity, DO, and seagrass tissue nutrients). This studyprovides the most comprehensive assessment of the status andtrends of SAV communities in western Biscayne Bay in thenearshore habitats most influenced by present and futurechanges in hydrology of the system through the activities ofthe CERP located just upstream of these environments (Lightand Dineen 1994).

In this study, co-sampled biological and physical parametersare used to delineate and characterize distinct SAV communitiesalong a continuous shoreline. Similar SAV community classi-fication approaches have been employed in Florida Bay wherefresh water inputs from the Everglades also delineate distinctphysical environments (Frankovich et al. 2011; Herbert et al.2011). Such baseline information is a crucial component of theadaptive management plan developed for the region, providingdata on seasonal and inter-annual trends and variability in SAVabundance and spatial distribution that can be used to ascertainimpacts of the natural and human drivers of the system. Thesedata are used to test hypotheses formulated by CERP and byresearchers in similar systems, namely that expansion ofmesohaline environments will: (1) increase seagrass cover; (2)expand the cover and distribution ofHalodule; and (3) decreasethe dominance of Thalassia (Fourqurean et al. 2003;RECOVER 2004, 2006; Herbert et al. 2011). In addition, wedocument nutrient availability for seagrasses in nearshore hab-itats (assessed as tissue nutrient concentrations) and test wheth-er: (1) nutrient availability is higher in areas close to canaldischarges; and (2) tissue nutrient levels are related to seagrass

Estuaries and Coasts

abundance. Finally, the period of record (2008–2011) includeda record-breaking cold snap (January 2010), allowing us toevaluate the impacts of this anomaly on seagrass abundancein western Biscayne Bay.

Methods

SAV Surveys

Seasonal surveys of nearshore (<500 m from shore) benthichabitats of Biscayne Bay were conducted in the dry(Jan–March) and wet (July–Sept) seasons (Fig. 1) using astratified random sampling design based on the US EPA’sEMAP sampling protocol (Jackson et al. 2000). Nearshorehabitats were divided into five, 100-m strata at increasingdistance from shore (<100, 100–200, 200–300, 30–400, and400–500 m from shore) (Lirman et al. 2008a, b). These stratawere further divided into cells of equal size and one surveypoint was generated within each subdivision at random. TheGPS coordinates for each point were exported into a GPS fornavigation in the field. At each site, non-overlapping digitalimages of the bottom were collected from the survey skiff at10-s intervals as the boat drifted along an approximately 25-msurvey track. These were analyzed to determine the percentcover for macroalgae and seagrass species. Also, a ThalassiaDominance Index was calculated for each site as the propor-tional cover of Thalassia (i.e. (Thalassia cover/Halodule cov-er)/Seagrass cover)). For each survey location, ten non-overlapping geo-tagged images were chosen at random fromthe image library and percent cover was estimated for eachbenthic category (Fourqurean et al. 2002). Cover was definedas the fraction of the total quadrat or frame that was obscuredby each taxon when viewed directly from above on a scalefrom 0 to 100 %. In addition, physical parameters(light (PAR), temperature, dissolved oxygen, salinity) wererecorded just below the water surface and at the bottom at eachsite. Light measurements just below the surface and at thebottom obtained with a 4-Π spherical quantum LI-COR sen-sor were used to calculate the extinction coefficient Kt (Kelbleet al. 2005). The number of sites surveyed was 431 in 2008,677 in 2009, 659 in 2010, and 756 in 2011 (sample effortincreased over time as project funding increased). The surveydomain encompassed 51 km2 (Fig. 1), representing an averageof 49 sites km−2, with an average distance between closestsites of 140 m.

Sites were classified using a Hierarchical Cluster Analysisusing the Average Distance Linkage method based on theaverage percent cover of not only seagrasses, but macroalgaeas well. For the classification of sites based on the abundanceof key taxa, macroalgae were divided into two groups previ-ously identified by Collado-Vides et al. (2011) as marine (e.g.,

Halimeda and Penicillus) or estuarine (e.g., Batophora,Laurencia, Polysiphonia, and Chara).

Seagrass Tissue Nutrients

Seagrass tissue nutrients were sampled in two distinct efforts.Tissue collections were completed at: (1) shoreline habitats(n = 72 sites; <50 m from shore) during July and August,2008; and (2) the 17 sites where water quality loggers aremaintained by Biscayne National Park during July andAugust, 2011. The shoreline sites were selected at randomfrom equally spaced shoreline segments. The 17 water-qualitysites were established by Biscayne National Park alonginshore-to-offshore transects to monitor water quality patternsin relation to CERP projects. Blade samples from eachseagrass species found at each site were processed followingmethods detailed by Collado-Vides et al. (2011) to determine% N and % P content. The nutrient data from the 2009shoreline surveys were used to test the hypothesis that freshwater entering the bay through canals that drain urban andagricultural upstream areas is a key source of nutrients to SAV.The % N and % P content of Thalassia and Halodule bladescollected from the shoreline habitats (<50 m from shore) weregrouped into canal (<1 km from the discharge site) and marine(>1 km from the canal discharge site) sites. The nutrient datacollected in 2011 from the inshore-to-offshore transects wereused to evaluate nutrient availability in relationship to land-based sources of fresh water and nutrients. A second objectiveof this collection was to evaluate whether the large buoys usedto mark the location of the water quality probes (YSI 6600series) serve as bird nesting stakes. Bird stakes are commonlyused as a seagrass restoration method to increase the input ofnutrients to the seagrass community from bird feces and priorresearch in Florida Bay has shown that the increased input of Pfrom bird feces can favor the growth of Halodule, a speciesknown to be able to rapidly acquire available nutrients (Powellet al. 1989, 1991). Thus, it was hypothesized that increasednutrient inputs at these sites would support the growth ofHalodule in offshore high-salinity environments wherehigh and stable salinity would normally favor the dom-inance of Thalassia (Fourqurean et al. 2003; Lirman andCropper 2003).

Nearshore sites do not have large buoys marking the loca-tion of the stations (these shallow sites are marked instead usingsmall styrofoam buoys that do not allow bird nesting) and thusprovide a control for the presence of large buoys that common-ly serve as bird stakes. At each of the water quality stations,seagrass blades were collected haphazardly from a radius of5 m around the buoys. Stations were grouped for analysis asnearshore (n= 7, small buoys, depth = 0.6 m, mean distance toshore = 160 m), mid (n = 4, large buoys, depth = 1.9 m, meandistance to shore = 2,900 m), and offshore (n = 7, large buoys,depth = 1.9 m, mean distance to shore = 3,400 m). Data

Estuaries and Coasts

collected in 2008 and 2011 were analyzed independently andwere not compared to each other. It is important to note that weuse here tissue nutrient content as a proxy for total nutrientavailability and do not aim to evaluate the source (e.g., watercolumn and sediments) of such nutrients, which is beyond thescope of this study.

Results

Percent Seagrass Cover: Spatial and Temporal Trends

The period of record in this study spanned eight consecutivedry and wet seasons between 2008 and 2011 (Fig. 2). Themean percent cover of the three seagrass species over theperiod of record was 22.8 % (SD = ±18.7). Mean seagrasscover for all years and strata combined was 18.4 % (15.9) inthe dry season and increased significantly in the wet season to27.8 % (20.3; t test, p < 0.01). For both Thalassia (20.1 vs.13.2 %) and Halodule (6.6 vs. 4.4 %), cover was significantly

higher in the warmer wet season than in the cooler dry season(all years combined, ANOVA, p < 0.05); no seasonal patternwas evident for Syringodium cover (0.8 vs. 1.0 %). When thesurvey domain was divided into inshore (<100 m) and off-shore (100–500m from shore) strata, significant differences inmean cover were found for all three species, with Halodulehaving higher cover inshore and Thalassia and Syringodiumhaving higher cover offshore (all seasons and years combined,t tests, p < 0.05 for each species). Finally, over the period ofrecord, Thalassia showed a significant increase over time(linear regression, p< 0.05), Syringodium showed a significantdecrease (p< 0.05), butHaloduledid not show any significanttrends in cover (p > 0.05).

No major physical impacts due to hurricanes or tropicalstorms were recorded during the study period, but a record-breaking winter cold-snap took place in Jan 2010 (Lirmanet al. 2011). During this time, seawater temperature reached6.5 °C in the shallow nearshore environments of westernBiscayne Bay. While this cold-water anomaly took place justbefore the 2010 dry-season SAV surveys, only limited impacts

Fig. 1 Map of study area and the location of survey sites. While each site may contain more than one species, the labels refer to the dominant taxa(seagrasses andmacroalgae) as identified in aHierarchical Cluster Analysis of data collected from nearshore habitats of western Biscayne Bay in 2008–2011

Estuaries and Coasts

were documented on seagrass cover. In fact, percent covervalues for Syringodium and Thalassia in the 2010 dry seasonwere higher than those recorded in preceding dry seasons andThalassia increased to its highest levels in the 2010 wetseason. The only direct impact of this disturbance was thedepression of the 2010 wet-season cover of Halodule (i.e.,lack of recovery to wet-season highs) in nearshore environ-ments that experienced the most drastic temperature declines.Data from 2011 show an increasing trend inHalodulecover innearshore habitats after this temporary depression (Fig. 2).

SAV Community Classification

The results of a Hierarchical Cluster Analysis revealed threemain clusters labeled here based on the dominant taxa: (1)Thalassia/marine algae, (2) Halodule/estuarine algae, and (3)

Syringodium (Fig. 1). The Syringodium-dominated communitywas only observed at 1 % of sites, followed by the Halodule-dominated community found at 22 % of sites, and, finally, bythe Thalassia-dominated community found at 77 % of sites.Sites dominated byHalodulewhere characterized by the lowestand most variable salinity values as well as the highest temper-ature values compared to the other two SAV community types.In contrast, Thalassia dominated communities were found indeeper habitats further from shore, and with higher, less vari-able salinity (Table 1). Differences in biotic and abiotic vari-ables were significant for all parameters among the three clas-ses established (ANOVA, p < 0.05). Halodule-dominatedhabitats had significantly lower depth, salinity, and dis-tance to shore, and significantly higher temperature,DO, and Kt compared to Thalassia-dominated habitats(Table 1).

In addition to differences in abiotic conditions, dis-tinct spatial patterns were observed for the three groups.Syringodium-dominated community sites had a very re-stricted spatial distribution, being limited to only thenorthernmost area of the sampling domain (i.e., N ofShoal Point; Fig. 1). Thalassia-dominated sites werefound throughout the study region. Halodule-dominatedsites had high-abundance foci in areas closer to shoreand exposed to the inflow of fresh water from man-made canals (i.e., S of Black Point) and potentialsources of nutrients from urban developments, marinas,and golf-courses (i.e., S of Shoal Point; Fig. 1).

Thalassia Halodule Syringodium

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Fig. 2 Seasonal and interannual patterns of mean percent cover for thestudy region. aAll sites combined, b inshore sites (<100 m from shore), coffshore sites (100–500 m from shore)

Table 1 The three SAV community types identified in a HierarchicalCluster Analysis of data collected in nearshore habitats of westernBiscayne Bay in 2008–2011

Clusters “Halodule” “Thalassia” “Syringodium”

% of sites 22 77 1

Distance to shore (m) 222.1 (148.2) 262.4 (137.8) 264.3 (94.9)

Thalassia cover 6.2 (7.8) 19.8 (15.8) 14.2 (13.6)

Syringodium cover 0.1 (0.7) 0.7 (2.7) 39.4 (15.4)

Halodule cover 13.9 (14.5) 1.3 (3.4) 0.4 (1.2)

Marine algae cover 0.4 (0.7) 1.2 (2.1) 0.2 (0.6)

Estuarine algae cover 13.6 (14.3) 2.3 (2.7) 1.1 (2.4)

Depth (m) 0.9 (0.4) 1.2 (0.5) 0.7 (0.3)

Temperature (°C) 28.2 (3.7) 27.5 (3.2) 26.5 (4.2)

Salinity 27.7 (6.2) 30.8 (5.3) 30.6 (2.1)

CV salinity 0.22 0.17 0.06

DO (mg/l) 7.0 (2.1) 6.6 (1.5) 5.9 (1.6)

Extinction Coeff (Kt) 0.7 (0.5) 0.6 (0.4) 0.6 (0.2)

The locations of the sites classified by cluster are found in Fig. 1.Significant differences (ANOVA, p<0.05) in biotic and abiotic variableswere detected among the three distinct clusters. Distance to shore wasestimated as the linear distance between the site coordinate and the closestpoint along the shoreline for all sites located within the sampling domain(<500 from shore)

Estuaries and Coasts

Physical-Biological Linkages

Taking into consideration the importance placed on salinity asa determinant of SAV community composition and abundancewithin the context of CERP (Fourqurean et al. 2003), thebenthic data collected in 2008–2011 were analyzed furtherto elucidate relationships between salinity and the probabilityof occurrence and abundance of seagrass and macroalgaespecies in the study region.

Seagrasses were present at 98 % of sites. The few locationsdevoid of seagrass were deeper sites (>1.9 m) with higher,stable salinity (Table 2). Both the mean and maximum coverof seagrasses showed marked relationships with salinity.Thalassia was absent from sites where salinity was <10 andreached maximum levels (>80 % cover) in sites with salinitybetween 25 and 30 (Fig. 3a, b). Syringodiumwas only foundin sites with salinity between 20 and 40, and reached highabundance (~70% cover) in sites with salinity between 25 and30 (the same salinity bin that yielded the highest cover ofThalassia). Finally, Halodule had the widest salinity distri-bution (based on presence–absence data), being found at allsalinity ranges, but reaching maximum levels (>70 % cov-er) at sites with salinity <10. The average salinity of siteswhere each seagrass species was absent (0 % cover) was32.4 (SD = ± 5.0) for Halodule, 30.0 (5.8) for Syringodium,and 23.8 (6.6) for Thalassia. In addition to low meansalinity, salinity variability (expressed as the coefficient ofvariation, CV), appears to favor Halodule as sites whereonly this species is found had the highest CV of all habitatssurveyed (Table 2). No clear directional relationships wereobserved between DO and light penetration (Kt) andseagrass presence or cover.

Based on the frequency of observation of Thalassia andHalodule, these two species were found to co-occur at allsalinities >10 (Thalassia is not observed in salinity <10).However, the salinity range in which both species had similarfrequency of occurrence was 15–25. Halodule dominates inhabitats <15, while Thalassia dominates in habitats>25 (Fig. 3). The mean abundance of each species was calcu-lated in sites where they are found as a single species as well as

in sites where they co-occur with one or two other species(Table 2). While Halodule reached higher cover when foundalone compared to sites where found with Thalassia,Thalassia had similar abundance when in co-occurrence withHalodule (Table 2). While these patterns do not provide adirect test of the impacts of resource competition on abun-dance, they do suggest the competitive advantage of Thalassiaover Halodulewhen both species are present.

To test the CERP hypotheses for seagrasses, survey siteswere further classified into the following salinity classes:mesohaline (<18), polyhaline (18–30), euhaline (30–40), andhyperhaline (>40). Only four sites showed oligohaline (<5)salinities, so these sites were grouped under the mesohalineclass. The cover ofHalodule, Thalassia, all seagrasses, and theThalassia Dominance Index were compared among classesusing a Kruskal–Wallis test followed by Steel–Dwassmultiplecomparison tests. The cover of Thalassia was significantlylower (p < 0.05) and the cover of Halodule was significantlyhigher (p < 0.05) in mesohaline habitats compared to all otherhabitats. The cover of all seagrasses combined was signifi-cantly higher in mesohaline habitats compared to all otherhabitats. Moreover, the ThalassiaDominance Index increasedsignificantly with increasing salinity, with the lowest levelsrecorded in mesohaline habitats (p < 0.05, Fig. 4).

Relationships between SAV taxa and physical variableswere further explored using logistic regression where pres-ence–absence data for seagrasses and macroalgae (Laurencia,Halimeda, Penicillus, Udotea, Batophora, Caulerpa, andAcetabularia) were regressed against salinity, temperature,depth, DO, and Kt recorded at the same time as the SAVsurveys. Salinity was the only variable that showed a signif-icant relationship to the occurrence of all the SAV speciestested (Table 3). While the likelihood of finding Thalassia,Halimeda, and Penicillus increased significantly with increas-ing salinity, all other taxa showed a significant negative rela-tionship with salinity. Temperature showed a significant rela-tionship to SAV occurrence for eight of the ten species eval-uated (all except Thalassia and Halodule). Batophora andAcetabularia showed positive relationships to temperature,but all other taxa had lower likelihood of occurrence with

Table 2 Average seagrass cover and physical parameters (±SD) for sites surveyed in western Biscayne Bay 2008–2011

Species % sites Tt cover(%)

Hw cover(%)

Sf cover(%)

Depth(m)

Temp(ºC)

Sal CVsal

Minsal

Maxsal

DO(mg/l)

Kt

No seagrass 2.0 0 0 0 1.9 (0.4) 28.4 (1.9) 37.2 (3.6) 9.6 28.6 40.5 5.6 (0.5) 0.5 (0.2)

All 3 species 5.8 27.0 (15.2) 3.9 (6.0) 5.0 (6.4) 1.2 (0.5) 26.0 (2.2) 29.6 (3.0) 10.4 23.2 39.1 6.5 (1.2) 0.7 (0.5)

Syringodium only *1 site* 0 0 74.3 1.8 31.4 28.3 – 28.3 28.3 4.4 0.5

Halodule only 5.2 0 19.7 (14.2) 0 0.6 (0.3) 27.9 (4.3) 23.7 (6.6) 28.0 4.8 34.6 7.8 (2.8) 0.9 (0.7)

Thalassia only 40.1 16.8 (13.0) 0 0 1.2 (0.5) 27.8 (3.3) 32.6 (5.2) 16.1 13.3 42.3 6.4 (1.4) 0.5 (0.4)

Thalassia and Halodule 39.8 17.4 (15.0) 6.1 (9.6) 0 1.0 (0.4) 27.5 (3.2) 28.1 (4.7) 17.2 10.9 41.6 6.8 (1.6) 0.7 (0.4)

Estuaries and Coasts

increasing temperature. Depth was related significantly to onlyfour species, DO to one species, and Kt to three species(Table 3). While sediment depth was not recorded in oursurveys, it is apparent that sediments availability did not limitthe occurrence of seagrasses as these were found at 98 % ofsites. Nevertheless, sediment depth may still influence seagrassbiomass and will have to be incorporated into future studies.

Seagrass Tissue Nutrients

While variable spatially, high % N and N:P ratios well abovethe 30:1 Redfield ratio indicate high N availability and P

limitation (Atkinson and Smith 1983). When the % N and %P tissue content of seagrass blades were related to the abun-dance of the seagrass within the shoreline stratum (<50 mfrom shore), a significant positive relationship was only foundbetween % P and the cover ofHalodule (linear regression, p<0.05). No significant differences in the % N and % P contentwere found based on proximity to fresh water canals for eitherseagrass species along the shoreline (t test, p > 0.1).

Thalassia tissue showed a decreasing trend in % Nwith increasing distance from shore, with significantlyhigher % N in nearshore habitats compared to mid andoffshore sites (Kruskal–Wallis test, p < 0.05). A similar

Thalassia Syringodium Halodule

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Fig. 4 Mean cover of seagrasses in western Biscayne Bay based onsalinity habitats. The panel on the right shows the mean value of theThalassiaDominance Index ((Thal cover/Halo cover)/seagrass cover) for

the different salinity habitats. Barswith different capital letters are signif-icantly different from each other based on the results of a Kruskal–Wallistest followed by Steel–Dwass multiple comparison tests (p<0.05)

Estuaries and Coasts

(but non-significant) trend of decreasing % P with in-creasing distance from shore was also observed forThalassia. Halodule showed highest levels of both %N (non-significant) and % P (significant) at midshoresites where birds commonly perched (Table 4; Fig. 5). Plimitation (as reflected in the N:P ratio) increased withincreas ing dis tance f rom shore for Thalass ia(non-significant) from 81.9 nearshore to 89.9 offshore,but decreased significantly for Halodule, which had thehighest value of N:P (80.2) within inshore habitatscompared to mid (65.5) and offshore habitats (68.4;Table 4, Fig. 5).

Discussion

Seagrasses are the dominant type of benthic macrophyte innearshore Biscayne Bay, found at 98 % of sites where, onaverage, they covered 23 % (SD = ±18.7) of the bottom. Thesites closest to shore (<100 m from shore) were co-dominatedby Thalassia and Halodule, while the sites further offshoreshowed dominance by Thalassia only. Sites dominated byHalodule and estuarine algae (Batophora, Laurencia, andPolysiphonia) had lower and more variable salinity comparedto sites dominated by Thalassia and marine macroalgae(Halimeda and Penicillus) that had higher and more stablesalinity. These patterns are in agreement with previous exper-iments, field reports, and modeling exercises that showedHalodule-dominated communities in habitats with low andvariable salinity and increased nutrient availability, andThalassia-dominated communities in habitats with stable sa-linity and reduced nutrient availability (Zieman et al. 1989;Quammen and Onuf 1993; Fourqurean et al. 2003;Lirman and Cropper 2003; Collado-Vides et al. 2011;Herbert et al. 2011).

Large seasonal changes in percent cover were documented,with wet-season cover increasing 50 % over that recorded inthe dry season for Thalassia and Halodule, and 30 % forSyringodium. Increases in seagrass productivity and biomassduring the warmer wet season in Florida were describedpreviously by Fourqurean et al. (2001) and Lirman et al.(2008b). Over the period of record (2008–2011), Thalassiashowed an increasing trend, Syringodium showed a decreas-ing trend, andHalodule remained at consistent abundance. Nosignificant impacts of the Jan 2010 extreme cold-water anom-aly were recorded, with the exception of the lack of a seasonalincrease in Halodule cover in the summer following the dis-turbance in the shallowest shoreline habitats.

Salinity, the physical factor identified as the key indicatorfor assessing the performance of the engineering projectsassociated with the Comprehensive Everglades RestorationPlan (designed to increase and improve the method of deliveryof fresh water into coastal habitats), was the only variable thatshowed a significant relationship with the occurrence of all theseagrass and macroalgae species encountered, stronglysupporting its selection as a key indicator of restoration suc-cess in Biscayne Bay. While salinity is clearly not the onlyvariable influencing SAVabundance and distribution, it is thefactor that is most easily manipulated through managementdecisions (Fourqurean et al. 2003). The restoration targets forBiscayne Bay include the spatial expansion of mesohalinesalinities, an overall increase in seagrass cover, as well as theexpansion in the cover of Halodule and a reduction in thedominance of Thalassia (RECOVER 2004, 2006). As hypoth-esized, mesohaline habitats of Biscayne Bay have significant-ly higher cover of Halodule and all seagrass species com-bined, as well as significantly lower Thalassia dominance.

Table 3 Results from a logistic regression analysis of SAV presence/absence data in relation to physical parameters measured at the time ofSAV sampling in western Biscayne Bay from 2008–2011

Salinity Temp Depth DO Kt ChiSq R2

Thalassia P ns ns N N <0.01 0.09

Halodule N ns N ns P <0.01 0.28

Syringodium N N P ns ns <0.01 0.05

Laurencia N N ns ns ns <0.01 0.08

Halimeda P N ns ns ns <0.01 0.08

Penicillus P N ns ns N <0.01 0.04

Batophora N P N ns ns <0.01 0.21

Caulerpa N N P ns ns <0.01 0.1

Acetabularia N P ns ns ns <0.01 0.03

Udotea N N ns ns ns <0.01 0.08

n 2,523 sites

P positive relation (p<0.05), N negative relation (p<0.05), ns no signifi-cant relation (p>0.05)

Table 4 Tissue nutrient content of seagrasses fromwestern Biscayne Bay

Shoreline Nearshore Mid Offshore

n sites 71 7 4 6

Depth (m) 0.7 (0.1) 0.6 1.9 1.9

Dist to shore (m) 25 160 2,900 3,400

Sal 27.1 (2.8) 24.4 (3.0) 29.5 (2.3) 32.9 (2.2)

Tt % cover 11.7 (10.7) 11.3 (12.2) 22.1 (23.0) 19.8 (9.2)

Tt % N 2.10 (0.27) 2.60 (0.18) 2.26 (0.10) 2.26 (0.17)

Tt % P 0.11 (0.20) 0.07 (0.01) 0.06 (0.01) 0.06 (0.02)

Tt N:P 62.8 (20.1) 81.9 (12.5) 83.2 (17.6) 89.9 (31.7)

Hw % cover 10.9 (12.2) 26.8 (17.6) 1.9 (3.7) 1.5 (2.8)

Hw % N 2.06 (0.29) 2.46 (0.15) 2.51 (0.04) 2.30 (0.40)

Hw % P 0.10 (0.15) 0.07 (0.03) 0.09 (0.02) 0.08 (0.01)

Hw N:P 56.1 (12.7) 80.2 (10.2) 65.5 (12.6) 68.4 (11.6)

Shoreline data were collected in 2008. Nearshore, Mid, and Offshore datawere collected in 2011. Data from each survey were analyzed separately

Tt Thalassia testudinum, Hw Halodule wrightii

Estuaries and Coasts

The co-existence of both species at high abundance is pres-ently achieved in habitats with a mean salinity between 15 and25; conditions only encountered in the vicinity of canal-discharge areas. Interestingly, the reverse pattern (i.e., de-crease in seagrass productivity and diversity) has taken placein the EbroDelta in Spain where salinity has been decreased incoastal lagoons over the past 150 years due to rice cultivation,resulting in an over-dominance of Ruppia and a displacementof Zostera (Prado et al. 2012). Thus, based on the observedseagrass community composition and cover patterns, we ex-pect increases in the extent of mesohaline habitats to achievethe established CERP goals.

Spatial patterns in tissue nutrient content yielded importantinformation on nutrient availability and effects on seagrassdistribution. Percent N and P as well as N:P ratios suggest thatnearshore habitats of Biscayne Bay receive high N inputs andare largely P-limited as indicated by average % N valuesabove the 1.8 % suggested for N limitation by Duarte (1990)and N:P ratios higher than the 30:1 ratio suggested for Plimitation by Atkinson and Smith (1983). Phosphorus limita-tion and high N availability have been reported for bothFlorida Bay and Biscayne Bay in the past (Fourqurean et al.1992; Collado-Vides et al. 2011). Nutrient availability, esti-mated as the percent N and P in seagrass tissue, did not show

clear spatial patterns among shoreline sites, indicating thatfresh water from canals is not the only source of nutrients,and that ground water and overland flows also need to beconsidered when predicting and managing nutrient inputsfrom the Everglades into coastal bays (Briceño et al. 2011).The data presented here raise concern for increases in Pavailability. While an initial benefit of increased P availabilitymay be an expansion in the spatial extent and biomass ofHalodule (the seagrass species that showed a direct relation-ship between % P and cover), further increases may result insignificant shifts from seagrass dominated to algal-dominatedcommunities (Lapointe et al. 1994, 2002) in a system that hasthus far escaped the ecological crisis recorded in Florida Baywhere significant mortality of both seagrasses and spongeswere observed (Durako 1994; Butler et al. 1995; Durakoet al. 2002).

Competition for resources, especially nutrients, has beencommonly cited as a key factor determining the success of oneseagrass species over another (assuming all other limitingfactors such as light and salinity allow for co-existence)(Fong and Harwell 1994; Fong et al. 1997). As expected dueto the carbonate sediments of Biscayne Bay (Short 1987),seagrasses here are P-limited. Higher P availability was doc-umented along the shoreline, adjacent to mangrove habitats

Thalassia testudium Halodule wrightii

Nearshore

% N

% P

N:P

ns

ns

ns

A

B B

A

B B

A

BB

Mid Offshore Nearshore Mid Offshore

Fig. 5 Box-and-whisker plotsshowing nutrient tissue content as% N and% P (of total dry weight)and N:P ratio from seagrasssamples collected at differentdistances from shore in 2011. Themid and offshore sites are markedby large buoys that serve as birdnests and thus experience nutrientenrichment through bird feces.The horizontal barswithin theboxes represent the median, theupper, and lower boundariesrepresent the lower and upperquartiles, and the whiskersrepresent the extreme values.Circles represent outliers. ns non-significant trend. Barswithdifferent capital letters aresignificantly different from eachother based on the results of aKruskal–Wallis test followed bySteel–Dwass multiplecomparison tests (p<0.05)

Estuaries and Coasts

and sources of fresh water (N:P = 53–63), as also documentedby Rudnick et al. (1999) in Florida Bay. P availability de-creased with increasing distance from shore (N:P = 53–63along shoreline habitats <50 m from shore compared to80–82 at 160 m from shore), but increased further offshorein those sites where bird nesting provided additional nutrientinputs (N:P = 65–68 in Halodule tissue in sites with birdnesting). The replacement of Thalassia by Halodule in high-P environments as those created offshore by the addition ofbird feces has been reported by Powell et al. (1989, 1991) andHerbert and Fourqurean (2008). Thus, the potential forHalodule to extend beyond nearshore habitats under scenarioswhere nutrient availability increases may expand the distribu-tion of Halodule beyond its optimal salinity “climate” inBiscayne Bay.

It is important to note that relationships between SAV coverand distribution and abiotic parameters were evaluated usingphysical data collected concurrently with the biological sam-pling. This approach, which provides a large number of pairedobservations, has been used successfully to explore linkagesbetween biotic and abiotic variables for macroalgae (e.g.,Collado-Vides et al. 2011), seagrasses (e.g., Fourqureanet al. 2003), and corals (e.g., Wagner et al. 2010), but it doesnot take into account the role that antecedent conditions,stochastic events, and temporal variability in physical param-eters can have on SAVabundance and distribution. An exam-ple of the problems raised by using spot measurements ofphysical variables that fluctuate significantly at diurnal andseasonal scales to explain species distributions is provided bythe lack of relationships between the occurrence of SAV taxaand dissolved oxygen shown here. The lack of significantrelationships with this factor is likely due to the fact that allmeasurements were taken during the daytime when photosyn-thesis results in oxygen hypersaturation in vegetated areas(Borum et al. 2005). If oxygen levels were measured pre-dawn when critically low levels of oxygen are often recordedin seagrass beds, different patterns would have likelyemerged. Thus, it is important that future studies incorporatemore dynamic physical records obtained at the sites wherebiotic parameters are sampled. The nearshore habitats ofBiscayne Bay are presently part of a water quality programthat includes in situ instruments recording physical variables,including salinity, at 15-min intervals. These data will beavailable for future studies to improve both the explanatoryand forecasting capabilities of our research. While it is truethat our point samples revealed significant differences be-tween habitats that relate to species distributions, the differ-ences among habitats were small enough (i.e., 3 and 2 ºC) toraise concerns about their ecological significance. The avail-ability of dynamic physical data will allow for a betterunderstanding of the role of daily, seasonal, and inter-annual variability in physical factors on SAV abundanceand distribution.

The evidence presented here suggests that the low abun-dance of Thalassia along the shoreline is not only due tohigher nutrient availability, but also due to the exclusion ofThalassia by the physiological impacts of low salinity. Thus,as modeled by Fong et al. (1997), Fourqurean et al. (2003),Lirman and Cropper (2003), Herbert et al. (2011), and Santosand Lirman (2012), further decreases in salinity would signif-icantly decrease the spatial coverage of Thalassia while in-creasing the suitable habitat for Halodule, as incorporatedexplicitly into CERP targets for Biscayne Bay (RECOVER2004, 2006).

Western Biscayne Bay provides excellent nearshore habitatfor seagrasses, with seagrasses present at 98 % of sites sur-veyed. However, overall cover is <25 %, suggesting room forimprovement in seagrass biomass through water managementpractices as hypothesized. Mean seagrass cover estimates innearshore Biscayne Bay are lower than those recorded inFlorida Bay (Fourqurean et al. 2002) and the Indian RiverLagoon in Florida (Steward et al. 2006); Kee’s Bayou in theNorth Central Gulf of Mexico (Stutes et al. 2007); and theLaguna Madre in Texas (Kopecky and Dunton 2006). Thecombined cover of Thalassia andHalodulewhen both speciesare present (23 %) is higher than the cover when only one ofthe species is present (17.4 % for Thalassia and 19.7 % forHalodule). Thus, it appears that creating salinity climates thatare conducive to the co-occurrence of both species is one wayto achieve the goal of increased seagrass cover as proposed(RECOVER 2004, 2006). Such environments are restrictedpresently to areas along the shoreline where canals dischargefresh water. An increase in the amount of fresh water willclearly expand the area suitable for Halodule–Thalassia coex-istence as shown by the habitat suitability model described bySantos and Lirman (2012). Similarly, a modification in thedelivery system from point sources of dischargemainly duringthe wet season to a more consistent overland flow would alsoexpand the spatial habitat suitable for co-existence, and in-crease abundance of seagrass-associated fish, reported to behigher in mixed beds (Chester and Thayer 1990).

While the focus of ecological restoration is presently onseagrasses as ecological engineers, the findings of this studyas well as those in Kendrick et al. (1990), Biber et al. (2004),and Collado-Vides et al. (2011) highlight the influence ofsalinity and nutrients on macroalgal abundance and distribu-tion. Macroalgae are important components of SAV commu-nities in Biscayne Bay, often exceeding the cover ofseagrasses (Lirman et al. 2008a, b). Based on the key role thatmacroalgae can play as habitat for fish and invertebrates, it isimportant to consider restoration impacts on these taxa(Holmquist 1994, 1997) and include both marine (potentiallosers) and estuarine (potential winners) taxa in future habitatsuitability studies.

Large-scale engineering projects are currently being imple-mented in western Biscayne Bay as part of the Biscayne Bay

Estuaries and Coasts

Coastal Wetlands Project (BBCW). The goal of these projectsis to build a spreader system that would distribute the freshwater that typically flows straight into the Bay more evenlyinto coastal wetlands, thus replacing canal discharges withoverland flows more similar to historical conditions(Browder and Ogden 1999; McIvor et al. 1994). While it stillremains to be determined whether additional fresh water canbe diverted into Biscayne Bay to achieve the stated restorationgoals, a system of culverts and spreaders has been built toimprove the delivery of fresh water into nearshore habitats.The data presented here suggest that an expansion in habitatswith mesohaline salinity will increase seagrass abundance andsupport co-dominance by Halodule and Thalassia but raiseconcern over the high N availability and the potential forincreases in P inputs to prompt a shift away from seagrass-dominated to microalgal-dominated communities. Continuedmonitoring of nearshore environments before, during, andafter implementation of these large-scale experiments willreveal whether these projects have indeed produced theintended impacts on seagrass communities of westernBiscayne Bay.

Acknowledgments We are indebted to our collaborators G. DeAngelo,J. Browder, C. Hill, B. Huntington, J. Herlan, N. Formel, T. Jackson, andG. Liehr for their help in the field and the lab. This research wasconducted under permit BISC-2011-SCI-0028. Funding was providedby the Army Corps of Engineers, the US Department of the Interior’sCritical Ecosystem Studies Initiative, and the RECOVERMonitoring andAssessment Program (MAP). We thank the anonymous reviewers of thisstudy as well as Dr. Marba for their insightful suggestions.

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