Forecasting Responses of Seagrass Distributions to Changing Water Quality Using Monitoring Data

Extensive data sets on water quality and seagrass distributions in Florida Bay have been assembled under complementary, but independent, monitoring programs. This paper presents the landscape-scale results from these monitoring programs and outlines a method for exploring the relationships between two such data sets. Seagrass species occurrence and abundance data were used to define eight benthic habitat classes from 677 sampling locations in Florida Bay. Water quality data from 28 monitoring stations spread across the Bay were used to construct a discriminant function model that assigned a probability of a given benthic habitat class occurring for a given combination of water quality variables. Mean salinity, salinity variability, the amount of light reaching the benthos, sediment depth, and mean nutrient concentrations were important predictor variables in the discriminant function model. Using a cross-validated classification scheme, this discriminant function identified the most likely benthic habitat type as the actual habitat type in most cases. The model predicted that the distribution of benthic habitat types in Florida Bay would likely change if water quality and water delivery were changed by human engineering of freshwater discharge from the Everglades. Specifically, an increase in the seasonal delivery of freshwater to Florida Bay should cause an expansion of seagrass beds dominated by Ruppia maritima and Halodule wrightii at the expense of the Thalassia testudinum-dominated community that now occurs in northeast Florida Bay. These statistical techniques should prove useful for predicting landscape-scale changes in community composition in diverse systems where communities are in quasi-equilibrium with environmental drivers.

Responses of seagrass communities to fertilization along a gradient of relative availability of nitrogen and phosphorus in a carbonate environment

Patterns of relative nutrient availability in south Florida suggest spatial differences regarding the importance of nitrogen (N) and phosphorus (P) to benthic primary producers. We did a 14-month in situ fertilization experiment to test predictions of N and P limitation in the subtropical nearshore marine waters of the upper Florida Keys. Six sites were divided into two groups (nearshore, offshore) representing the endpoints of an N: P stoichiometric gradient. Twenty-four plots were established at each site with six replicates of each treatment (1N, 1P, 1N1P, control), for a total of 144 experimental plots. The responses of benthic communities to N and P enrichment varied appreciably between nearshore and offshore habitats. Offshore seagrass beds were strongly limited by nitrogen, and nearshore beds were affected by nitrogen and phosphorus. Nutrient addition at offshore sites increased the length and aboveground standing crop of the two seagrasses, Thalassia testudinum and Syringodium filiforme, and growth rates of T. testudinum. Nutrient addition at nearshore sites increased the relative abundance of macroalgae, epiphytes, and sediment microalgae. N limitation of seagrass in this carbonate system was clearly demonstrated. However, added phosphorus was retained in the system more effectively than N, suggesting that phosphorus might have important long-term effects on these benthic communities. The observed species-specific responses to nutrient enrichment underscores the need to monitor all primary producers when addressing questions of nutrient limitation and eutrophication in seagrass communities.

Ecosystem Structure and Function Still Altered Two Decades After Short-Term Fertilization of a Seagrass Meadow

An oligotrophic phosphorus (P) limited seagrass ecosystem in Florida Bay was experimentally fertilized in a unique way. Perches were installed to encourage seabirds to roost and deliver an external source of nutrients via defecation. Two treatments were examined: (1) a chronic 23-year fertilization and (2) an earlier 28-month fertilization that was discontinued when the chronic treatment was initiated. Because of the low mobility of P in carbonate sediments, we hypothesized long-term changes to ecosystem structure and function in both treatments. Structural changes in the chronic treatment included a shift in the dominant seagrass species from Thalassia testudinum to Halodule wrightii, large increases in epiphytic biomass and sediment chlorophyll-a, and a decline in species richness. Functional changes included increased benthic metabolism and quantum efficiency. Initial changes in the 28-month fertilization were similar, but after 23 years of nutrient depuration T. testudinum has reestablished itself as the dominant species. However, P remains elevated in the sediment and H. wrightii has maintained a presence. Functionally the discontinued treatment remains altered. Biomass exceeds that in the chronic treatment and indices of productivity, elevated relative to control, are not different from the chronic fertilization. Cessation of nutrient loading has resulted in a superficial return to the pre-disturbance character of the community, but due to the nature of P cycles functional changes persist.

Nutrient impacts on epifaunal density and species composition in a subtropical seagrass bed

The capacity of epifauna to control algal proliferation following nutrient input depends on responses of both grazers and upper trophic level consumers to enrichment. We examined the responses of Thalassia testudinum (turtle grass) epifaunal assemblages to nutrient enrichment at two sites in Florida Bay with varying levels of phosphorus limitation. We compared epifaunal density, biomass, and species diversity in 2 m2 plots that had either ambient nutrient concentrations or had been enriched with nitrogen and phosphorus for 6 months. At the severely P-limited site, total epifaunal density and biomass were two times higher in enriched than in unenriched plots. Caridean shrimp, grazing isopods, and gammarid amphipods accounted for much of the increase in density; brachyuran crabs, primary predatory fish, and detritivorous sea cucumbers accounted for most of the increase in biomass. At the less P-limited site, total epifaunal density and biomass were not affected by nutrient addition, although there were more caridean shrimp and higher brachyuran crab and pink shrimp biomass in enriched plots. At both sites, some variation in epifaunal density and biomass was explained by features of the macrophyte canopy, such as T. testudinum and Halodule wrightii percent cover, suggesting that enrichment may change the refuge value of the macrophyte canopy for epifauna. Additional variation in epifaunal density and biomass was explained by epiphyte pigment concentrations, suggesting that enrichment may change the microalgal food resources that support grazing epifauna. Increased epifaunal density in enriched plots suggests that grazers may be able to control epiphytic algal proliferation following moderate nutrient input to Florida Bay.

The effects of carbon dioxide fertilization on the ecology of tropical seagrass communities

Increasing atmospheric CO2 concentrations associated with climate change will likely influence a wide variety of ecosystems. Terrestrial research has examined the effects of increasing CO2 concentrations on the functionality of plant systems; with studies ranging in scale from the short-term responses of individual leaves, to long-term ecological responses of complete forests. While terrestrial plants have received much attention, studies on the responses of marine plants (seagrasses) to increased CO 2(aq) concentrations remain relatively sparse, with most research limited to small-scale, ex situ experimentation. Furthermore, few studies have attempted to address similarities between terrestrial and seagrass responses to increases in CO2(aq). The goals of this dissertation are to expand the scope of marine climate change research, and examine how the tropical seagrass, Thalassia testudinum responds to increasing CO 2(aq)concentrations over multiple spatial and temporal scales. ^ Manipulative laboratory and field experimentation reveal that, similar to terrestrial plants, seagrasses strongly respond to increases in CO 2(aq) concentrations. Using a novel field technique, in situ field manipulations show that over short time scales, seagrasses respond to elevated CO2(aq) by increasing leaf photosynthetic rates and the production of soluble carbohydrates. Declines in leaf nutrient (nitrogen and phosphorus) content were additionally detected, paralleling responses from terrestrial systems. Over long time scales, seagrasses increase total above- and belowground biomass with elevated CO2(aq), suggesting that, similar to terrestrial research, pervasive increases in atmospheric and oceanic CO2(aq) concentrations stand to influence the productivity and functionality of these systems. Furthermore, field experiments reveal that seagrass epiphytes, which comprise an important component of seagrass ecosystems, additionally respond to increased CO2(aq) with strong declines in calcified taxa and increases in fleshy taxa. ^ Together, this work demonstrates that increasing CO2(aq) concentrations will alter the functionality of seagrass ecosystems by increasing plant productivity and shifting the composition of the epiphyte community. These results have implications for future rates of carbon storage and sediment production within these widely distributed systems.^

Ecological indicators for assessing and communicating seagrass status and trends in Florida Bay

A suite of seagrass indicator metrics is developed to evaluate four essential measures of seagrass community status for Florida Bay. The measures are based on several years of monitoring data using the Braun-Blanquet Cover Abundance (BBCA) scale to derive information about seagrass spatial extent, abundance, species diversity and presence of target species. As ecosystem restoration proceeds in south Florida, additional freshwater will be discharged to Florida Bay as a means to restore the bay's hydrology and salinity regime. Primary hypotheses about restoring ecological function of the keystone seagrass community are based on the premise that hydrologic restoration will increase environmental variability and reduce hypersalinity. This will create greater niche space and permit multiple seagrass species to co-exist while maintaining good environmental conditions for Thalassia testudinum, the dominant climax seagrass species. Greater species diversity is considered beneficial to habitat for desired higher trophic level species such as forage fish and shrimp. It is also important to maintenance of a viable seagrass community that will avoid die-off events observed in the past. Indicator metrics are assigned values at the basin spatial scale and are aggregated to five larger zones. Three index metrics are derived by combining the four indicators through logic gates at the zone spatial scale and aggregated to derive a single bay-wide system status score standardized on the System-wide Indicator protocol. The indicators will provide a way to assess progress toward restoration goals or reveal areas of concern. Reporting for each indicator, index and overall system status score is presented in a red–yellow–green format that summarizes information in a readily accessible form for mangers, policy-makers and stakeholders in planning and implementing an adaptive management strategy.

Quantitative and Qualitative Aspects of Dissolved Organic Carbon Leached from Senescent Plants in an Oligotrophic Wetland

We conducted a series of experiments whereby dissolved organic matter (DOM) was leached from various wetland and estuarine plants, namely sawgrass (Cladium jamaicense), spikerush (Eleocharis cellulosa), red mangrove (Rhizophora mangle), cattail (Typha domingensis), periphyton (dry and wet mat), and a seagrass (turtle grass; Thalassia testudinum). All are abundant in the Florida Coastal Everglades (FCE) except for cattail, but this species has a potential to proliferate in this environment. Senescent plant samples were immersed into ultrapure water with and without addition of 0.1% NaN3 (w/ and w/o NaN3, respectively) for 36 days. We replaced the water every 3 days. The amount of dissolved organic carbon (DOC), sugars, and phenols in the leachates were analyzed. The contribution of plant leachates to the ultrafiltered high molecular weight fraction of DOM (>1 kDa; UDOM) in natural waters in the FCE was also investigated. UDOM in plant leachates was obtained by tangential flow ultrafiltration and its carbon and phenolic compound compositions were analyzed using solid state 13C cross-polarization magic angle spinning nuclear magnetic resonance (13C CPMAS NMR) spectroscopy and thermochemolysis in the presence of tetramethylammonium hydroxide (TMAH thermochemolysis), respectively. The maximum yield of DOC leached from plants over the 36-day incubations ranged from 13.0 to 55.2 g C kg−1 dry weight. This amount was lower in w/o NaN3 treatments (more DOC was consumed by microbes than produced) except for periphyton. During the first 2 weeks of the 5 week incubation period, 60–85% of the total amount of DOC was leached, and exponential decay models fit the leaching rates except for periphyton w/o NaN3. Leached DOC (w/ NaN3) contained different concentrations of sugars and phenols depending on the plant types (1.09–7.22 and 0.38–12.4 g C kg−1 dry weight, respectively), and those biomolecules comprised 8–34% and 4–28% of the total DOC, respectively. This result shows that polyphenols that readily leach from senescent plants can be an important source of chromophoric DOM (CDOM) in wetland environments. The O-alkyl C was found to be the major C form (55±9%) of UDOM in plant leachates as determined by 13C CPMAS NMR. The relative abundance of alkyl C and carbonyl C was consistently lower in plant-leached UDOM than that in natural water UDOM in the FCE, which suggests that these constituents increase in relative abundance during diagenetic processing. TMAH thermochemolysis analysis revealed that the phenolic composition was different among the UDOM leached from different plants, and was expected to serve as a source indicator of UDOM in natural water. Polyphenols are, however, very reactive and photosensitive in aquatic environments, and thus may loose their plant-specific molecular characteristics shortly. Our study suggests that variations in vegetative cover across a wetland landscape will affect the quantity and quality of DOM leached into the water, and such differences in DOM characteristics may affect other biogeochemical processes.

Ocean Acidification Outweighs Nutrient Effects in Structuring Seagrass Epiphyte Communities

Developing a framework for assessing interactions between multiple anthropogenic stressors remains an important goal in environmental research. In coastal ecosystems, the relative effects of aspects of global climate change (e.g. CO2 concentrations) and localized stressors (e.g. eutrophication), in combination, have received limited attention. Using a long-term (11 month) field experiment, we examine how epiphyte assemblages in a tropical seagrass meadow respond to factorial manipulations of dissolved carbon dioxide (CO2(aq)) and nutrient enrichment. In situ CO2(aq) manipulations were conducted using clear, open-top chambers, which replicated carbonate parameter forecasts for the year 2100. Nutrient enrichment consisted of monthly additions of slow-release fertilizer, nitrogen (N) and phosphorus (P), to the sediments at rates equivalent to theoretical maximum rates of anthropogenic loading within the region (1.54 g N m−2 d−1 and 0.24 g P m−2 d−1). Epiphyte community structure was assessed on a seasonal basis and revealed declines in the abundance of coralline algae, along with increases in filamentous algae under elevated CO2(aq). Surprisingly, nutrient enrichment had no effect on epiphyte community structure or overall epiphyte loading. Interactions between CO2(aq) and nutrient enrichment were not detected. Furthermore, CO2(aq)-mediated responses in the epiphyte community displayed strong seasonality, suggesting that climate change studies in variable environments should be conducted over extended time-scales. Synthesis. The observed responses indicate that for certain locations, global stressors such as ocean acidification may take precedence over local eutrophication in altering the community structure of seagrass epiphyte assemblages. Given that nutrient-driven algal overgrowth is commonly cited as a widespread cause of seagrass decline, our findings highlight that alternate climate change forces may exert proximate control over epiphyte community structure.

Mechanisms of Bicarbonate Use Influence the Photosynthetic Carbon Dioxide Sensitivity of Tropical Seagrasses

The photosynthetic bicarbonate () use properties of three widely distributed tropical seagrasses were compared using a series of laboratory experiments. Photosynthetic rates of Thalassia testudinum, Halodule wrightii, and Syringodium filiforme were monitored in an enclosed chamber while being subjected to shifts in pH and dissolved inorganic carbon. Specific mechanisms of seagrass use were compared by examining the photosynthetic effects of the carbonic anhydrase inhibitor acetazolamide (AZ). All seagrasses increased photosynthetic rates with reduced pH, suggesting a large effect of dissolved aqueous carbon dioxide (CO2(aq)). However, there was considerable interspecific variation in pH response. T. testudinum was highly sensitive, increasing photosynthetic rates by 100% as the pH was reduced from 8.2 to 7.4, whereas rates in H. wrightii and S. filiforme increased by only 20% over a similar range, and displayed prominent photosynthetic plateaus, indicating an increased capacity for use. Additional incubations that manipulated [] under constant [CO2(aq)] support these findings, as only H. wrightii and S. filiforme increased photosynthetic rates with increasing []. T. testudinum responded to AZ addition, indicating that carbonic anhydrase enzymes facilitate limited use. H. wrightii and S. filiforme showed no response to AZ, suggesting alternate, more efficient mechanisms of use. Estimated kinetic parameters, Ks(CO2) and Vmax, revealed interspecific variation and further support these conclusions. Variation in photosynthetic pH responses and AZ sensitivity indicate distinctions in the carbon use properties of seagrasses exposed to similar environmental conditions. These results suggest that not all seagrasses will similarly respond to future increases in CO2(aq) availability. Attention towards potential shifts in competitive interactions within multispecific seagrass beds is warranted.

Data compilation on the biological response to ocean acidification: environmental and experimental context of data sets and related literature

The exponential growth of studies on the biological response to ocean acidification over the last few decades has generated a large amount of data. To facilitate data comparison, a data compilation hosted at the data publisher PANGAEA was initiated in 2008 and is updated on a regular basis (doi:10.1594/PANGAEA.149999). By January 2015, a total of 581 data sets (over 4 000 000 data points) from 539 papers had been archived. Here we present the developments of this data compilation five years since its first description by Nisumaa et al. (2010). Most of study sites from which data archived are still in the Northern Hemisphere and the number of archived data from studies from the Southern Hemisphere and polar oceans are still relatively low. Data from 60 studies that investigated the response of a mix of organisms or natural communities were all added after 2010, indicating a welcomed shift from the study of individual organisms to communities and ecosystems. The initial imbalance of considerably more data archived on calcification and primary production than on other processes has improved. There is also a clear tendency towards more data archived from multifactorial studies after 2010. For easier and more effective access to ocean acidification data, the ocean acidification community is strongly encouraged to contribute to the data archiving effort, and help develop standard vocabularies describing the variables and define best practices for archiving ocean acidification data.

Human-driven Benthic Jellyfish Blooms: Causes and Consequences for Coastal Marine Ecosystems

Coastal marine ecosystems are among the most impacted globally, attributable to individual and cumulative effects of human disturbance. Anthropogenic nutrient loading is one stressor that commonly affects nearshore ecosystems, including seagrass beds, and has positive and negative effects on the structure and function of coastal systems. An additional, previously unexplored mechanistic pathway through which nutrients may indirectly influence nearshore systems is by driving blooms of benthic jellyfish. My dissertation research, conducted on Abaco Island, Bahamas, focused on elucidating the role that benthic jellyfish have in structuring systems in which they are common (i.e., seagrass beds), and explored mechanistic processes that may drive blooms of this taxa. To establish that human disturbances (e.g., elevated nutrient availability) may drive increased abundance and size of benthic jellyfish, Cassiopea spp., I conducted surveys in human-impacted and unimpacted coastal sites. Jellyfish were more abundant (and larger) from human-impacted areas, positively correlated to elevated nutrient availability. In order to elucidate mechanisms linking Cassiopea spp. with elevated nutrients, I evaluated whether zooxanthellae from Cassiopea were higher from human-disturbed systems, and whether Cassiopea exhibited increased size following nutrient input. I demonstrated that zooxanthellae population densities were elevated in human-impacted sites, and that nutrients led to positive jellyfish growth. As heightened densities of Cassiopea jellyfish may exert top-down and bottom-up controls on flora and fauna in impacted seagrass beds, I sought to examine ecological responses to Cassiopea. I evaluated whether there was a relationship between high Cassiopea densities and lower benthic fauna abundance and diversity in shallow seagrass beds. I found that Cassiopea have subtle effects on benthic fauna. However, through an experiment conducted in a seagrass bed in which nutrients and Cassiopea were added, I demonstrated that Cassiopea can result in seagrass habitat modification, with negative consequences for benthic fauna. My dissertation research demonstrates that increased human-driven benthic jellyfish densities may have indirect and direct effects on flora and fauna of coastal marine systems. This knowledge will advance our understanding of how human disturbances shift species interactions in coastal ecosystems, and will be critical for effective management of jellyfish blooms.

Spatial and seasonal variability in elemental content, δ13C, and δ15N ofThalassia testudinum from South Florida and its implications for ecosystem studies

Elemental and isotopic composition of leaves of the seagrassThalassia testudinum was highly variable across the 10,000 km2 and 8 years of this study. The data reported herein expand the reported range in carbon:nitrogen (C:N) and carbon:phosphorus (C:P) ratios and δ13C and δ15N values reported for this species worldwide; 13.2–38.6 for C:N and 411–2,041 for C:P. The 981 determinations in this study generated a range of −13.5‰ to −5.2‰ for δ13C and −4.3‰ to 9.4‰ for δ15N. The elemental and isotope ratios displayed marked seasonality, and the seasonal patterns could be described with a simple sine wave model. C:N, C:P, δ13C, and δ15N values all had maxima in the summer and minima in the winter. Spatial patterns in the summer maxima of these quantities suggest there are large differences in the relative availability of N and P across the study area and that there are differences in the processing and the isotopic composition of C and N. This work calls into question the interpretation of studies about nutrient cycling and food webs in estuaries based on few samples collected at one time, since we document natural variability greater than the signal often used to imply changes in the structure or function of ecosystems. The data and patterns presented in this paper make it clear that there is no threshold δ15N value for marine plants that can be used as an unambiguous indicator of human sewage pollution without a thorough understanding of local temporal and spatial variability.

Estimating the efficiency of a small beam trawl for sampling tiger prawns Penaeus esculentus and P. semisulcatus in seagrass by removal experiments

The efficiency with which a small beam trawl (1 x 0.5 m mouth) sampled postlarvae and juveniles of tiger prawns Penaeus esculentus and P, semisulcatus at night was estimated in 3 tropical seagrass communities (dominated by Thalassia hemprichii, Syringodium isoetifolium and Enhalus acoroides, respectively) in the shallow waters of the Gulf of Carpentaria in northern Australia. An area of seagrass (40 x 3 m) was enclosed by a net and the beam trawl was repeatedly hand-hauled over the substrate. Net efficiency (q) was calculated using 4 methods: the unweighted Leslie, weighted Leslie, DeLury and Maximum-likelihood (ML) methods. The Maximum-likelihood is the preferred method for estimating efficiency because it makes the fewest assumptions and is not affected by zero catches. The major difference in net efficiencies was between postlarvae (mean ML q +/- 95% confidence limits = 0.66 +/- 0.16) and juveniles of both species (mean q for juveniles in water less than or equal to 1.0 m deep = 0.47 +/- 0.05), i.e. the beam trawl was more efficient at capturing postlarvae than juveniles. There was little difference in net efficiency for P, esculentus between seagrass types (T, hemprichii versus S. isoetifolium), even though the biomass and morphologies of seagrass in these communities differed greatly (biomasses were 54 and 204 g m(-2), respectively). The efficiency of the net appeared to be the same for juveniles of the 2 species in shallow water, but was lower for juvenile P, semisulcatus at high tide when the water was deeper (1.6 to 1.9 m) (0.35 +/- 0.08). The lower efficiency near the time of high tide is possibly because the prawns are more active at high than low tide, and can also escape above the net. Factors affecting net efficiency and alternative methods of estimating net efficiency are discussed.