Relative significance of pelagic, benthic and allochthonous organic matter to microbial carbon cycling in a phosphorus-depleted subtropical estuary (Florida Bay)

Heterotrophic bacteria are important decomposers and transformers of primary production and provide an important link between detritus and the aquatic food web. In seagrass ecosystems, much of seagrass primary production is unavailable through direct grazing and must undergo microbial reworking before seagrass production can enter the aquatic food web. The goal of my dissertation research is to understand better the role heterotrophic bacteria play in carbon cycling in seagrass estuaries. My dissertation research focuses on Florida Bay, a seagrass estuary that has experienced recent changes in carbon source availability, which may have altered ecosystem function. My dissertation research investigates the importance of seagrass, algal and/or cyanobacterial, and allochthonous-derived organic matter to heterotrophic bacteria in Florida Bay and helps establish the carbon base of the estuarine food web. ^ A three tiered approach to the study of heterotrophic bacterial carbon cycling and trophic influences in Florida Bay was used: (1) Spatiotemporal observations of environmental parameters (hydrology, nutrients, extracellular enzymes, and microbial abundance, biomass, and production); (2) Microbial grazing experiments under different levels of top-down and bottom-up influence; and (3) Bulk and compound-specific (bacteria-biomarker fatty acid analysis) stable carbon isotope analysis. ^ In Florida Bay, spatiotemporal patterns in microbial extracellular enzyme (also called ectoenzyme) activities indicate that microorganisms hydrolyzed selectively fractions of the estuarine organic matter pool. The microbial community hydrolyzed organic acids, peptides, and phosphate esters and did not use storage and structural carbohydrates. Organic matter use by heterotrophic bacterioplankton in Florida Bay was co-regulated by bottom-up (resource availability) and top-down (grazer mediated) processes. A bacterial carbon budget based on bacterial, epiphytic, and seagrass production indicates that heterotrophic bacterial carbon cycles are supported primarily through epiphytic production with mixing from seagrass production. Stable carbon isotope analysis of bacteria biomarkers and carbon sources in Florida Bay corroborate the results of the bacterial carbon budget. These results support previous studies of aquatic consumers in Florida Bay, indicating that epiphytic/benthic algal and/or cyanobacterial production with mixing from seagrass-derived organic matter is the carbon base of the seagrass estuarine food web. ^

Experimental nutrient enrichment causes complex changes in seagrass, microalgae, and macroalgae community structure in Florida Bay

We evaluated how changes in nutrient supply altered the composition of epiphytic and benthic microalgal communities in a Thalassia testudinum (turtle grass) bed in Florida Bay. We established study plots at four sites in the bay and added nitrogen (N) and phosphorus (P) to the sediments in a factorial design. After 18, 24, and 30 months of fertilization we measured the pigment concentrations in the epiphytic and benthic microalgal assemblages using high performance liquid chromatography. Overall, the epiphytic assemblage was P-limited in the eastern portion of the bay, but each phototrophic group displayed unique spatial and temporal responses to N and P addition. Epiphytic chlorophyll a, an indicator of total microalgal load, and epiphytic fucoxanthin, an indicator of diatoms, increased in response to P addition at one eastern bay site, decreased at another eastern bay site, and were not affected by P or N addition at two western bay sites. Epiphytic zeaxanthin, an indicator of the cyanobacteria/coralline red algae complex, and epiphytic chlorophyll b, an indicator of green algae, generally increased in response to P addition at both eastern bay sites but did not respond to P or N addition in the western bay. Benthic chlorophyll a, chlorophyll b, fucoxanthin, and zeaxanthin showed complex responses to N and P addition in the eastern bay, suggesting that the benthic assemblage is limited by both N and P. Benthic assemblages in the western bay were variable over time and displayed few responses to N or P addition. The contrasting nutrient limitation patterns between the epiphytic and benthic communities in the eastern bay suggest that altering nutrient input to the bay, as might occur during Everglades restoration, can shift microalgal community structure, which may subsequently alter food web support for upper trophic levels.

Stable isotopes reveal complex changes in trophic relationships following nutrient addition in a coastal marine ecosystem

Complex links between the top-down and bottomup forces that structure communities can be disrupted by anthropogenic alterations of natural habitats.We used relative abundance and stable isotopes to examine changes in epifaunal food webs in seagrass (Thalassia testudinum) beds following 6 months of experimental nutrient addition at two sites in Florida Bay (USA) with different ambient fertility. At a eutrophic site, nutrient addition did not strongly affect food web structure, but at a nutrient-poor site, enrichment increased the abundances of crustacean epiphyte grazers, and the diets of these grazers became more varied. Benthic grazers did not change in abundance but shifted their diet away from green macroalgae + associated epiphytes and towards an opportunistic seagrass (Halodule wrightii) that occurred only in nutrient addition treatments. Benthic predators did not change in abundance, but their diets were more varied in enriched plots. Food chain length was short and unaffected by site or nutrient treatment, but increased food web complexity in enriched plots was suggested by increasingly mixed diets. Strong bottom-up modifications of food web structure in the nutrient-limited site and the limited top-down influences of grazers on seagrass epiphyte biomass suggest that, in this system, the bottom-up role of nutrient enrichment can have substantial impacts on community structure, trophic relationships, and, ultimately, the productivity values of the ecosystem.

Modeling seasonal dynamics of small fish cohorts in fluctuating freshwater marsh landscapes

Small-bodied fishes constitute an important assemblage in many wetlands. In wetlands that dry periodically except for small permanent waterbodies, these fishes are quick to respond to change and can undergo large fluctuations in numbers and biomasses. An important aspect of landscapes that are mixtures of marsh and permanent waterbodies is that high rates of biomass production occur in the marshes during flooding phases, while the permanent waterbodies serve as refuges for many biotic components during the dry phases. The temporal and spatial dynamics of the small fishes are ecologically important, as these fishes provide a crucial food base for higher trophic levels, such as wading birds. We develop a simple model that is analytically tractable, describing the main processes of the spatio-temporal dynamics of a population of small-bodied fish in a seasonal wetland environment, consisting of marsh and permanent waterbodies. The population expands into newly flooded areas during the wet season and contracts during declining water levels in the dry season. If the marsh dries completely during these times (a drydown), the fish need refuge in permanent waterbodies. At least three new and general conclusions arise from the model: (1) there is an optimal rate at which fish should expand into a newly flooding area to maximize population production; (2) there is also a fluctuation amplitude of water level that maximizes fish production, and (3) there is an upper limit on the number of fish that can reach a permanent waterbody during a drydown, no matter how large the marsh surface area is that drains into the waterbody. Because water levels can be manipulated in many wetlands, it is useful to have an understanding of the role of these fluctuations.

Spatiotemporal patterns in community structure of macroinvertebrates inhabiting calcareous periphyton mats

Calcareous floating periphyton mats in the southern Everglades provide habitat for a diverse macroinvertebrate community that has not been well characterized. Our study described this community in an oligotrophic marsh, compared it with the macroinvertebrate community associated with adjacent epiphytic algae attached to macrophytes in the water column, and detected spatial patterns in density and community structure. The floating periphyton mat (floating mat) and epiphytic algae in the water column (submerged epiphyton) were sampled at 4 sites (1 km apart) in northern Shark River Slough, Everglades National Park (ENP), in the early (July) and late (November) wet season. Two perpendicular 90-m transects were established at each site and 100 samples were taken in a nested design. Sites were located in wet-prairie spikerush-dominated sloughs with similar water depths and emergent macrophyte communities. Floating mats were sampled by taking cores (6-cm diameter) that were sorted under magnification to enumerate infauna retained on a 250-μm-mesh sieve and with a maximum dimension >1 mm. Our results showed that floating mats provide habitat for a macroinvertebrate community with higher densities (no. animals/g ash-free dry mass) of Hyalella azteca, Dasyhelea spp., and Cladocera, and lower densities of Chironomidae and Planorbella spp. than communities associated with submerged epiphyton. Densities of the most common taxa increased 3× to 15× from early to late wet season, and community differences between the 2 habitat types became more pronounced. Floating-mat coverage and estimated floating-mat biomass increased 20 to 30% and 30 to 110%, respectively, at most sites in the late wet season. Some intersite variation was observed in individual taxa, but no consistent spatial pattern in any taxon was detected at any scale (from 0.2 m to 3 km). Floating mats and their resident macroinvertebrate communities are important components in the Everglades food web. This community should be included in environmental monitoring programs because degradation and eventual loss of the calcareous periphyton mat is associated with P enrichment in this ecosystem.

Organic Biogeochemistry of Detrital Flocculent Material (Floc) in a Subtropical, Coastal Wetland

Flocculent materials (floc), in aquatic systems usually consist of a non-consolidated layer of biogenic, detrital material relatively rich in organic matter which represents an important food-web component for invertebrates and fish. Thus, variations in its composition could impact food webs and change faunal structure. Transport, remineralization rates and deposition of floc may also be important factors in soil/sediment formation. In spite of its relevance and sensitivity to external factors, few chemical studies have been carried out on the biogeochemistry of floc material. In this study, we focused on the molecular characterization of the flocculent organic matter (OM), the assessment of its origin and its environmental fate at five stations along a freshwater to marine ecotone, namely the Taylor Slough, Everglades National Park (ENP), Florida. To tackle this issue, suspended, unconsolidated, detrital floc samples, soils/sediments and plants were analyzed for bulk properties, biomarkers and pigments. Both geochemical proxies and biomass-specific biomarkers were used to assess OM sources and transformations. Our results show that the detrital organic matter of the flocculent material is largely regulated by local vegetation inputs, ranging from periphyton, emergent and submerged plants and terrestrial plants such as mangroves, with molecular evidence of different degrees of diagenetic reworking, including fungal activity. Evidence is presented for both hydrodynamic transport of floc materials, and incorporation of floc OM into soils/sediments. However, some molecular parameters showed a decoupling between floc and underlying soil/sediment OM, suggesting that physical transport, incorporation and degradation/remineralization of OM in floc may be controlled by a combination of a variety of complex biogeochemical variables including hydrodynamic transport, hydroperiod characteristics, primary productivity, nutrient availability, and OM quality among others. Further investigations are needed to better understand the ecological role of floc in freshwater and coastal wetlands.

Biotic and abiotic determinants of intermediate-consumer trophic diversity in the Florida everglades

Food-web structure can shape population dynamics and ecosystem functioning and stability. We investigated the structure of a food-web fragment consisting of dominant intermediate consumers (fishes and crayfishes) in the Florida Everglades, using stable isotope analysis to quantify trophic diversity along gradients of primary production (periphyton), disturbance (marsh drying) and intermediate-consumer density (a possible indicator of competition). We predicted that trophic diversity would increase with resource availability and decrease after disturbance, and that competition could result in greater trophic diversity by favouring resource partitioning. Total trophic diversity, measured by niche area, decreased with periphyton biomass and an ordination axis representing several bluegreen algae species. Consumers’ basal resource diversity, estimated by δ13C values, was similarly related to algal community structure. The range of trophic levels (δ15N range) increased with time since the most recent drying and reflooding event, but decreased with intermediate-consumer density, and was positively related to the ordination axis reflecting increases in green algae and decreases in filamentous bluegreen algae. Our findings suggest that algal quality, independent of quantity, influences food-web structure and demonstrate an indirect role of nutrient enrichment mediated by its effects on periphyton palatability and biomass. These results reveal potential mechanisms for anthropogenic effects on Everglades communities.

Aquatic fauna as indicators for Everglades restoration: Applying dynamic targets in assessments

A major goal of the Comprehensive Everglades Restoration Plan (CERP) is to recover historical (pre-drainage) wading bird rookeries and reverse marked decreases in wading bird nesting success in Everglades National Park. To assess efforts to restore wading birds, a trophic hypothesis was developed that proposes seasonal concentrations of small-fish and crustaceans (i.e., wading bird prey) were a key factor to historical wading bird success. Drainage of the Everglades has diminished these seasonal concentrations, leading to a decline in wading bird nesting and displacing them from their historical nesting locations. The trophic hypothesis predicts that restoring historical hydrological patterns to pre-drainage conditions will recover the timing and location of seasonally concentrated prey, ultimately restoring wading bird nesting and foraging to the southern Everglades. We identified a set of indicators using small-fish and crustaceans that can be predicted from hydrological targets and used to assess management success in regaining suitable wading bird foraging habitat. Small-fish and crustaceans are key components of the Everglades food web and are sensitive to hydrological management, track hydrological history with little time lag, and can be studied at the landscape scale. The seasonal hydrological variation of the Everglades that creates prey concentrations presents a challenge to interpreting monitoring data. To account for the variable hydrology of the Everglades in our assessment, we developed dynamic hydrological targets that respond to changes in prevailing regional rainfall. We also derived statistical relationships between density and hydrological drivers for species representing four different life-history responses to drought. Finally, we use these statistical relationships and hydrological targets to set restoration targets for prey density. We also describe a report-card methodology to communicate the results of model-based assessments for communication to a broad audience.

Does landscape context affect habitat value? The importance of seascape ecology in back-reef systems

Seascape ecology provides a useful framework from which to understand the processes governing spatial variability in ecological patterns. Seascape context, or the composition and pattern of habitat surrounding a focal patch, has the potential to impact resource availability, predator-prey interactions, and connectivity with other habitats. For my dissertation research, I combined a variety of approaches to examine how habitat quality for fishes is influenced by a diverse range of seascape factors in sub-tropical, back-reef ecosystems. In the first part of my dissertation, I examined how seascape context can affect reef fish communities on an experimental array of artificial reefs created in various seascape contexts in Abaco, Bahamas. I found that the amount of seagrass at large spatial scales was an important predictor of community assembly on these reefs. Additionally, seascape context had differing effects on various aspects of habitat quality for the most common reef species, White grunt Haemulon plumierii. The amount of seagrass at large spatial scales had positive effects on fish abundance and secondary production, but not on metrics of condition and growth. The second part of my dissertation focused on how foraging conditions for fish varied across a linear seascape gradient in the Loxahatchee River estuary in Florida, USA. Gray snapper, Lutjanus griseus, traded food quality for quantity along this estuarine gradient, maintaining similar growth rates and condition among sites. Additional work focused on identifying major energy flow pathways to two consumers in oyster-reef food webs in the Loxahatchee. Algal and microphytobenthos resource pools supported most of the production to these consumers, and body size for one of the consumers mediated food web linkages with surrounding mangrove habitats. All of these studies examined a different facet of the importance of seascape context in governing ecological processes occurring in focal habitats and underscore the role of connectivity among habitats in back-reef systems. The results suggest that management approaches consider the surrounding seascape when prioritizing areas for conservation or attempting to understand the impacts of seascape change on focal habitat patches. For this reason, spatially-based management approaches are recommended to most effectively manage back-reef systems.

A Review of the Effects of Altered Hydrology and Salinity on Vertebrate Fauna and Their Habitats in Northeastern Florida Bay

Estuarine productivity is highly dependent on the freshwater sources of the estuary. In Florida Bay, Taylor Slough was historically the main source of fresh water. Beginning in about 1960, and culminating with the completion of the South Dade Conveyance System in 1984, water management practice began to change the quantity and distribution of flow from Taylor Slough into Northeastern Florida Bay. These practices altered salinity and hydrologic parameters that had measurable negative impacts on vertebrate fauna and their habitats. Here, I review those impacts from published and unpublished literature and anecdotal observations. Almost all vertebrates covered in this review have shown some form of population decline since 1984; most of the studies implicate declines in food resources as the main stressor on their populations. My conclusion is that the diversion of fresh water resulted in an ecological cascade starting with hydrologic stresses on primary then secondary producers culminating in population declines at the top of the food web.

Slow Isotope Turnover Rates and Low Discrimination Values in the American Alligator: Implications for Interpretation of Ectotherm Stable Isotope Data

Stable isotope analysis has become a standard ecological tool for elucidating feeding relationships of organisms and determining food web structure and connectivity. There remain important questions concerning rates at which stable isotope values are incorporated into tissues (turnover rates) and the change in isotope value between a tissue and a food source (discrimination values). These gaps in our understanding necessitate experimental studies to adequately interpret field data. Tissue turnover rates and discrimination values vary among species and have been investigated in a broad array of taxa. However, little attention has been paid to ectothermic top predators in this regard. We quantified the turnover rates and discrimination values for three tissues (scutes, red blood cells, and plasma) in American alligators (Alligator mississippiensis). Plasma turned over faster than scutes or red blood cells, but turnover rates of all three tissues were very slow in comparison to those in endothermic species. Alligator δ15N discrimination values were surprisingly low in comparison to those of other top predators and varied between experimental and control alligators. The variability of δ15N discrimination values highlights the difficulties in using δ15N to assign absolute and possibly even relative trophic levels in field studies. Our results suggest that interpreting stable isotope data based on parameter estimates from other species can be problematic and that large ectothermic tetrapod tissues may be characterized by unique stable isotope dynamics relative to species occupying lower trophic levels and endothermic tetrapods.

Metacommunity Structure Along Resource and Disturbance Gradients in Everglades Wetlands

We evaluated metacommunity hypotheses of landscape arrangement (indicative of dispersal limitation) and environmental gradients (hydroperiod and nutrients) in structuring macroinvertebrate and fish communities in the southern Everglades. We used samples collected at sites from the eastern boundary of the southern Everglades and from Shark River Slough, to evaluate the role of these factors in metacommunity structure. We used eigenfunction spatial analysis to model community structure among sites and distance-based redundancy analysis to partition the variability in communities between spatial and environmental filters. For most animal communities, hydrological parameters had a greater influence on structure than nutrient enrichment, however both had large effects. The influence of spatial effects indicative of dispersal limitation was weak and only periphyton infauna appeared to be limited by regional dispersal. At the landscape scale, communities were well-mixed, but strongly influenced by hydrology. Local-scale species dominance was influenced by water-permanence and nutrient enrichment. Nutrient enrichment is limited to water inflow points associated with canals, which may explain its impact in this data set. Hydroperiod and nutrient enrichment are controlled by water managers; our analysis indicates that the decisions they make have strong effects on the communities at the base of the Everglades food web.

Simulating Mechanisms for Dispersal, Production and Stranding of Small Forage Fish in Temporary Wetland Habitats

Movement strategies of small forage fish (<8 cm total length) between temporary and permanent wetland habitats affect their overall population growth and biomass concentrations, i.e., availability to predators. These fish are often the key energy link between primary producers and top predators, such as wading birds, which require high concentrations of stranded fish in accessible depths. Expansion and contraction of seasonal wetlands induce a sequential alternation between rapid biomass growth and concentration, creating the conditions for local stranding of small fish as they move in response to varying water levels. To better understand how landscape topography, hydrology, and fish behavior interact to create high densities of stranded fish, we first simulated population dynamics of small fish, within a dynamic food web, with different traits for movement strategy and growth rate, across an artificial, spatially explicit, heterogeneous, two-dimensional marsh slough landscape, using hydrologic variability as the driver for movement. Model output showed that fish with the highest tendency to invade newly flooded marsh areas built up the largest populations over long time periods with stable hydrologic patterns. A higher probability to become stranded had negative effects on long-term population size, and offset the contribution of that species to stranded biomass. The model was next applied to the topography of a 10 km × 10 km area of Everglades landscape. The details of the topography were highly important in channeling fish movements and creating spatiotemporal patterns of fish movement and stranding. This output provides data that can be compared in the future with observed locations of fish biomass concentrations, or such surrogates as phosphorus ‘hotspots’ in the marsh.

Using Stable Isotopes to Investigate Trophic Interactions of Bottlenose Dolphins (Tursiops truncatus) in the Coastal Everglades

Top predators are best known for their ability to affect their communities through inflicting mortality on prey and inducing behavioral modifications (e.g. risk effects). Recent scientific evidence suggests that predators may have additional roles in bottom-up processes such as transporting materials within and across habitat boundaries. The Florida Coastal Everglades (FCE) is an “upside-down” oligotrophic estuary where productivity decreases from the mouth of the estuary to freshwater marshes. Research in the FCE suggest that predators can act as mobile links between disparate habitats and can potentially affect nutrient and biogeochemical dynamics through localized behaviors (e.g. American alligators and juvenile bull sharks). To date, little is known about bottlenose dolphins (Tursiops truncatus) in the FCE beyond broad-scale patterns of abundance. Because they are highly mobile mammals commonly found in coastal waters, bottlenose dolphins are an interesting case study for investigating the influence of ecology on the evolution of local adaptations. Within this influence lies the potential for investigation of the related roles those adaptations play in coastal ecosystems due to their high metabolic rates, movement capabilities, and tendency to display specialized foraging behaviors. Stable isotope analysis of biopsy samples were used to investigate habitat use, trophic interactions, and patterns of individual specialization in bottlenose dolphins to gain functional insights into ecosystem dynamics. δ13 C isotopic values are used to differentiate the relative importance of a food web to the diet of an organism, while δ15 N values are used to evaluate the relative trophic position of an organism. Dolphin δ13 C isotopic values seem to suggest that dolphins are foraging within single ecosystems and may not be moving nutrients across ecosystem boundaries while their δ15 N isotopic values appear to be of a top predator, at a similar level to bull sharks and alligators in FCE. Further research is necessary to provide vital insight into the large predators’ role in affecting the evolution of local adaptations. Conducting this research should also provide information for predicting how future changes occurring due to restoration dynamics (see CERP: evergladesplan.org) and climate change will affect the ecological roles of these animals.

Using Stable Isotopes to Investigate Trophic Interactions of Bottlenose Dolphins (Tursiops truncatus) in the Coastal Everglades”

Top predators are best known for their ability to affect their communities through inflicting mortality on prey and inducing behavioral modifications (e.g. risk effects). Recent scientific evidence suggests that predators may have additional roles in bottom-up processes such as transporting materials within and across habitat boundaries. The Florida Coastal Everglades (FCE) is an “upside-down” oligotrophic estuary where productivity decreases from the mouth of the estuary to freshwater marshes. Research in the FCE suggest that predators can act as mobile links between disparate habitats and can potentially affect nutrient and biogeochemical dynamics through localized behaviors (e.g. American alligators and juvenile bull sharks). To date, little is known about bottlenose dolphins (Tursiops truncatus) in the FCE beyond broad-scale patterns of abundance. Because they are highly mobile mammals commonly found in coastal waters, bottlenose dolphins are an interesting case study for investigating the influence of ecology on the evolution of local adaptations. Within this influence lies the potential for investigation of the related roles those adaptations play in coastal ecosystems due to their high metabolic rates, movement capabilities, and tendency to display specialized foraging behaviors. Stable isotope analysis of biopsy samples were used to investigate habitat use, trophic interactions, and patterns of individual specialization in bottlenose dolphins to gain functional insights into ecosystem dynamics. δ13 C isotopic values are used to differentiate the relative importance of a food web to the diet of an organism, while δ15 N values are used to evaluate the relative trophic position of an organism. Dolphin δ13 C isotopic values seem to suggest that dolphins are foraging within single ecosystems and may not be moving nutrients across ecosystem boundaries while their δ15 N isotopic values appear to be of a top predator, at a similar level to bull sharks and alligators in FCE. Further research is necessary to provide vital insight into the large predators’ role in affecting the evolution of local adaptations. Conducting this research should also provide information for predicting how future changes occurring due to restoration dynamics (see CERP: evergladesplan.org) and climate change will affect the ecological roles of these animals.