A synthesis of long-term research by the Florida Coastal Everglades LTER Program

This paper synthesizes research conducted during the first 5–6 years of the Florida Coastal Everglades Long-Term Ecological Research Program (FCE LTER). My objectives are to review our research to date, and to present a new central theme and conceptual approach for future research. Our research has focused on understanding how dissolved organic matter (DOM) from upstream oligotrophic marshes interacted with a marine source of the limiting nutrient, phosphorus (P), to control productivity in the oligohaline estuarine ecotone. We have been working along freshwater to marine transects in two drainage basins located in Everglades National Park (ENP). The Shark River Slough transect (SRS) has a direct connection to the Gulf of Mexico, providing this estuarine ecotone with a source of marine P. The oligohaline ecotone along our southern Everglades transect (TS/Ph), however, is separated from this marine P source by the Florida Bay estuary. We originally hypothesized an ecosystem productivity peak in the SRS ecotone, driven by the interaction of marine P and Everglades DOM, but no such productivity peak in the TS/Ph ecotone because of this lack of marine P. Our research to date has tended to show the opposite pattern, however, with many ecosystem components showing enhanced productivity in the TS/Ph ecotone, but not in the SRS ecotone. Water column P concentrations followed a similar pattern, with unexpectedly high P in the TS/Ph ecotone during the dry season. Our organic geochemical research has shown that Everglades DOM is more refractory than originally hypothesized. We have also begun to understand the importance of detrital organic matter production and transport to ecotone dynamics and as the base of aquatic food webs. Our future research will build on this substantial body of knowledge about these oligotrophic estuaries. We will direct our efforts more strongly on biophysical dynamics in the oligohaline ecotone regions. Specifically, we will be focusing on inputs to these regions from four primary water sources: freshwater Everglades runoff, net precipitation, marine inputs, and groundwater. We are hypothesizing that dry season groundwater inputs of P will be particularly important to TS/Ph ecotone dynamics because of longer water residence times in this area. Our organic geochemical, biogeochemical, and ecosystem energetics work will focus more strongly on the importance of detrital organics and will take advantage of a key Everglades Restoration project, scheduled for 2008 or 2009, that will increase freshwater inputs to our SRS transect only. Finally, we will also begin to investigate the human dimensions of restoration, and of a growing population in south Florida that will become increasingly dependent on the Everglades for critical ecosystem services (including fresh water) even as its growth presents challenges to Everglades sustainability.

Factors affecting the concentration and flux of materials in two southern Everglades mangrove wetlands

Concentrations and fluxes of C, N, and P were measured in dwarf and fringe mangrove wetlands along the Taylor River, Florida, USA from 1996 to 1998. Data from these studies revealed considerable spatial and temporal variability. Concentrations of C, N, and P in the dwarf wetland showed seasonal trends, while water source was better at explaining concentrations in the fringe wetland. The total and dissolved organic carbon (TOC and DOC), total nitrogen (TN), and total phosphorus (TP) content of both wetlands was higher during the wet season or when water was flowing to the south (Everglades source). Concentrations of nitrate plus nitrite (NOx –), ammonium (NH4 +), and soluble reactive phosphorus (SRP) in the fringe wetland were all highest during the dry season or northerly flow (bay source). Nutrient concentrations most effectively explained patterns of flux in both wetlands. Increased wetland uptake of a given constituent was usually a function of its availability in the water column. However, the release of NOx – from the dwarf wetland was related to the NH4 + concentration, suggesting a nitrification signal. Nitrogen flux in the dwarf wetland was also related to surface water salinity and temperature. Our findings indicate that freshwater Everglades marshes are an important source of dissolved organic matter to these wetlands, while Florida Bay may be a source of dissolved inorganic nutrients. Our data also suggest that temperature, salinity, and nutrient concentrations (as driven by season and water source) influence patterns of materials flux in this mangrove wetland. Applying long-term water quality data to the relationships we extracted from these flux data, we estimated that TN and TP were imported by the dwarf wetland 87 ± 10 and 48 ± 17% of the year, respectively. With Everglades restoration, modifications in freshwater delivery may have considerable effects on the exchanges of nutrients and organic matter in these transitional mangrove wetlands.

Social and seasonal plasticity of the electric fish, Brachyhypopomus gauderio

The South American electric knifefish, Brachyhypopomus gauderio, uses weakly electric fields to see and communicate in the dark. Only one study to date has investigated natural behavior in this species during the breeding season; this study proposed that B. guarerio has an exploded lek polygyny breeding system. To test this hypothesis, artificial marshes simulating the native vegetation, temperature, and water conductivities of the South American subtropics were created to study seasonal variation in associative behavior of B. gauderio during the breeding and non-breeding seasons. Mark/recapture methods were used to keep track of individual fish and their dispersion inside the experimental designs. The experimental design proved to be extremely successful at eliciting reproduction. Differences were found in seasonal variations of social behaviors between adult and juvenile populations. Although no apparent sex. differences in movement patterns were found during the breeding season; a trend for male-male aversion was found, suggesting male-male avoidance as a possible strategy guiding aspects of social behaviors in this species. Further, movement may be a tactic for mate seeking as the individuals who moved the most during the breeding season obtained the most opposite sex interactions. These findings support the exploded lek polygyny model. Social interactions are subject to complex regulation by social, physiologic and ecological factors; the extent to which these associations are repeatable may provide novel insights on the evolution of sociality as it has been shaped by natural selection.

A conceptual model of ecological interactions in the mangrove estuaries of the Florida Everglades

A brackish water ecotone of coastal bays and lakes, mangrove forests, salt marshes, tidal creeks, and upland hammocks separates Florida Bay, Biscayne Bay, and the Gulf of Mexico from the freshwater Everglades. The Everglades mangrove estuaries are characterized by salinity gradients that vary spatially with topography and vary seasonally and inter-annually with rainfall, tide, and freshwater flow from the Everglades. Because of their location at the lower end of the Everglades drainage basin, Everglades mangrove estuaries have been affected by upstream water management practices that have altered the freshwater heads and flows and that affect salinity gradients. Additionally, interannual variation in precipitation patterns, particularly those caused to El Nin˜o events, control freshwater inputs and salinity dynamics in these estuaries. Two major external drivers on this system are water management activities and global climate change. These drivers lead to two major ecosystem stressors: reduced freshwater flow volume and duration, and sea-level rise. Major ecological attributes include mangrove forest production, soil accretion, and resilience; coastal lake submerged aquatic vegetation; resident mangrove fish populations; wood stork (Mycteria americana) and roseate spoonbill (Platelea ajaja) nesting colonies; and estuarine crocodilian populations. Causal linkages between stressors and attributes include coastal transgression, hydroperiods, salinity gradients, and the ‘‘white zone’’ freshwater/estuarine interface. The functional estuary and its ecological attributes, as influenced by sea level and freshwater flow, must be viewed as spatially dynamic, with a possible near-term balancing of transgression but ultimately a long-term continuation of inland movement. Regardless of the spatio-temporal timing of this transgression, a salinity gradient supportive of ecologically functional Everglades mangrove estuaries will be required to maintain the integrity of the South Florida ecosystem.

Five new species of yeasts from fresh water and marine habitats in the Florida Everglades

Yeast populations in the Shark River Slough of the Florida Everglades, USA, were examined during a 3-year period (2002–2005) at six locations ranging from fresh water marshes to marine mangroves. Seventy-four described species (33 ascomycetes and 41 basidiomycetes) and an approximately equal number of undescribed species were isolated during the course of the investigation. Serious human pathogens, such as Candida tropicalis, were not observed, which indicates that their presence in coastal waters is due to sources of pollution. Some of the observed species were widespread throughout the fresh water and marine habitats, whereas others appeared to be habitat restricted. Species occurrence ranged from prevalent to rare. Five representative unknown species were selected for formal description. The five species comprise two ascomycetes: Candida sharkiensis sp. nov. (CBS 11368T) and Candida rhizophoriensis sp. nov. (CBS 11402T) (Saccharomycetales, Metschnikowiaceae), and three basidiomycetes: Rhodotorula cladiensis sp. nov. (CBS 10878T) in the Sakaguchia clade (Cystobasidiomycetes), Rhodotorula evergladiensis sp. nov. (CBS 10880T) in the Rhodosporidium toruloides clade (Microbotryomycetes, Sporidiobolales) and Cryptococcus mangaliensis sp. nov. (CBS 10870T) in the Bulleromyces clade (Agaricomycotina, Tremellales).

Water Uptake Patterns of an Invasive Exotic Plant in Coastal Saline Habitats

Schinus terebinthifolius Raddi (Schinus) is one of the most widely found woody exotic species in South Florida. This exotic is distributed across environments with different hydrologic regimes, from upland pine forests to the edges of sawgrass marshes and into saline mangrove forests. To determine if this invasive exotic had different physiological attributes compared to native species in a coastal habitat, we measured predawn xylem water potentials (Ψ), oxygen stable isotope signatures (δ18O), and sodium (Na+) and potassium (K+) contents of sap water from plants within: (1) a transition zone (between a mangrove forest and upland pineland) and (2) an upland pineland in Southwest Florida. Under dynamic salinity and hydrologic conditions, Ψ of Schinus appeared less subject to fluctuations caused by seasonality when compared with native species. Although stem water δ18O values could not be used to distinguish the depth of Schinus and native species' water uptake in the transition zone, Ψ and sap Na+/K+ patterns showed that Schinus was less of a salt excluder relative to the native upland species during the dry season. This exotic also exhibited Na+/K+ ratios similar to the mangrove species, indicating some salinity tolerance. In the upland pineland, Schinus water uptake patterns were not significantly different from those of native species. Differences between Schinus and native upland species, however, may provide this exotic an advantage over native species within mangrove transition zones.

Chilling damage in a changing climate in coastal landscapes of the subtropical zone: a case study from south Florida

Extensive portions of the southern Everglades are characterized by series of elongated, raised peat ridges and tree islands oriented parallel to the predominant flow direction, separated by intervening sloughs. Tall herbs or woody species are associated with higher elevations and shorter emergent or floating species are associated with lower elevations. The organic soils in this “Ridge-and-Slough” landscape have been stable over millennia in many locations, but degrade over decades under altered hydrologic conditions. We examined soil, pore water, and leaf phosphorus (P) and nitrogen (N) distributions in six Ridge and Slough communities in Shark Slough, Everglades National Park. We found P enrichment to increase and N to decrease monotonically along a gradient from the most persistently flooded sloughs to rarely flooded ridge environments, with the most dramatic change associated with the transition from marsh to forest. Leaf N:P ratios indicated that the marsh communities were strongly P-limited, while data from several forest types suggested either N-limitation or co-limitation by N and P. Ground water stage in forests exhibited a daytime decrease and partial nighttime recovery during periods of surface exposure. The recovery phase suggested re-supply from adjacent flooded marshes or the underlying aquifer, and a strong hydrologic connection between ridge and slough. We therefore developed a simple steady-state model to explore a mechanism by which a phosphorus conveyor belt driven by both evapotranspiration and the regional flow gradient can contribute to the characteristic Ridge and Slough pattern. The model demonstrated that evapotranspiration sinks at higher elevations can draw in low concentration marsh waters, raising local soil and water P concentrations. Focusing of flow and nutrients at the evapotranspiration zone is not strong enough to overcome the regional gradient entirely, allowing the nutrient to spread downstream and creating an elongated concentration plume in the direction of flow. Our analyses suggest that autogenic processes involving the effects of initially small differences in topography, via their interactions with hydrology and nutrient availability, can produce persistent physiographic patterns in the organic sediments of the Everglades.

Forest Resource Islands in a Sub-tropical Marsh: Soil–Site Relationships in Everglades Hardwood Hammocks

Spatial heterogeneity in soils is often characterized by the presence of resource-enriched patches ranging in size from a single shrub to wooded thickets. If the patches persist long enough, the primary constraint on production may transition from one limiting environmental factor to another. Tree islands that are scattered throughout the Florida Everglades basin comprise nutrient-enriched patches, or resource islands, in P-limited oligotrophic marshes. We used principal component analysis and multiple regressions to characterize the belowground environment (soil, hydrology) of one type of tree island, hardwood hammocks, and examined its relationship with the three structural variables (basal area, biomass, and canopy height) indicative of site productivity. Hardwood hammocks in the southern Everglades grow on two distinct soil types. The first, consisting of shallow, organic, relatively low-P soils, is common in the seasonally flooded Marl Prairie landscape. In contrast, hammocks on islands embedded in long hydroperiod marsh have deeper, alkaline, mineral soils with extremely high P concentrations. However, this edaphic variation does not translate simply into differences in forest structure and production. Relative water depth was unrelated to all measures of forest structure and so was soil P, but the non-carbonate component of the mineral soil fraction exhibited a strong positive relationship with canopy height. The development of P-enriched forest resource islands in the Everglades marsh is accompanied by the buildup of a mineral soil; however, limitations on growth in mature islands appear to differ substantively from those that dominate incipient stages in the transformation from marsh to forest. Key words: resource island; tree

Pattern of nutrient availability and plant community assemblage in Everglades Tree Islands, Florida, USA

We address the relative importance of nutrient availability in relation to other physical and biological factors in determining plant community assemblages around Everglades Tree Islands (Everglades National Park, Florida, USA). We carried out a one-time survey of elevation, soil, water level and vegetation structure and composition at 138 plots located along transects in three tree islands in the Park’s major drainage basin. We used an RDA variance partitioning technique to assess the relative importance of nutrient availability (soil N and P) and other factors in explaining herb and tree assemblages of tree island tail and surrounded marshes. The upland areas of the tree islands accumulate P and show low N concentration, producing a strong island-wide gradient in soil N:P ratio. While soil N:P ratio plays a significant role in determining herb layer and tree layer community assemblage in tree island tails, nevertheless part of its variance is shared with hydrology. The total species variance explained by the predictors is very low. We define a strong gradient in nutrient availability (soil N:P ratio) closely related to hydrology. Hydrology and nutrient availability are both factors influencing community assemblages around tree islands, nevertheless both seem to be acting together and in a complex mechanism. Future research should be focused on segregating these two factors in order to determine whether nutrient leaching from tree islands is a factor determining community assemblages and local landscape pattern in the Everglades, and how this process might be affected by water management.

Exploring the role of large predators in marsh food webs: evidence for a behaviorally-mediated trophic cascade

The influence of large predators on lower trophic levels in oligotrophic, structurally complex, and frequently disturbed aquatic environments is generally thought to be limited. We looked for effects of large predators in two semi-permanent, spikerush-dominated marshes by excluding large fish (>12 mm body depth) and similarly sized herpetofauna from 1 m2 cages (exclosures) for 2 weeks. The exclosures allowed for colonization by intermediate (in size and trophic position) consumers, such as small fish, shrimp, and crayfish. Exclosures were compared to control cages that allowed large fish to move freely in and out. At the end of the experiment, intermediate-consumer densities were higher in exclosures than in controls at both sites. Decapod crustaceans, especially the riverine grass shrimp (Palaemonetes paludosus), accounted for the majority of the response. Effects of large fish on shrimp were generally consistent across sites, but per capita effects were sensitive to estimates of predator density. Densities of intermediate consumers in our exclosures were similar to marsh densities, while the open controls had lower densities. This suggests that these animals avoided our experimental controls because they were risky relative to the surrounding environment, while the exclosures were neither avoided nor preferred. Although illuminating about the dynamics of open-cage experiments, this finding does not influence the main results of the study. Small primary consumers (mostly small snails, amphipods, and midges) living on floating periphyton mats and in flocculent detritus (“floc”) were less abundant in the exclosures, indicative of a trophic cascade. Periphyton mat characteristics (i.e., biomass, chlorophyll a, TP) were not clearly or consistently affected by the exclosure, but TP in the floc was lower in exclosures. The collective cascading effects of large predators were consistent at both sites despite differences in drought frequency, stem density, and productivity.

Assessing the net effect of anthropogenic disturbance on aquatic communities in wetlands: community structure relative to distance from canals

Anthropogenic alterations of natural hydrology are common in wetlands and often increase water permanence, converting ephemeral habitats into permanent ones. Since aquatic organisms segregate strongly along hydroperiod gradients, added water permanence caused by canals can dramatically change the structure of aquatic communities. We examined the impact of canals on the abundance and structure of wetland communities in South Florida, USA. We sampled fishes and macroinvertebrates from marsh transects originating at canals in the central and southern Everglades. Density of all aquatic organisms sampled increased in the immediate proximity of canals, but was accompanied by few compositional changes based on analysis of relative abundance. Large fish (>8 cm), small fish (<8 >cm) and macroinvertebrates (>5 mm) increased in density within 5 m of canals. This pattern was most pronounced in the dry season, suggesting that canals may serve as dry-down refugia. Increases in aquatic animal density closely matched gradients of phosphorus enrichment that decreased with distance from canals. Thus, the most apparent impact of canals on adjacent marsh communities was as conduits for nutrients that stimulated local productivity; any impact of their role as sources of increased sources of predators was not apparent. The effect of predation close to canals was overcompensated by increased secondary productivity and/or immigration toward areas adjacent to canals in the dry season. Alternatively, the consumptive effect of predatory fishes using canals as dry-season refuges is very small or spread over the expanse of marshes with open access to canals.

Seasonal fish community variation in headwater mangrove creeks in the southwestern Everglades: an examination of their role as dry-down refuges

The connectivity between the fish community of estuarine mangroves and that of freshwater habitats upstream remains poorly understood. In the Florida Everglades, mangrove-lined creeks link freshwater marshes to estuarine habitats downstream and may act as dry-season refuges for freshwater fishes. We examined seasonal dynamics in the fish community of ecotonal creeks in the southwestern region of Everglades National Park, specifically Rookery Branch and the North and watson rivers. Twelve low-order creeks were sampled via electrofishing, gill nets, and minnow traps during the wet season, transition period, and dry season in 2004-2005. Catches were greater in Rookery Branch than in the North and watson rivers, particularly during the transition period. Community composition varied seasonally in Rookery Branch, and to a greater extent for the larger species, reflecting a pulse of freshwater taxa into creeks as marshes upstream dried periodically. The pulse was short-lived, a later sample showed substantial decreases in freshwater fish numbers. No evidence of a similar influx was seen in the North and watson rivers, which drain shorter hydroperiod marshes and exhibit higher salinities. These results suggest that head-water creeks can serve as important dry-season refugia. Increased freshwater flow resulting from Everglades restoration may enhance this connectivity.

Seagrass ecosystems as a globally significant carbon stock

The protection of organic carbon stored in forests is considered as an important method for mitigating climate change. Like terrestrial ecosystems, coastal ecosystems store large amounts of carbon, and there are initiatives to protect these ‘blue carbon’ stores. Organic carbon stocks in tidal salt marshes and mangroves have been estimated, but uncertainties in the stores of seagrass meadows—some of the most productive ecosystems on Earth—hinder the application of marine carbon conservation schemes. Here, we compile published and unpublished measurements of the organic carbon content of living seagrass biomass and underlying soils in 946 distinct seagrass meadows across the globe. Using only data from sites for which full inventories exist, we estimate that, globally, seagrass ecosystems could store as much as 19.9 Pg organic carbon; according to a more conservative approach, in which we incorporate more data from surface soils and depth-dependent declines in soil carbon stocks, we estimate that the seagrass carbon pool lies between 4.2 and 8.4 Pg carbon. We estimate that present rates of seagrass loss could result in the release of up to 299 Tg carbon per year, assuming that all of the organic carbon in seagrass biomass and the top metre of soils is remineralized.

Across-scale patterning of plant-soil-water interactions surrounding tree islands in Southern Everglades landscapes

The freshwater Everglades is a complex system containing thousands of tree islands embedded within a marsh-grassland matrix. The tree island-marsh mosaic is shaped and maintained by hydrologic, edaphic and biological mechanisms that interact across multiple scales. Preserving tree islands requires a more integrated understanding of how scale-dependent phenomena interact in the larger freshwater system. The hierarchical patch dynamics paradigm provides a conceptual framework for exploring multi-scale interactions within complex systems. We used a three-tiered approach to examine the spatial variability and patterning of nutrients in relation to site parameters within and between two hydrologically defined Everglades landscapes: the freshwater Marl Prairie and the Ridge and Slough. Results were scale-dependent and complexly interrelated. Total carbon and nitrogen patterning were correlated with organic matter accumulation, driven by hydrologic conditions at the system scale. Total and bioavailable phosphorus were most strongly related to woody plant patterning within landscapes, and were found to be 3 to 11 times more concentrated in tree island soils compared to surrounding marshes. Below canopy resource islands in the slough were elongated in a downstream direction, indicating soil resource directional drift. Combined multi-scale results suggest that hydrology plays a significant role in landscape patterning and also the development and maintenance of tree islands. Once developed, tree islands appear to exert influence over the spatial distribution of nutrients, which can reciprocally affect other ecological processes.

Molecular characterization of Cladium peat from the Florida Everglades: biomarker associations with humic fractions

The accumulation and preservation of peat soils in Everglades freshwater marshes and mangrove swamps is an essential process in the ecological functioning of these ecosystems. Human intervention and climate change have modified nutrient dynamics and hydroperiod in the Everglades and peat loss due to such anthropogenic activities is evident. However, not much is known on the molecular level regarding the biogeochemical characteristics, which allow peat to be preserved in the Everglades. Lipid biomarkers trapped within or bound to humic-type structures can provide important geochemical information regarding the origin and microbial transformation of OM in peat. Four lipid fractions obtained from a Cladium peat, namely the freely extractable fraction and those associated with humin, humic acid, and fulvic acid fractions, showed clear differences in their molecular distribution suggesting different OM sources and structural and diagenetic states of the source material. Both, higher plant derived and microbial lipids were found in association with these humic-type substances. Most biomarker distributions suggest an increment in the microbial/terrestrial lipid ratio from the free to humin to humic to fulvic fractions. Microbial reworking of lipids, and the incorporation of microbial biomarkers into the humic-type fractions was evident, as well as the preservation of diagenetic byproducts. The lipid distribution associated with the fulvic acids suggests a high degree of microbial reworking for this fraction. Evidence for this 3D structure was obtained through the presence of the relatively high abundance of α,ω-dicarboxylic acids and phenolic and benzenecarboxylic compounds. The increment in structural complexity of the phenolic and benzencarboxylic compounds in combination with the reduction in the carbon chain length of the dicarboxylic acids from the free to fulvic fraction suggests the latter to be structurally the most stable, compacted and diagenetically altered substrate. This analytical approach can now be applied to peat samples from other areas within the Everglades ecosystem, affected differently by human intervention with the aim to assess changes in organic matter preservation.