Fatty acids and stable isotopes as indicators of early-life feeding and potential maternal resource dependency in the bull shark Carcharhinus leucas

The degree of reliance of newborn sharks on energy reserves from maternal resource allocation and the timescales over which these animals develop foraging skills are critical factors towards understanding the ecological role of top predators in marine ecosystems. We used muscle tissue stable carbon isotopic composition and fatty acid analysis of bull sharks Carcharhinus leucas to investigate early-life feeding ecology in conjunction with maternal resource dependency. Values of δ13C of some young-of-the-year sharks were highly enriched, reflecting inputs from the marine-based diet and foraging locations of their mothers. This group of sharks also contained high levels of the 20:3ω9 fatty acid, which accumulates during periods of essential fatty acid deficiency, suggesting inadequate or undeveloped foraging skills and possible reliance on maternal provisioning. A loss of maternal signal in δ13C values occurred at a length of approximately 100 cm, with muscle tissue δ13C values reflecting a transition from more freshwater/estuarine-based diets to marine-based diets with increasing length. Similarly, fatty acids from sharks >100 cm indicated no signs of essential fatty acid deficiency, implying adequate foraging. By combining stable carbon isotopes and fatty acids, our results provided important constraints on the timing of the loss of maternal isotopic signal and the development of foraging skills in relation to shark size and imply that molecular markers such as fatty acids are useful for the determination of maternal resource dependency.

Patterns and ecosystem consequences of shark declines in the ocean

Whereas many land predators disappeared before their ecological roles were studied, the decline of marine apex predators is still unfolding. Large sharks in particular have experienced rapid declines over the last decades. In this study, we review the documented changes in exploited elasmobranch communities in coastal, demersal, and pelagic habitats, and synthesize the effects of sharks on their prey and wider communities. We show that the high natural diversity and abundance of sharks is vulnerable to even light fishing pressure. The decline of large predatory sharks reduces natural mortality in a range of prey, contributing to changes in abundance, distribution, and behaviour of small elasmobranchs, marine mammals, and sea turtles that have few other predators. Through direct predation and behavioural modifications, top-down effects of sharks have led to cascading changes in some coastal ecosystems. In demersal and pelagic communities, there is increasing evidence of mesopredator release, but cascading effects are more hypothetical. Here, fishing pressure on mesopredators may mask or even reverse some ecosystem effects. In conclusion, large sharks can exert strong top-down forces with the potential to shape marine communities over large spatial and temporal scales. Yet more empirical evidence is needed to test the generality of these effects throughout the ocean.

Mangrove tannins in aquatic ecosystems: Their fate and possible influence on dissolved organic carbon and nitrogen cycling

We describe the fate of mangrove leaf tannins in aquatic ecosystems and their possible influence on dissolved organic nitrogen (DON) cycling. Tannins were extracted and purified from senescent yellow leaves of the red mangrove (Rhizophora mangle) and used for a series of model experiments to investigate their physical and chemical reactivity in natural environments. Physical processes investigated included aggregation, adsorption to organic matter-rich sediments, and co-aggregation with DON in natural waters. Chemical reactions included structural change, which was determined by excitation–emission matrix fluorescence spectra, and the release of proteins from tannin–protein complexes under solar-simulated light exposure. A large portion of tannins can be physically eliminated from aquatic environments by precipitation in saline water and also by binding to sediments. A portion of DON in natural water can coprecipitate with tannins, indicating that mangrove swamps can influence DON cycling in estuarine environments. The chemical reactivity of tannins in natural waters was also very high, with a half-life of less than 1 d. Proteins were released gradually from tannin–protein complexes incubated under light conditions but not under dark conditions, indicating a potentially buffering role of tannin– protein complexes on DON recycling in mangrove estuaries. Although tannins are not detected at a significant level in natural waters, they play an important ecological role by preserving nitrogen and buffering its cycling in estuarine ecosystems through the prevention of rapid DON export/loss from mangrove fringe areas and/or from rapid microbial mineralization.

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.

Diel and seasonal variation in the use of a nearshore sandflat by a ray community in a near pristine system

Knowledge of movements and habitat use is necessary to assess a species’ ecological role and is especially important for mesopredators because they provide the link between upper and lower trophic levels. Using acoustic telemetry, we examined coarse-scale diel and seasonal movements of elasmobranch mesopredators on a shallow sandflat in Shark Bay, Western Australia. Giant shovelnose rays (Glaucostegus typus) and reticulate whiprays (Himantura uarnak) were most often detected in nearshore microhabitats and were regularly detected throughout the day and year, although reticulate whiprays tended to frequent the monitored array over longer periods. Pink whiprays (H. fai) and cowtail stingrays (Pastinachus atrus) were also detected throughout the day, but were far less frequently detected. Overall, there was no apparent spatial or temporal partitioning of the sandflats, but residency to the area varied between species. In addition, ray presence throughout the year suggests that previously observed differences in seasonal abundance are likely because of seasonal changes in habitat use rather than large-scale migrations. Continuous use of the sandflats and limited movements within this ray community suggests that rays have the potential to be a structuring force on this system and that focusing on nearshore habitats is important for managing subtropical ray populations.

Enhanced Growth of Tetracycline-susceptible Soil Bacteria Treated with Iron and Oxytetracycline

Antibiotic resistance has become an important area of research because of the excessive use of antibiotics in clinical and agricultural settings that are driving the evolution of antibiotic resistant bacteria. However, drug tolerance is a naturally occurring phenomenon in soil communities, and is often linked to those soils that are exposed to heavy metals as well as antibiotics. Resistance to antibiotics maybe coupled with resistance to heavy metals in soil bacteria through efflux pumps that can be regulated by iron. Although considered s a heavy metal, iron is an essential component of life that regulates gene expression through the Ferric Uptake Regulator (Fur) protein. This master regulator protein is known to control siderophore production, and other biological pathways. As a suspected controller of biofilm formation, the role of Fur in environmental antibiotic resistance may be greater than is currently realized. In this study, we sought to explore a potential Fur-regulated drug tolerance pathway by understanding the response of soil bacteria when stressed with oxytetracycline and iron. Bacteria were collected from two locations in Miami Dade County. Isolates were first tested using Kirby-Bauer Disk Diffusion tests for antibiotic resistance/susceptibility and identified by 16S rDNA sequencing. A 96-well growth assay was developed to measure planktonic cell growth with 3 mM FeCl3, Oxytetracycline HCl, and the combination treatments. A Microtiter Dish Biofilm Formation Assay was employed and Fur diversity was evaluated. Tetracycline-susceptible bacterial isolates developed drug resistance with iron supplementation, but iron did not enhance biofilm formation. Development of a Fur-dependent drug resistance may be selected for, but further study is required to evaluate Fur evolution in the studied isolates. Gene expression analysis is also needed to further understand the ecological role of Fur and antibiotic resistance.

Multi-Tissue Stable Isotope Analysis and Acoustic Telemetry Reveal Seasonal Variability in the Trophic Interactions of Juvenile Bull Sharks in a Coastal Estuary

Understanding how natural and anthropogenic drivers affect extant food webs is critical to predicting the impacts of climate change and habitat alterations on ecosystem dynamics. In the Florida Everglades, seasonal reductions in freshwater flow and precipitation lead to annual migrations of aquatic taxa from marsh habitats to deep-water refugia in estuaries. The timing and intensity of freshwater reductions, however, will be modified by ongoing ecosystem restoration and predicted climate change. Understanding the importance of seasonally pulsed resources to predators is critical to predicting the impacts of management and climate change on their populations. As with many large predators, however, it is difficult to determine to what extent predators like bull sharks (Carcharhinus leucas) in the coastal Everglades make use of prey pulses currently. We used passive acoustic telemetry to determine whether shark movements responded to the pulse of marsh prey. To investigate the possibility that sharks fed on marsh prey, we modelled the predicted dynamics of stable isotope values in bull shark blood and plasma under different assumptions of temporal variability in shark diets and physiological dynamics of tissue turnover and isotopic discrimination. Bull sharks increased their use of upstream channels during the late dry season, and although our previous work shows long-term specialization in the diets of sharks, stable isotope values suggested that some individuals adjusted their diets to take advantage of prey entering the system from the marsh, and as such this may be an important resource for the nursery. Restoration efforts are predicted to increase hydroperiods and marsh water levels, likely shifting the timing, duration and intensity of prey pulses, which could have negative consequences for the bull shark population and/or induce shifts in behaviour. Understanding the factors influencing the propensity to specialize or adopt more flexible trophic interactions will be an important step in fully understanding the ecological role of predators and how ecological roles may vary with environmental and anthropogenic changes.

Contrasting patterns of individual specialization and trophic coupling in two marine apex predators

1. Apex predators are often assumed to be dietary generalists and, by feeding on prey from multiple basal nutrient sources, serve to couple discrete food webs. But there is increasing evidence that individual level dietary specialization may be common in many species, and this has not been investigated for many marine apex predators. 2. Because of their position at or near the top of many marine food webs, and the possibility that they can affect populations of their prey and induce trophic cascades, it is important to understand patterns of dietary specialization in shark populations. 3. Stable isotope values from body tissues with different turnover rates were used to quantify patterns of individual specialization in two species of ‘generalist’ sharks (bull sharks, Carcharhinus leucas, and tiger sharks, Galeocerdo cuvier). 4. Despite wide population-level isotopic niche breadths in both species, isotopic values of individual tiger sharks varied across tissues with different turnover rates. The population niche breadth was explained mostly by variation within individuals suggesting tiger sharks are true generalists. In contrast, isotope values of individual bull sharks were stable through time and their wide population level niche breadth was explained by variation among specialist individuals. 5. Relative resource abundance and spatial variation in food-predation risk tradeoffs may explain the differences in patterns of specialization between shark species. 6. The differences in individual dietary specialization between tiger sharks and bull sharks results in different functional roles in coupling or compartmentalizing distinct food webs. 7. Individual specialization may be an important feature of trophic dynamics of highly mobile marine top predators and should be explicitly considered in studies of marine food webs and the ecological role of top predators.

A conceptual ecological model to facilitate understanding the role of invasive species in large-scale ecosystem restoration

We developed a conceptual ecological model (CEM) for invasive species to help understand the role invasive exotics have in ecosystem ecology and their impacts on restoration activities. Our model, which can be applied to any invasive species, grew from the eco-regional conceptual models developed for Everglades restoration. These models identify ecological drivers, stressors, effects and attributes; we integrated the unique aspects of exotic species invasions and effects into this conceptual hierarchy. We used the model to help identify important aspects of invasion in the development of an invasive exotic plant ecological indicator, which is described a companion paper in this special issue journal. A key aspect of the CEM is that it is a general ecological model that can be tailored to specific cases and species, as the details of any invasion are unique to that invasive species. Our model encompasses the temporal and spatial changes that characterize invasion, identifying the general conditions that allow a species to become invasive in a de novo environment; it then enumerates the possible effects exotic species may have collectively and individually at varying scales and for different ecosystem properties, once a species becomes invasive. The model provides suites of characteristics and processes, as well as hypothesized causal relationships to consider when thinking about the effects or potential effects of an invasive exotic and how restoration efforts will affect these characteristics and processes. In order to illustrate how to use the model as a blueprint for applying a similar approach to other invasive species and ecosystems, we give two examples of using this conceptual model to evaluate the status of two south Florida invasive exotic plant species (melaleuca and Old World climbing fern) and consider potential impacts of these invasive species on restoration.

Phylogenetic and ecological significance in the evolution of Cetacean tonal sounds

Cetaceans are aquatic mammals that rely primarily on sound for most daily tasks. A compendium of sounds is emitted for orientation, prey detection, and predator avoidance, and to communicate. Communicative sounds are among the most studied Cetacean signals, particularly those referred to as tonal sounds. Because tonal sounds have been studied especially well in social dolphins, it has been assumed these sounds evolved as a social adaptation. However, whistles have been reported in ‘solitary’ species and have been secondarily lost three times in social lineages. Clearly, therefore, it is necessary to examine closely the association, if any, between whistles and sociality instead of merely assuming it. Several hypotheses have been proposed to explain the evolutionary history of Cetacean tonal sounds. The main goal of this dissertation is to cast light on the evolutionary history of tonal sounds by testing these hypotheses by combining comparative phylogenetic and field methods. This dissertation provides the first species-level phylogeny of Cetacea and phylogenetic tests of evolutionary hypotheses of cetacean communicative signals. Tonal sounds evolution is complex in that has likely been shaped by a combination of factors that may influence different aspects of their acoustical structure. At the inter-specific level, these results suggest that only tonal sound minimum frequency is constrained by body size. Group size also influences tonal sound minimum frequency. Species that live in large groups tend to produce higher frequency tonal sounds. The evolutionary history of tonal sounds and sociality may be intertwined, but in a complex manner rejecting simplistic views such as the hypothesis that tonal sounds evolved ‘for’ social communication in dolphins. Levels of social and tonal sound complexity nevertheless correlate indicating the importance of tonal sounds in social communication. At the intraspecific level, tonal sound variation in frequency and temporal parameters may be product of genetic isolation and local levels of underwater noise. This dissertation provides one of the first insights into the evolution of Cetacean tonal sounds in a phylogenetic context, and points out key species where future studies would be valuable to enrich our understanding of other factors also playing a role in tonal sound evolution. ^

Ecological effects of low-level phosphorus additions on two plant communities in a neotropical freshwater wetland ecosystem

We conducted a low-level phosphorus (P) enrichment study in two oligotrophic freshwater wetland communities (wet prairies [WP] and sawgrass marsh [SAW]) of the neotropical Florida Everglades. The experiment included three P addition levels (0, 3.33, and 33.3 mg P m−2 month−1), added over 2 years, and used in situ mesocosms located in northeastern Everglades National Park, Fla., USA. The calcareous periphyton mat in both communities degraded quickly and was replaced by green algae. In the WP community, we observed significant increases in net aboveground primary production (NAPP) and belowground biomass. Aboveground live standing crop (ALSC) did not show a treatment effect, though, because stem turnover rates of Eleocharis spp., the dominant emergent macrophyte in this community, increased significantly. Eleocharis spp. leaf tissue P content decreased with P additions, causing higher C:P and N:P ratios in enriched versus unenriched plots. In the SAW community, NAPP, ALSC, and belowground biomass all increased significantly in response to P additions. Cladium jamaicense leaf turnover rates and tissue nutrient content did not show treatment effects. The two oligotrophic communities responded differentially to P enrichment. Periphyton which was more abundant in the WP community, appeared to act as a P buffer that delayed the response of other ecosystem components until after the periphyton mat had disappeared. Periphyton played a smaller role in controlling ecosystem dynamics and community structure in the SAW community. Our data suggested a reduced reliance on internal stores of P by emergent macrophytes in the WP that were exposed to P enrichment. Eleocharis spp. rapidly recycled P through more rapid aboveground turnover. In contrast, C. jamaicense stored added P by initially investing in belowground biomass, then shifting growth allocation to aboveground tissue without increasing leaf turnover rates. Our results suggest that calcareous wetland systems throughout the Caribbean, and oligotrophic ecosystems in general, respond rapidly to low-level additions of their limiting nutrient.

The Role of the Everglades Mangrove Ecotone Region (EMER) in Regulating Nutrient Cycling and Wetland Productivity in South Florida

The authors summarize the main findings of the Florida Coastal Everglades Long-Term Ecological Research (FCE-LTER) program in the EMER, within the context of the Comprehensive Everglades Restoration Plan (CERP), to understand how regional processes, mediated by water flow, control population and ecosystem dynamics across the EMER landscape. Tree canopies with maximum height <3 m cover 49% of the EMER, particularly in the SE region. These scrub/dwarf mangroves are the result of a combination of low soil phosphorus (P < 59 μg P g dw−1) in the calcareous marl substrate and long hydroperiod. Phosphorus limits the EMER and its freshwater watersheds due to the lack of terrigenous sediment input and the phosphorus-limited nature of the freshwater Everglades. Reduced freshwater delivery over the past 50 years, combined with Everglades compartmentalization and a 10 cm rise in coastal sea level, has led to the landward transgression (1.5 km in 54 years) of the mangrove ecotone. Seasonal variation in freshwater input strongly controls the temporal variation of nitrogen and P exports (99%) from the Everglades to Florida Bay. Rapid changes in nutrient availability and vegetation distribution during the last 50 years show that future ecosystem restoration actions and land use decisions can exert a major influence, similar to sea level rise over the short term, on nutrient cycling and wetland productivity in the EMER.

Potential role of sponge communities in controlling phytoplankton blooms in Florida Bay

An unprecedented series of ecological disturbances have been recurring within Florida Bay since the summer of 1987. Persistent and widespread phytoplankton and cyanobacteria blooms have coincided with the large scale decimation of sponge communities. One hypothesis is that the large scale loss of suspension-feeding sponges has rendered the Florida Bay ecosystem susceptible to these recurring blooms. The primary objective of this study was to experimentally evaluate the potential for suspension-feeding sponges to control nuisance phytoplankton blooms within Florida Bay prior to a large sponge die-off event. To achieve this objective, we determined the extent and biomass of the surviving sponge community in the different basins of Florida Bay. Many areas within Florida Bay possessed sponge densities and biomasses of 1 to 3 ind. m–2 or 100 to 300 g m–2 respectively. The dominant species includedSpheciospongia vesparia, Chondrilla nucula, Cinachyra alloclada, Tedania ignis and Ircinia sp., which accounted for 68% of individual sponges observed and 88% of sponge biomass. Laboratory grazing rates of these dominant sponges were experimentally determined on 4 different algal food treatments: a monoculture of cyanobacteria Synechococcus elongatus, a monoculture of the diatom Cyclotella choctawhatcheeana, a monoculture of the dinoflagellate Prorocentrum hoffmanianum, and an equal volume of the 3 monocultures combined. To estimate the impact of a mass sponge mortality event on the system-wide filtration rate of Florida Bay, we combined estimates of the current sponge biomass and laboratory sponge filtration rates with estimates of mean volumes of the sub-basins of Florida Bay. This study implies that the current blooms occurring within the central region of Florida Bay can be explained by the loss of the dominant suspension feeder in this system, and there is no need to invoke a new addition of nutrients within this region for the blooms to occur.

Phylogenetic and Ecological Significance in the Evolution of Cetacean Tonal Sounds

Cetaceans are aquatic mammals that rely primarily on sound for most daily tasks. A compendium of sounds is emitted for orientation, prey detection, and predator avoidance, and to communicate. Communicative sounds are among the most studied Cetacean signals, particularly those referred to as tonal sounds. Because tonal sounds have been studied especially well in social dolphins, it has been assumed these sounds evolved as a social adaptation. However, whistles have been reported in ‘solitary’ species and have been secondarily lost three times in social lineages. Clearly, therefore, it is necessary to examine closely the association, if any, between whistles and sociality instead of merely assuming it. Several hypotheses have been proposed to explain the evolutionary history of Cetacean tonal sounds. The main goal of this dissertation is to cast light on the evolutionary history of tonal sounds by testing these hypotheses by combining comparative phylogenetic and field methods. This dissertation provides the first species-level phylogeny of Cetacea and phylogenetic tests of evolutionary hypotheses of cetacean communicative signals. Tonal sounds evolution is complex in that has likely been shaped by a combination of factors that may influence different aspects of their acoustical structure. At the inter-specific level, these results suggest that only tonal sound minimum frequency is constrained by body size. Group size also influences tonal sound minimum frequency. Species that live in large groups tend to produce higher frequency tonal sounds. The evolutionary history of tonal sounds and sociality may be intertwined, but in a complex manner rejecting simplistic views such as the hypothesis that tonal sounds evolved ‘for’ social communication in dolphins. Levels of social and tonal sound complexity nevertheless correlate indicating the importance of tonal sounds in social communication. At the intraspecific level, tonal sound variation in frequency and temporal parameters may be product of genetic isolation and local levels of underwater noise. This dissertation provides one of the first insights into the evolution of Cetacean tonal sounds in a phylogenetic context, and points out key species where future studies would be valuable to enrich our understanding of other factors also playing a role in tonal sound evolution.