Non-consumptive effects of predators in coral reef communities and the indirect consequences of marine protected areas

Predators exert strong direct and indirect effects on ecological communities by intimidating their prey. Non-consumptive effects (NCEs) of predators are important features of many ecosystems and have changed the way we understand predator-prey interactions, but are not well understood in some systems. For my dissertation research I combined a variety of approaches to examine the effect of predation risk on herbivore foraging and reproductive behaviors in a coral reef ecosystem. In the first part of my dissertation, I investigated how diet and territoriality of herbivorous fish varied across multiple reefs with different levels of predator biomass in the Florida Keys National Marine Sanctuary. I show that both predator and damselfish abundance impacted diet diversity within populations for two herbivores in different ways. Additionally, reef protection and the associated recovery of large predators appeared to shape the trade-off reef herbivores made between territory size and quality. In the second part of my dissertation, I investigated context-dependent causal linkages between predation risk, herbivore foraging behavior and resource consumption in multiple field experiments. I found that reef complexity, predator hunting mode, light availability and prey hunger influenced prey perception of threat and their willingness to feed. This research argues for more emphasis on the role of predation risk in affecting individual herbivore foraging behavior in order to understand the implications of human-mediated predator removal and recovery in coral reef ecosystems.^

Non-Consumptive Effects of Predators in Coral Reef Communities and the Indirect Consequences of Marine Protected Areas

Predators exert strong direct and indirect effects on ecological communities by intimidating their prey. Non-consumptive effects (NCEs) of predators are important features of many ecosystems and have changed the way we understand predator-prey interactions, but are not well understood in some systems. For my dissertation research I combined a variety of approaches to examine the effect of predation risk on herbivore foraging and reproductive behaviors in a coral reef ecosystem. In the first part of my dissertation, I investigated how diet and territoriality of herbivorous fish varied across multiple reefs with different levels of predator biomass in the Florida Keys National Marine Sanctuary. I show that both predator and damselfish abundance impacted diet diversity within populations for two herbivores in different ways. Additionally, reef protection and the associated recovery of large predators appeared to shape the trade-off reef herbivores made between territory size and quality. In the second part of my dissertation, I investigated context-dependent causal linkages between predation risk, herbivore foraging behavior and resource consumption in multiple field experiments. I found that reef complexity, predator hunting mode, light availability and prey hunger influenced prey perception of threat and their willingness to feed. This research argues for more emphasis on the role of predation risk in affecting individual herbivore foraging behavior in order to understand the implications of human-mediated predator removal and recovery in coral reef ecosystems.

Density-Dependent Effects of Coral Reef Restoration on Herbivory and Community Interactions

Coral reefs are among the most productive ecosystems in the world. Yet, with their recent declines due to disease, climate change, and overfishing, restoration of these habitats is one of the main concerns for ecologists, resource managers, and government organizations. Coral reef restoration aims to promote key ecosystem processes to shift these habitats to their historical state of high coral cover, but few studies have focused on effective ways to promote resilience. In addition, little is known about the impact of restoration on the fish communities. The aim of this study is to understand how the community of herbivorous fishes is affected by the density of coral outplants inside a special protection area located in the Florida Keys National Marine Sanctuary. Grazing rates, number of visits and time spent foraging were compared using video footage of sites previously devoid of corals, and six months after coral restorations had occurred. Coral transplantations did not appear to attract herbivores nor increase grazing rates of fishes. Instead Sparisoma and Acanthurus fishes appear to respond to changes in the environment by modifying their grazing behavior. However, there was an observed increase in visits by Acanthurus species after transplantation for all the sites sampled within the reef. These fishes seemed to prefer low coral cover sites for grazing. This study highlights the importance of examining coral restorations impacts at the community level. Understanding how restoration influences herbivores and other guilds of reef fishes will allow individuals to not only determine if these habitats are returning to their “original” state, but provide more information on the ways these systems cope with changes in the environment.

A Comparative Study of Concurrent Acoustic and Diver Survey Data, and Fish Community Descriptions of a High Latitude Coral Reef, Florida, USA

Fisheries independent data on relatively unstudied nekton communities were used to explore the efficacy of new tools to be applied in the investigation of shallow coastal coral reef habitats. These data obtained through concurrent diver visual and acoustic surveys provided descriptions of spatial community distribution patterns across seasonal temporal scales in a previously undocumented region. Fish density estimates by both diver and acoustic methodologies showed a general agreement in ability to detect distributional patterns across reef tracts, though magnitude of density estimates were different. Fish communities in southeastern Florida showed significant trends in spatial distribution and seasonal abundance, with higher estimates of biomass obtained in the dry season. Further, community composition shifted across reef tracts and seasons as a function of the movements of several key reef species.

Effects of Multiple Ecological Drivers on Recruitment and Succession of Coral Reef Macroalgal Communities

The study evaluated the effects of herbivory pressure, nutrient availability and potential propagule supply on recruitment and succession of coral reef macroalgal communities. Recruitment and succession tiles were placed in a nutrient-herbivory factorial experiment and macroalgal abundances were evaluated through time. Proportional abundances of macroalgal form-functional groups on recruitment and succession tiles were similar to field established communities within treatments, evidencing possible effects of adult macroalgae as propagule supply. Macroalgal abundance of recruitment tiles increased with nutrient loading and herbivory reduction combined whereas on succession tiles nutrient loading increased abundance of articulated-calcareous only when herbivores were excluded. Macroalgal field established communities were only affected by herbivory reduction.

Biogeochemical Contributions of Tree Islands to Everglades Wetland Landscape Nitrogen Cycling During Seasonal Inundation

In the Florida Everglades, tree islands are conspicuous heterogeneous elements in the herbaceous wetland landscape. We characterized the biogeochemical role of a seasonally flooded tree island during wet season inundation, specifically examining hydrologically mediated flows of nitrogen (N) and N retention by the tree island. We estimated ecosystem N standing stocks and fluxes, soil and litter N transformation rates, and hydrologic fluxes of N to quantify the net ecosystem N mass flux. Results showed that hydrologic sources of N were dominated by surface water loads of nitrate (NO3) and ammonium (NH4). Nitrate immobilization by soils and surficial leaf litter was an important sink for surface water dissolved inorganic N (DIN). We estimated that the net annual DIN retention by a seasonally flooded tree island was 20.5 ± 5.0 g m−2 during wet season inundation. Based on the estimated tree island surface water DIN loading rate, a seasonally flooded tree island retained 76% of imported DIN. As such, seasonally flooded tree islands have the potential to retain 55% of DIN entering the marsh landscape via upstream canal overland flow in the wet season. By increasing reactive surface area and DOC availability, we suggest that tree islands promote convergence of elements that enhance DIN retention. Tree islands of this region are thus important components of landscape-scale restoration efforts that seek to reduce sources of anthropogenic DIN to downstream estuaries.

A Geospatial Database of Tree Islands within the Mustang Corner Fire Incident of 2008

Fire, which affects community structure and composition at all trophic levels, is an integral component of the Everglades ecosystem (Wade et al. 1980; Lockwood et al. 2003). Without fire, the Everglades as we know it today would be a much different place. This is particularly true for the short-hydroperiod marl prairies that predominate on the eastern and western flanks of Shark River Slough, Everglades National Park (Figure 1). In general, fire in a tropical or sub-tropical grassland community favors the dominance of C4 grasses over C3 species (Roscoe et al. 2000; Briggs et al. 2005). Within this pyrogenic graminoid community also, periodic natural fires, together with suitable hydrologic regime, maintain and advance the dominance of C4 vs C3 graminoids (Sah et al. 2008), and suppress the encroachment of woody stems (Hanan et al. 2009; Hanan et al. unpublished manuscript) originating from the tree islands that, in places, dominate the landscape within this community. However, fires, under drought conditions and elevated fuel loads, can spread quickly throughout the landscape, oxidizing organic soils, both in the prairie and in the tree islands, and, in the process, lead to shifts in vegetation composition. This is particularly true when a fire immediately precedes a flood event (Herndon et al. 1991; Lodge 2005; Sah et al. 2010), or if so much soil is consumed during the fire that the hydrologic regime is permanently altered as a result of a decrease in elevation (Zaffke 1983).

Investigating Stakeholders’ Preferences for Coral Reef Research Funding in Florida

Abstract: Heavily used and highly valuable, the Florida Reef is one of the world's most threatened ecosystems. Stakeholders from a densely urbanized coastal region in proximity to the reef system recognize its degradation, but their comprehension of climate change and commitment to pay for sustainable management and research funding have been opaque. With an emphasis on recreational anglers, residential stakeholders were surveyed online about their marine activities, perceptions of resources and threats, and willingness to pay (WTP) for dedicated coral reef research funding in Florida. The majority of stakeholders are wealthy, well educated, and politically independent. Supermajorities favored the two scenarios of taxation for a Florida Coral Reef Research Fund, and the scenario with matching federal funds earned higher support. In regression analyses, several factors emerged as significant contributors to stakeholders’ preferences, and the four recurring factors in extended models were prioritizing the environment over the economy, donating to environmental causes, concern about coral reefs, and concern about climate change, with the latter indicating a recent shift of opinion. Status in terms of income and education were found insignificant, and surprisingly income was negatively correlated with WTP. Perceptions through lenses of environmental and emotional attachments appear to overwhelm conventional status-based factors. Applied statewide, the first scenario's extrapolated WTP (based on a sales tax rate of 2.9%) would generate $675 million annually, and the extrapolated WTP under the second scenario, with matching federal funds (based on a sales tax rate of 3.0%) would generate $1.4 billion. Keywords: willingness to pay, coral reef research, taxation, climate change, stakeholder, perceptions, Florida Reef, recreational fishing, anglers

Herbivore and nutrient impact on primary producer assemblages in a tropical marine environment

Globally, human populations are increasing and coastal ecosystems are becoming increasingly impacted by anthropogenic stressors. As eutrophication and exploitation of coastal resources increases, primary producer response to these drivers becomes a key indicator of ecosystem stability. Despite the importance of monitoring primary producers such as seagrasses and macroalgae, detailed studies on the response of these benthic habitat components to drivers remain relatively sparse. Utilizing a multi-faceted examination of turtle-seagrass and sea urchin-macroalgae consumer and nutrient dynamics, I elucidate the impact of these drivers in Akumal, Quintana Roo, Mexico. In Yal Ku Lagoon, macroalgae bioindicators signified high nutrient availability, which is important for further studies, but did not consistently follow published trends reflecting decreased δ 15N content with distance from suspected source. In Akumal Bay, eutrophication and grazing by turtles and fishes combine to structure patches within the seagrass beds. Grazed seagrass patches had higher structural complexity and productivity than patches continually grazed by turtles and fishes. Results from this study indicate that patch abandonment may follow giving-up density theory, the first to be recorded in the marine environment. As Diadema antillarum populations recover after their massive mortality thirty years ago, the role these echinoids will have in reducing macroalgae cover and altering ecosystem state remains to be clear. Although Diadema antillarum densities within the coral reef ecosystem were comparable to other regions within the Caribbean, the echinoid population in Akumal Bay was an insufficient driver to prevent dominance of a turf-algal-sediment (TAS) state. After a four year study, declining coral cover coupled with increased algal cover suggests that the TAS-dominated state is likely to persist over time despite echinoid recovery. Studies on macroalgal diversity and nutrients within this same region of echinoids indicated diversity and nutrient content of macroalgae increased, which may further increase the persistence of the algal-dominated state. This study provides valuable insight into the variable effects of herbivores and nutrients on primary producers within a tropical coastal ecosystem. Results from this work challenge many of the currently accepted theories on primary producer response to nutrients and herbivory while providing a framework for further studies into these dynamics.

Regional climate gradients in precipitation and temperature in response to climate teleconnections in the Greater Everglades ecosystem of South Florida

Precipitation and temperature in Florida responds to climate teleconnections from both the Pacific and Atlantic regions. In this region south of Lake Okeechobee, encompassing NWS Climate Divisions 5, 6, and 7, modern movement of surface waters are managed by the South Florida Water Management District and the US Army Corps of Engineers for flood control, water supply, and Everglades restoration within the constraints of the climatic variability of precipitation and evaporation. Despite relatively narrow, low-relief, but multi-purposed land separating the Atlantic Ocean from the Gulf of Mexico, South Florida has patterns of precipitation and temperature that vary substantially on spatial scales of 101–102 km. Here we explore statistically significant linkages to precipitation and temperature that vary seasonally and over small spatial scales with El Niño-Southern Oscillation (ENSO), the Atlantic Multidecadal Oscillation (AMO), and the Pacific Decadal Oscillation (PDO). Over the period from 1952 to 2005, ENSO teleconnections exhibited the strongest influence on seasonal precipitation. The Multivariate ENSO Index was positively correlated with winter (dry season) precipitation and explained up to 34 % of dry season precipitation variability along the southwest Florida coast. The AMO was the most influential of these teleconnections during the summer (wet season), with significant positive correlations to South Florida precipitation. These relationships with modern climate parameters have implications for paleoclimatological and paleoecological reconstructions, and future climate predictions from the Greater Everglades system.

Compositional Effects of Sea-Level Rise in a Patchy Landscape: The Dynamics of Tree Islands in the Southeastern Coastal Everglades

The landscape structure of emergent wetlands in undeveloped portions of the southeastern coastal Everglades is comprised of two distinct components: scattered forest fragments, or tree islands, surrounded by a low matrix of marsh or shrub-dominated vegetation. Changes in the matrix, including the inland transgression of salt-tolerant mangroves and the recession of sawgrass marshes, have been attributed to the combination of sea level rise and reductions in fresh water supply. In this study we examined concurrent changes in the composition of the region’s tree islands over a period of almost three decades. No trend in species composition toward more salt-tolerant trees was observed anywhere, but species characteristic of freshwater swamps increased in forests in which fresh water supply was augmented. Tree islands in the coastal Everglades appear to be buffered from some of the short term effects of salt water intrusion, due to their ability to build soils above the surface of the surrounding wetlands, thus maintaining mesophytic conditions. However, the apparent resistance of tree islands to changes associated with sea level rise is likely to be a temporary stage, as continued salt water intrusion will eventually overwhelm the forests’ capacity to maintain fresh water in the rooting zone.

Ecosystem responses to hydrologic change and mechanisms of nitrogen sequestration in seasonally flooded tree islands of the southern Everglades

In the Florida Everglades, tree islands are conspicuous heterogeneous elements in a complex wetland landscape. I investigated the effects of increased freshwater flow in southern Everglades seasonally flooded tree islands, and characterized biogeochemical interactions among tree islands and the marsh landscape matrix, specifically examining hydrologic flows of nitrogen (N), and landscape N sequestration capacity. I utilized ecological trajectories of key ecosystem variables to differentiate effects of increased sheetflow and hydroperiod. I utilized stable isotope analyses and nutrient content of tree island ecosystem components to test the hypothesis that key processes in tree island nitrogen cycling would favor ecosystem N sequestration. I combined estimates of tree island ecosystem N standing stocks and fluxes, soil and litter N transformation rates, and hydrologic inputs of N to quantify the net sequestration of N by a seasonally flooded tree island. ^ Results show that increased freshwater flow to seasonally flooded tree islands promoted ecosystem oligotrophy, whereas reduced flows allowed some plant species to cycle P less efficiently. As oligotrophy is a defining parameter of Everglades wetlands, and likely promotes belowground production and peat development, reintroducing freshwater flow from an upstream canal had a favorable effect on ecosystem dynamics of tree islands in the study area. Important factors influencing the stable isotopic composition of nitrogen and carbon were: (1) a contribution to soil N by soil invertebrates, animal excrement, and microbes, (2) a possible NO3 source from an upstream canal and an "open" ecosystem N cycle, and (3) greater availability of phosphorus in tree islands relative to the marsh landscape, suggesting that tree island N cycling favors N sequestration. Hydrologic sources of N were dominated by surface water loads of NO3- and NH 4+, and an important soil N transformation promoting the net loss of surface water DIN was nitrate immobilization associated with soils and surficial leaf litter. The net inorganic N sequestration capacity of a seasonally flooded tree island was 50 g yr-1 m -2. Thus, tree islands likely have an important function in landscape sequestration of inorganic N, and may reduce significant anthropogenic N loads to downstream coastal systems. ^

Specificity, stability and comparative physiology of coral-Symbiodinium mutualisms: Evaluating the potential for acclimation and/or adaptation in reef corals

The relationship between reef corals and endosymbiotic dinoflagellates is fundamental to the existence of coral reefs. To evaluate the fidelity of coral-Symbiodinium mutualisms, corals maintained in aquaria for years were analyzed by denaturant gradient gel electrophoresis (DGGE). Comparing Symbiodinium populations of captive aquarium colonies with known associations in nature is a practical way of examining partner flexibility. The finding of "normal" symbiont populations in corals existing under highly variable conditions supports the premise that most coral colonies possess stable associations. High sensitivity real-time PCR (rtPCR) was used to evaluate background populations of the putatively stress-tolerant Symbiodinium D in reef corals of the Caribbean. Analyses of samples collected during periods of environmental stability indicate the ability of Symbiodinium D to associate with a wider diversity of host taxa than previously recognized. To gain a broader perspective with regard to the ecology of Symbiodinium D1a, rtPCR and DGGE were used to evaluate the symbiont populations of reef corals from Barbados before and after the 2005 mass coral bleaching. Background populations were observed in 56% of the host genera prior to observations of bleaching. These findings indicate that 'stress', not 'bleaching', caused the displacement of 'natural' symbiont population and the opportunistic proliferation of D1a in many host taxa. Of the 12 host taxa monitored before and after the bleaching event, there was a 40% increase in colonies hosting Symbiodinium D1a. Together, these studies elucidate the mechanism responsible for recent observations reporting the emergence of Symbiodinium D following thermal disturbances. These observations are now most easily explained as the disproportionate growth of existing in hospite symbiont populations, rather than novel symbiont acquisition subsequent to bleaching. To evaluate the comparative "fitness" of corals able to host multiple symbiont types, rates of calcification were measured in P. verrucosa hosting either Symbiodinium C1b-c or D1 at elevated temperature. Rates of calcification decreased significantly for both host-symbiont combinations, but differences attributable to symbiont composition were not detected. This research improves our knowledge of the symbiosis biology and ecology of reef corals and contributes information necessary to most accurately predict the response of these ecosystems to global climate changes.

Ecosystem structure, nutrient dynamics, and hydrologic relationships in tree islands of the southern Everglades, Florida, USA

Tree islands are an important structural component of many graminoid-dominated wetlands because they increase ecological complexity in the landscape. Tree island area has been drastically reduced with hydrologic modifications within the Everglades ecosystem, yet still little is known about the ecosystem ecology of Everglades tree islands. As part of an ongoing study to investigate the effects of hydrologic restoration on short hydroperiod marshes of the southern Everglades, we report an ecosystem characterization of seasonally flooded tree islands relative to locations described by variation in freshwater flow (i.e. locally enhanced freshwater flow by levee removal). We quantified: (1) forest structure, litterfall production, nutrient utilization, soil dynamics, and hydrologic properties of six tree islands and (2) soil and surface water physico-chemical properties of adjacent marshes. Tree islands efficiently utilized both phosphorus and nitrogen, but indices of nutrient-use efficiency indicated stronger P than N limitation. Tree islands were distinct in structure and biogeochemical properties from the surrounding marsh, maintaining higher organically bound P and N, but lower inorganic N. Annual variation resulting in increased hydroperiod and lower wet season water levels not only increased nitrogen use by tree species and decreased N:P values of the dominant plant species (Chrysobalanus icaco), but also increased soil pH and decreased soil temperature. When compared with other forested wetlands, these Everglades tree islands were among the most nutrient efficient, likely a function of nutrient immobilization in soils and the calcium carbonate bedrock. Tree islands of our study area are defined by: (1) unique biogeochemical properties when compared with adjacent short hydroperiod marshes and other forested wetlands and (2) an intricate relationship with marsh hydrology. As such, they may play an important and disproportionate role in nutrient and carbon cycling in Everglades wetlands. With the loss of tree islands that has occurred with the degradation of the Everglades system, these landscape processes may have been altered. With this baseline dataset, we have established a long-term ecosystem-scale experiment to follow the ecosystem trajectory of seasonally flooded tree islands in response to hydrologic restoration of the southern Everglades.