Indirect and direct controls of macroinvertebrates and small fish by abiotic factors and trophic interactions in the Florida Everglades

1. The roles of nutrients, disturbance and predation in regulating consumer densities have long been of interest, but their indirect effects have rarely been quantified in wetland ecosystems. The Florida Everglades contains gradients of hydrological disturbance (marsh drying) and nutrient enrichment (phosphorus), often correlated with densities of macroinvertebrate infauna (macroinvertebrates inhabiting periphyton), small fish and larger invertebrates, such as snails, grass shrimp, insects and crayfish. However, most causal relationships have yet to be quantified. 2.  We sampled periphyton (content and community structure) and consumer (small omnivores, carnivores and herbivores, and infaunal macroinvertebrates inhabiting periphyton) density at 28 sites spanning a range of hydrological and nutrient conditions and compared our data to seven a priori structural equation models. 3.  The best model included bottom-up and top-down effects among trophic groups and supported top-down control of infauna by omnivores and predators that cascaded to periphyton biomass. The next best model included bottom-up paths only and allowed direct effects of periphyton on omnivore density. Both models suggested a positive relationship between small herbivores and small omnivores, indicating that predation was unable to limit herbivore numbers. Total effects of time following flooding were negative for all three consumer groups even when both preferred models suggested positive direct effects for some groups. Total effects of nutrient levels (phosphorus) were positive for consumers and generally larger than those of hydrological disturbance and were mediated by changes in periphyton content. 4.  Our findings provide quantitative support for indirect effects of nutrient enrichment on consumers, and the importance of both algal community structure and periphyton biomass to Everglades food webs. Evidence for top-down control of infauna by omnivores was noted, though without substantially greater support than a competing bottom-up-only model.

Top down control in a relatively pristine seagrass ecosystem

The loss of large-bodied herbivores and/or top predators has been associated with large-scale changes in terrestrial, freshwater, and marine ecosystems around the world. Understanding the consequences of these declines has been hampered by a lack of studies in relatively pristine systems. To fill this gap, I investigated the dynamics of the relatively pristine seagrass ecosystem of Shark Bay, Australia. I began by examining the seagrass species distributions, stoichiometry, and patterns of nutrient limitation across the whole of Shark Bay. Large areas were N-limited, P-limited, or limited by factors other than nutrients. Phosphorus-limitation was centered in areas of restricted water exchange with the ocean. Nutrient content of seagrasses varied seasonally, but the strength of seasonal responses were species-specific. Using a cafeteria-style experiment, I found that fast-growing seagrass species, which had higher nutrient content experienced higher rates of herbivory than slow-growing species that are dominant in the bay but have low nutrient content. Although removal rates correlated well with nutrient content at a broad scale, within fast-growing species removal rates were not closely tied to N or P content. Using a combination of stable isotope analysis and animal borne video, I found that green turtles (Chelonia mydas)—one of the most abundant large-bodied herbivores in Shark Bay—appear to assimilate little energy from seagrasses at the population level. There was, however, evidence of individual specialization in turtle diets with some individuals foraging largely on seagrasses and others feeding primarily on macroalgae and gelatinous macroplankton. Finally, I used exclusion cages, to examine whether predation-sensitive habitat shifts by megagrazers (green turtles, dugongs) transmitted a behavior-mediated trophic cascade (BMTC) between sharks and seagrasses. In general, data were consistent with predictions of a behavior-mediated trophic cascade. Megaherbivore impacts on seagrasses were large only in the microhabitat where megaherbivores congregate to reduce predation risk. My study highlights the importance of large herbivores in structuring seagrass communities and, more generally, suggests that roving top predators likely are important in structuring communities—and possibly ecosystems—through non-consumptive pathways.

Microhabitat Selection by Marine Mesoconsumers in a Thermally Heterogeneous Habitat: Behavioral Thermoregulation or Avoiding Predation Risk?

Habitat selection decisions by consumers has the potential to shape ecosystems. Understanding the factors that influence habitat selection is therefore critical to understanding ecosystem function. This is especially true of mesoconsumers because they provide the link between upper and lower tropic levels. We examined the factors influencing microhabitat selection of marine mesoconsumers – juvenile giant shovelnose rays (Glaucostegus typus), reticulate whiprays (Himantura uarnak), and pink whiprays (H. fai) – in a coastal ecosystem with intact predator and prey populations and marked spatial and temporal thermal heterogeneity. Using a combination of belt transects and data on water temperature, tidal height, prey abundance, predator abundance and ray behavior, we found that giant shovelnose rays and reticulate whiprays were most often found resting in nearshore microhabitats, especially at low tidal heights during the warm season. Microhabitat selection did not match predictions derived from distributions of prey. Although at a course scale, ray distributions appeared to match predictions of behavioral thermoregulation theory, fine-scale examination revealed a mismatch. The selection of the shallow nearshore microhabitat at low tidal heights during periods of high predator abundance (warm season) suggests that this microhabitat may serve as a refuge, although it may come with metabolic costs due to higher temperatures. The results of this study highlight the importance of predators in the habitat selection decisions of mesoconsumers and that within thermal gradients, factors, such as predation risk, must be considered in addition to behavioral thermoregulation to explain habitat selection decisions. Furthermore, increasing water temperatures predicted by climate change may result in complex trade-offs that might have important implications for ecosystem dynamics.

The role of teleost grazers in a relatively pristine seagrass ecosystem

Trophic downgrading of ecosystems necessitates a functional understanding of trophic cascades. Identifying the presence of cascades, and the mechanisms through which they occur, is particularly important for seagrass meadows, which are among the most threatened ecosystems on Earth. Shark Bay, Western Australia provides a model system to investigate the potential importance of top-down effects in a relatively pristine seagrass ecosystem. The role of megagrazers in the Shark Bay system has been previously investigated, but the role of macrograzers (i.e., teleosts), and their importance relative to megagrazers, remains unknown. The objective of my dissertation was to elucidate the importance of teleost macrograzers in transmitting top-down effects in seagrass ecosystems. Seagrasses and macroalgae were the main food of the abundant teleost Pelates octolineatus, but stable isotopic values suggested that algae may contribute a larger portion of assimilated food than suggested by gut contents. Pelates octolineatus is at risk from numerous predators, with pied cormorants (Phalacrocorax varius) taking the majority of tethered P. octolineatus. Using a combination of fish trapping and unbaited underwater video surveillance, I found that the relative abundance of P. octolineatus was greater in interior areas of seagrass banks during the cold season, and that the mean length of P. octolineatus was greater in these areas compared to along edges of banks. Finally, I used seagrass transplants and exclosure experiments to determine the relative effect of megagrazers and macrograzers on the establishment and persistence of three species of seagrasses in interior microhabitats. Teleost grazing had the largest impact on seagrass species with the highest nutrient content, and these impacts were primarily observed during the warm season. My findings are consistent with predictions of a behaviorally-mediated trophic cascade initiated by tiger sharks (Galeocerdo cuvier) and transmitted through herbivorous fishes and their predators.

Factors influencing movements and foraging ecology of American alligators (Alligator mississippiensis) in a dynamic subtropical coastal ecosystem

Top predators can have large effects on community and population dynamics but we still know relatively little about their roles in ecosystems and which biotic and abiotic factors potentially affect their behavioral patterns. Understanding the roles played by top predators is a pressing issue because many top predator populations around the world are declining rapidly yet we do not fully understand what the consequences of their potential extirpation could be for ecosystem structure and function. In addition, individual behavioral specialization is commonplace across many taxa, but studies of its prevalence, causes, and consequences in top predator populations are lacking. In this dissertation I investigated the movement, feeding patterns, and drivers and implications of individual specialization in an American alligator (Alligator mississippiensis ) population inhabiting a dynamic subtropical estuary. I found that alligator movement and feeding behaviors in this population were largely regulated by a combination of biotic and abiotic factors that varied seasonally. I also found that the population consisted of individuals that displayed an extremely wide range of movement and feeding behaviors, indicating that individual specialization is potentially an important determinant of the varied roles of alligators in ecosystems. Ultimately, I found that assuming top predator populations consist of individuals that all behave in similar ways in terms of their feeding, movements, and potential roles in ecosystems is likely incorrect. As climate change and ecosystem restoration and conservation activities continue to affect top predator populations worldwide, individuals will likely respond in different and possibly unexpected ways.

Perceived Risk of Predation Affects Reproductive Life - History Traits in Gambusia holbrooki, but Not in Heterandria formosa

Key to predicting impacts of predation is understanding the mechanisms through which predators impact prey populations. While consumptive effects are well-known, non-consumptive predator effects (risk effects) are increasingly being recognized as important. Studies of risk effects, however, have focused largely on how trade-offs between food and safety affect fitness. Less documented, and appreciated, is the potential for predator presence to directly suppress prey reproduction and affect life-history characteristics. For the first time, we tested the effects of visual predator cues on reproduction of two prey species with different reproductive modes, lecithotrophy (i.e. embryonic development primarily fueled by yolk) and matrotrophy (i.e. energy for embryonic development directly supplied by the mother to the embryo through a vascular connection). Predation risk suppressed reproduction in the lecithotrophic prey (Gambusia holbrokii) but not the matrotroph (Heterandria formosa). Predator stress caused G. holbrooki to reduce clutch size by 43%, and to produce larger and heavier offspring compared to control females. H. formosa, however, did not show any such difference. In G. holbrooki we also found a significantly high percentage (14%) of stillbirths in predator-exposed treatments compared to controls (2%). To the best of our knowledge, this is the first direct empirical evidence of predation stress affecting stillbirths in prey. Our results suggest that matrotrophy, superfetation (clutch overlap), or both decrease the sensitivity of mothers to environmental fluctuation in resource (food) and stress (predation risk) levels compared to lecithotrophy. These mechanisms should be considered both when modeling consequences of perceived risk of predation on prey-predator population dynamics and when seeking to understand the evolution of reproductive modes.

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.

Effects of an extreme temperature event on the behavior and age structure of an estuarine top predator, Carcharhinus leucas

The frequency of extreme environmental events is predicted to increase in the future. Understanding the short- and long-term impacts of these extreme events on large-bodied predators will provide insight into the spatial and temporal scales at which acute environmental disturbances in top-down processes may persist within and across ecosystems. Here, we use long-term studies of movements and age structure of an estuarine top predator—juvenile bull sharks Carcharhinus leucas—to identify the effects of an extreme ‘cold snap’ from 2 to 13 January 2010 over short (weeks) to intermediate (months) time scales. Juvenile bull sharks are typically year-round residents of the Shark River Estuary until they reach 3 to 5 yr of age. However, acoustic telemetry revealed that almost all sharks either permanently left the system or died during the cold snap. For 116 d after the cold snap, no sharks were detected in the system with telemetry or captured during longline sampling. Once sharks returned, both the size structure and abundance of the individuals present in the nursery had changed considerably. During 2010, individual longlines were 70% less likely to capture any sharks, and catch rates on successful longlines were 40% lower than during 2006−2009. Also, all sharks caught after the cold snap were young-of-the-year or neonates, suggesting that the majority of sharks in the estuary were new recruits and several cohorts had been largely lost from the nursery. The longer-term impacts of this change in bull shark abundance to the trophic dynamics of the estuary and the importance of episodic disturbances to bull shark population dynamics will require continued monitoring, but are of considerable interest because of the ecological roles of bull sharks within coastal estuaries and oceans.

Intra-Population Variation in Activity Ranges, Diel Patterns, Movement Rates, and Habitat Use of American Alligators in a Subtropical Estuary

Movement and habitat use patterns are fundamental components of the behaviors of mobile animals and help determine the scale and types of interactions they have with their environments. These behaviors are especially important to quantify for top predators because they can have strong effects on lower trophic levels as well as the wider ecosystem. Many studies of top predator movement and habitat use focus on general population level trends, which may overlook important intra-population variation in behaviors that now appear to be common. In an effort to better understand the prevalence of intra-population variation in top predator movement behaviors and the potential effects of such variation on ecosystem dynamics, we examined the movement and habitat use patterns of a population of adult American alligators (Alligator mississippiensis) in a subtropical estuary for nearly four years. We found that alligators exhibited divergent behaviors with respect to activity ranges, movement rates, and habitat use, and that individualized behaviors were stable over multiple years. We also found that the variations across the three behavioral metrics were correlated such that consistent behavioral types emerged, specifically more exploratory individuals and more sedentary individuals. Our study demonstrates that top predator populations can be characterized by high degrees of intra-population variation in terms of movement and habitat use behaviors that could lead to individuals filling different ecological roles in the same ecosystem. By extension, one-size-fits-all ecosystem and species-specific conservation and management strategies that do not account for potential intra-population variation in top predator behaviors may not produce the desired outcomes in all cases.

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.

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.

Mosquito larvicides from cyanobacteria

Cyanobacteria (blue-green algae) produce a diverse array of toxic or otherwise bioactive metabolites. These allelochemicals may also play a role in defense against potential predators and grazers, particularly aquatic invertebrates and their larvae, including mosquitoes. Compounds derived from cyanobacteria collected from the Florida Everglades and other Florida waterways were investigated as insecticides against the mosquito Aedes aegypti, a vector of dengue and yellow fever. Screening of cyanobacterial biomass revealed several strains that exhibited mosquito larvicidal activity. Guided via bioassay guided fractionation, a non-polar compound from Leptolyngbya sp. 21-9-3 was found to be the most active component. Characterization revealed the prospective compound to be a monounsaturated fatty acid with the molecular formula C16H30O2. This is the first evidence of mosquito larvicidal activity for this particular fatty acid. With larvicidal becoming more prevalent, fatty acids should be explored for future mosquito control strategies.^

Using stable isotopes to investigate trophic interactions of bottlenose dolphins (Tursiops truncatus) in the Florida Coastal Everglades

Top predators are known for their ability to 1) affect their communities through predation and 2) induce behavioral modifications. Recent research suggests that they may also play “bottom-up” roles in ecosystems, including 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. Therefore, movements of predators may be important in ecosystem dynamics. While other estuarine predators in the FCE have been shown to potentially move nutrients among ecosystems, the potential for bottlenose dolphins (Tursiops truncatus) to play a similar role in the systems has not been investigated. Stable isotope analysis of biopsy samples were used to investigate spatial variation in trophic interactions of dolphins to see if they might transport nutrients. Values of δ15 N suggest dolphins feed at a trophic level similar to other top predators in the ecosystem while δ13 C suggest that dolphins forage largely within food webs where they were sampled rather than transporting nutrients across ecosystem boundaries. The exception may be dolphins foraging in rivers, which may transport nutrients downstream; a pattern opposite to that of bull sharks and alligators in these habitats. Further research is necessary to predict how future changes occurring due to restoration and climate will affect the ecological roles of dolphins.

The rodent fauna of Long Pine Key, Everglades National Park: a comparison of habitat types

Rodents are often involved at several stages of trophic dynamics. Consequently they often play crucial roles in the structure and function of many complex ecological systems. This study sought to address the lack of baseline data concerning rodents in tropical areas, and south Florida in particular. Live trapping took place in the four major habitat types of the Long Pine Key area of Everglades National Park over the course of one year. I compared population structures and abundance of murid rodents in the four habitat types, and tested multiple weather variables for their effectiveness as predictors of rodent abundance. I found the Long Pine Key area to be depauperate in terms of species diversity. Each of the four species of rodent encountered favored a particular habitat type. The density of the understory vegetation and the avoidance of avian predators in particular appear to be the most important factors in the distribution and abundance of rodents in the Long Pine Key area of Everglades National Park.

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.