Does Landscape Context Affect Habitat Value? The Importance of Seascape Ecology in Back-reef Systems

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

The interactive effects of predators, resources, and disturbance on freshwater snail populations from the Everglades

The origins of population dynamics depend on interplay between abiotic and biotic factors; the relative importance of each changing across space and time. Predation is a central feature of ecological communities that removes individuals (consumption) and alters prey traits (non-consumptive). Resource quality mitigates non-consumptive predator effects by stimulating growth and reproduction. Disturbance resets predator-prey interactions by removing both. I integrate experiments, time-series analysis, and performance trials to examine the relative importance of these on the population dynamics of a snail species by studying a variety of their traits. A review of ninety-three published articles revealed that snail abundance was much less in the Everglades and similar ecosystems compared to all other freshwater ecosystems considered. Separating consumptive from non-consumptive (cues) predator effects at different phosphorous levels with an experiment determined that phosphorous stimulated, but predator cues inhibited snail growth (34% vs. 23%), activity (38% vs. 53%), and reproductive effort (99% vs. 90%) compared to controls. Cues induced taller shells and smaller openings and moved to refugia where they reduced periphyton by 8%. Consumptive predator effects were minor in comparison. In a reciprocal transplant cage experiment along a predator cue and phosphorous gradient created by a canal, snails grew 10% faster and produced 37% more eggs far from the canal (fewer cues) when fed phosphorous-enriched periphyton from near the canal. Time-series analysis at four sites and predator performance trials reveal that phosphorous-enriched regions support larger snail populations, seasonal drying removes snails at all sites, crayfish negatively affect populations in enriched regions, and molluscivorous fish consume snails in the wet season. Combining these studies reveals interplay between resources, predators, and seasonality that limit snail populations in the Everglades and lead to their low abundance compared to other freshwater ecosystems. Resource quality is emerging as the critical factor because improving resources profoundly improved growth and reproduction; seasonal drying and predation become important at times and places. This work contributes to the general understanding in ecology of the relative importance of different factors that structure populations and provides evidence that bolsters monitoring efforts to assess the Comprehensive Everglades Restoration Plan that show phosphorous enrichment is a major driver of ecosystem change.

Applying stable isotopes to examine food-web structure: an overview of analytical tools

Stable isotope analysis has emerged as one of the primary means for examining the structure and dynamics of food webs, and numerous analytical approaches are now commonly used in the field. Techniques range from simple, qualitative inferences based on the isotopic niche, to Bayesian mixing models that can be used to characterize food-web structure at multiple hierarchical levels. We provide a comprehensive review of these techniques, and thus a single reference source to help identify the most useful approaches to apply to a given data set. We structure the review around four general questions: (1) what is the trophic position of an organism in a food web?; (2) which resource pools support consumers?; (3) what additional information does relative position of consumers in isotopic space reveal about food-web structure?; and (4) what is the degree of trophic variability at the intrapopulation level? For each general question, we detail different approaches that have been applied, discussing the strengths and weaknesses of each. We conclude with a set of suggestions that transcend individual analytical approaches, and provide guidance for future applications in the field.

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.

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

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

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.

Spatial and Temporal Patterns in the Distribution, Behavior, and Activity of Fishes in Canals of the Everglades

Landscape characteristics, disturbances, and temporal variability influence predator-prey relationships, but are often overlooked in experimental studies. In the Everglades, seasonal disturbances force the spatial overlap of predators and prey, potentially increasing predation risk for prey. This study examined seasonal and diel patterns of fish use of canals and assessed predation risk for small fishes using an encounter rate model. I deployed an imaging sonar in Everglades canals to quantify density and swimming speeds of fishes, and detect anti-predator behaviors by small fishes. Generally, seasonal declines of marsh water-levels increased the density of large fishes in canals. Densities of small and large fishes were positively correlated and, as small-fish density increased, schooling frequency also increased. At night, schools disbanded and small fishes were observed congregating along the canal edge. The encounter rate model predicted highest predator-prey encounters during the day, but access to cover may reduce predation risk for small fishes.

A Suite of Prey Traits Determine Predator and Nutrient Enrichment Effects in a Tri-Trophic Food Chain

Predation, predation risk, and resource quality affect suites of prey traits that collectively impact individual fitness, population dynamics, and community structure. However, studies of multi-trophic level effects generally focus on a single prey trait, failing to capture trade-offs among suites of covarying traits that govern population responses and emergent community patterns. We used structural equation models (SEM) to summarize the non-lethal and lethal effects of crayfish, Procambarus fallax, and phosphorus (P) addition, which affected prey food quality (periphyton), on the interactive effects of behavioral, morphological, developmental, and reproductive traits of snails, Planorbella duryi. Univariate and multivariate analyses suggested trade-offs between production (growth, reproduction) and defense (foraging behavior, shell shape) traits of snails in response to non-lethal crayfish and P addition, but few lethal effects. SEM revealed that non-lethal crayfish effects indirectly limited per capita offspring standing stock by increasing refuge use, slowing individual growth, and inducing snails to produce thicker, compressed shells. The negative effects of non-lethal crayfish on snails were strongest with P addition; snails increased allocation to shell defense rather than growth or reproduction. However, compared to ambient conditions, P addition with non-lethal crayfish still yielded greater per capita offspring standing stock by speeding individual snail growth enabling them to produce more offspring that also grew faster. Increased refuge use in response to non-lethal crayfish led to a non-lethal trophic cascade that altered the spatial distribution of periphyton. Independent of crayfish effects, snails stimulated periphyton growth through nutrient regeneration. These findings illustrate the importance of studying suites of traits that reveal costs associated with inducing different traits and how expressing those traits impacts population and community level processes.

Antipredator behavior and cue recognition by multiple Everglades prey to a novel cichlid predator

Novel predator introductions are thought to have a high impact on native prey, especially in freshwater systems. Prey may fail to recognize predators as a threat, or show inappropriate or ineffective responses. The ability of prey to recognize and respond appropriately to novel predators may depend on the prey’s use of general or specific cues to detect predation threats.We used laboratory experiments to examine the ability of three native Everglades prey species (Eastern mosquitofish, flagfish and riverine grass shrimp) to respond to the presence, as well as to the chemical and visual cues of a native predator (warmouth) and a recentlyintroduced non-native predator (African jewelfish). We used prey from populations that had not previously encountered jewelfish. Despite this novelty, the native warmouth and nonnative jewelfish had overall similar predatory effects, except on mosquitofish, which suffered higher warmouth predation. When predators were present, the three prey taxa showed consistent and strong responses to the non-native jewelfish, which were similar in magnitude to the responses exhibited to the native warmouth. When cues were presented, fish prey responded largely to chemical cues, while shrimp showed no response to either chemical or visual cues. Overall, responses by mosquitofish and flagfish to chemical cues indicated low differentiation among cue types, with similar responses to general and specific cues. The fact that antipredator behaviours were similar toward native and non-native predators suggests that the susceptibility to a novel fish predator may be similar to that of native fishes, and prey may overcome predator novelty, at least when predators are confamilial to other common and longer-established non-native threats.

Multiple predator effects and native prey responses to two non-native Everglades cichlids

Non-native predators may have negative impacts on native communities, and these effects may be dependent on interactions among multiple non-native predators. Sequential invasions by predators can enhance risk for native prey. Prey have a limited ability to respond to multiple threats since appropriate responses may conflict, and interactions with recent invaders may be novel. We examined predator–prey interactions among two non-native predators, a recent invader, the African jewelfish, and the longer-established Mayan cichlid, and a native Florida Everglades prey assemblage. Using field enclosures and laboratory aquaria, we compared predatory effects and antipredator responses across five prey taxa. Total predation rates were higher for Mayan cichlids, which also targeted more prey types. The cichlid invaders had similar microhabitat use, but varied in foraging styles, with African jewelfish being more active. The three prey species that experienced predation were those that overlapped in habitat use with predators. Flagfish were consumed by both predators, while riverine grass shrimp and bluefin killifish were eaten only by Mayan cichlids. In mixed predator treatments, we saw no evidence of emergent effects, since interactions between the two cichlid predators were low. Prey responded to predator threats by altering activity but not vertical distribution. Results suggest that prey vulnerability is affected by activity and habitat domain overlap with predators and may be lower to newly invading predators, perhaps due to novelty in the interaction.

Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions

We present a framework for explaining variation in predator invasion success and predator impacts on native prey that integrates information about predator–prey naïveté, predator and prey behavioral responses to each other, consumptive and non-consumptive effects of predators on prey, and interacting effects of multiple species interactions. We begin with the ‘naïve prey’ hypothesis that posits that naïve, native prey that lack evolutionary history with non-native predators suffer heavy predation because they exhibit ineffective antipredator responses to novel predators. Not all naïve prey, however, show ineffective antipredator responses to novel predators. To explain variation in prey response to novel predators, we focus on the interaction between prey use of general versus specific cues and responses, and the functional similarity of non-native and native predators. Effective antipredator responses reduce predation rates (reduce consumptive effects of predators, CEs), but often also carry costs that result in non-consumptive effects (NCEs) of predators. We contrast expected CEs versus NCEs for non-native versus native predators, and discuss how differences in the relative magnitudes of CEs and NCEs might influence invasion dynamics. Going beyond the effects of naïve prey, we discuss how the ‘naïve prey’, ‘enemy release’ and ‘evolution of increased competitive ability’ (EICA) hypotheses are inter-related, and how the importance of all three might be mediated by prey and predator naïveté. These ideas hinge on the notion that non-native predators enjoy a ‘novelty advantage’ associated with the naïveté of native prey and top predators. However, non-native predators could instead suffer from a novelty disadvantage because they are also naïve to their new prey and potential predators. We hypothesize that patterns of community similarity and evolution might explain the variation in novelty advantage that can underlie variation in invasion outcomes. Finally, we discuss management implications of our framework, including suggestions for managing invasive predators, predator reintroductions and biological control.

Habitat use and foraging ecology of a batoid community in Shark Bay, Western Australia

Worldwide declines in populations of large elasmobranchs and the potential cascading effects on marine ecosystems have garnered considerable attention. Far less appreciated are the potential ecological impacts of changes in abundances of small to medium bodied elasmobranchs mesopredators. Crucial to elucidating the role of these elasmobranchs is an understanding of their habitat use and foraging ecology in pristine conditions. I investigated the trophic interactions and factors driving spatiotemporal variation in abundances of elasmobranch mesopredators in the relatively pristine ecosystem of Shark Bay, Australia. First, I describe the species composition and seasonal habitat use patterns of elasmobranch mesopredator on the sandflats of Shark Bay. Juvenile batoids dominated this diverse community and were extremely abundant in nearshore microhabitats during the warm season. Stomach content analysis and stable isotopic analysis revealed that there is a large degree of dietary overlap between common batoid species. Crustaceans, which tend to be found in seagrass habitats, dominated diets. Despite isotopic differences between many species, overlap in isotopic niche space was high and there was some degree of individual specialization. I then, investigated the importance of abiotic (temperature and water depth) and biotic (prey and predator abundance) factors in shaping batoid habitat use. Batoids were most abundant and tended to rest in shallow nearshore waters when temperatures were high. This pattern coincides with periods of large shark abundance suggesting batoids were seeking refuge from predators rather than selecting optimal temperatures. Finally, I used acoustic telemetry to examine batoid residency and diel use of the sandflats. Individual batoids were present on the sandflats during both the warm and cold seasons and throughout the diel cycle, suggesting lower sandflat densities during the cold season were a result of habitat shifts rather than migration out of Shark Bay. Combined, habitat use and dietary results suggest that batoids have the potential to seasonally impact sandflat dynamics through their presence, although foraging may be limited on the sandflats. Interestingly, my results suggest that elasmobranch mesopredators in pristine ecosystems probably are not regulated by food supply and their habitat use patterns and perhaps ecosystem impacts may be influenced by their predators.

The influence of body size on the ecology of coastal fish predators in the Bahamas

Body size is a fundamental structural characteristic of organisms, determining critical life history and physiological traits, and influencing population dynamics, community structure, and ecosystem function. For my dissertation, I focused on effects of body size on habitat use and diet of important coastal fish predators, as well as their influence on faunal communities in Bahamian wetlands. First, using acoustic telemetry and stable isotope analysis, I identified high variability in movement patterns and habitat use among individuals within a gray snapper (Lutjanus griseus) and schoolmaster snapper (L. apodus) population. This intrapopulation variation was not explained by body size, but by individual behavior in habitat use. Isotope values differed between individuals that moved further distances and individuals that stayed close to their home sites, suggesting movement differences were related to specific patterns of foraging behavior. Subsequently, while investigating diet of schoolmaster snapper over a two-year period using stomach content and stable isotope analyses, I also found intrapopulation diet variation, mostly explained by differences in size class, individual behavior and temporal variability. I then developed a hypothesis-testing framework examining intrapopulation niche variation between size classes using stable isotopes. This framework can serve as baseline to categorize taxonomic or functional groupings into specific niche shift scenarios, as well as to help elucidate underlying mechanisms causing niche shifts in certain size classes. Finally, I examined the effect of different-sized fish predators on epifaunal community structure in shallow seagrass beds using exclusion experiments at two spatial scales. Overall, I found that predator effects were rather weak, with predator size and spatial scale having no impact on the community. Yet, I also found some evidence of strong interactions on particular common snapper prey. As Bahamian wetlands are increasingly threatened by human activities (e.g., overexploitation, habitat degradation), an enhanced knowledge of the ecology of organisms inhabiting these systems is crucial for developing appropriate conservation and management strategies. My dissertation research contributed to this effort by providing critical information about the resource use of important Bahamian fish predators, as well as their effect on faunal seagrass communities.

Fish population dynamics in a seasonally varying wetland

Small fishes in seasonally flooded environments such as the Everglades are capable of spreading into newly flooded areas and building up substantial biomass. Passive drift cannot account for the rapidity of observed population expansions. To test the ‘reaction–diffusion’ mechanism for spread of the fish, we estimated their diffusion coefficient and applied a reaction–diffusion model. This mechanism was also too weak to account for the spatial dynamics. Two other hypotheses were tested through modeling. The first—the ‘refuge mechanism’—hypothesizes that small remnant populations of small fishes survive the dry season in small permanent bodies of water (refugia), sites where the water level is otherwise below the surface. The second mechanism, which we call the ‘dynamic ideal free distribution mechanism’ is that consumption by the fish creates a prey density gradient and that fish taxis along this gradient can lead to rapid population expansion in space. We examined the two alternatives and concluded that although refugia may play an important role in recolonization by the fish population during reflooding, only the second, taxis in the direction of the flooding front, seems capable of matching empirical observations. This study has important implications for management of wetlands, as fish biomass is an essential support of higher trophic levels.