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

Environmental and Individual Factors Shaping the Habitat Use and Trophic Interactions of Juvenile Bull Sharks (Carcharhinus leucas) in a Subtropical Estuary

Top predators serve important roles within their respective ecosystem through top-down and bottom-up effects, yet understanding how these roles vary among individuals within predator populations is still in its early stages. Such individuality can have important implications for the functional roles predators play within their respective ecosystems. Therefore, elucidating the factors that drive persistent individual differences within populations is crucial for understanding how individuals, and in turn populations, will respond to environmental changes and anthropogenic stressors, and the implications of these responses for particular ecological functions. In this dissertation I investigated the movements, residency patterns, and trophic interactions of a juvenile bull shark (Carcharhinus leucas) population in a coastal estuary that serves as a nursery. I found that bull sharks undergo ontogenetic niche shifts in their diets and habitat use, with a gradual shift from using freshwater and estuarine resources to marine resources as sharks grew. This behavioral shift appeared to be driven by age-based differences in tradeoffs between safety from predators and availability of prey. Nested within population-level trends in behavior, there was considerable, and consistent, individual variation in both movements and trophic interactions suggesting individual specialization and divergent behavioral tactics within the population. Different behavioral types likely play different roles in food web connectivity and ecosystem dynamics, thus understanding the drivers and importance of phenotypic variability among species will be crucial for improving management strategies and predicting the responses of species and ecosystems to impending changes in environmental conditions and human impacts

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

Move it or lose it: interspecific variation in risk response of pond-breeding anurans

Changes in behavior are often the proximate response of animals to human disturbance, with variability in tolerance levels leading some species to exhibit striking shifts in life history, fitness, and/or survival. Thus, elucidating the effects of disturbance on animal behavior, and how this varies among taxonomically similar species with inherently different behaviors and life histories is of value for management and conservation. We evaluated the risk response of three anuran species—southern leopard frog (Lithobates sphenocephalus), Blanchard’s cricket frog (Acris blanchardi), and green tree frog (Hyla cinerea)—to determine how differences in microhabitat use (arboreal vs ground-dwelling) and body size (small vs medium) may play a role in response to a potential threat within a human-altered subtropical forest. Each species responded to risk with both flight and freeze behaviors, however, behaviors were species- and context-specific. As distance to cover increased, southern leopard frogs increased freezing behavior, green tree frogs decreased freezing behavior, and Blanchard’s cricket frogs increased flight response. The propensity of green tree frogs to use the canopy of vegetation as refugia, and the small body size of Blanchard’s cricket frogs likely led to greater flight response as distance to cover increased, whereas innate reliance on camouflage among southern leopard frogs may place them at greater risk to landscaping, agricultural, and transportation practices in open terrain. As such, arboreal and small-bodied species may inherently be better suited in human altered-landscapes compared to larger, ground-dwelling species. As land-use change continues to modify habitats, understanding how species respond to changes in their environment continues to be of importance, particularly in ecosystems where human-wildlife interactions are expected to increase in frequency

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

Are stable isotope ratios suitable for describing niche partitioning and individual specialization?

As concerns about anthropogenic and natural disturbance grow, understanding animal resource use patterns has been increasingly prioritized to predict how changes in environmental conditions, food web structure, and population dynamics will affect biological resilience. Among the tools used to assess resource use, stable isotope analysis has proliferated in ecological studies, particularly in relation to describing intra- and interspecific variation in trophic interactions. Despite a growing need to disseminate scientific information, the inherent limitations of stable isotope ratios and inappropriate synonymizing of distinct evolutionary and ecological processes may mislead ecological inferences in natural systems. This situation necessitates a re-evaluation of the utility of stable isotope ratios to address certain ecological questions. Here, we assess the efficacy of stable isotope ratios to describe two fundamental ecological processes, niche partitioning and individual specialization. Investigation of these processes has increased substantially in accordance with increased access to stable isotope data. This article discusses the circumstances and approaches that are necessary to evaluate niche partitioning and individual specialization, and outlines key considerations for the associated application of stable isotope ratios

Size-based variation in intertissue comparisons of stable carbon and nitrogen isotopic signatures of bull sharks (Carcharhinus leucas) and tiger sharks (Galeocerdo cuvier)

Stable isotopes are important tools for understanding the trophic roles of elasmobranchs. However, whether different tissues provide consistent stable isotope values within an individual are largely unknown. To address this, the relationships among carbon and nitrogen isotope values were quantified for blood, muscle, and fin from juvenile bull sharks (Carcharhinus leucas) and blood and fin from large tiger sharks (Galeocerdo cuvier) collected in two different ecosystems. We also investigated the relationship between shark size and the magnitude of differences in isotopic values between tissues. Isotope values were significantly positively correlated for all paired tissue comparisons, but R2 values were much higher for δ13C than for δ15N. Paired differences between isotopic values of tissues were relatively small but varied significantly with shark total length, suggesting that shark size can be an important factor influencing the magnitude of differences in isotope values of different tissues. For studies of juvenile sharks, care should be taken in using slow turnover tissues like muscle and fin, because they may retain a maternal signature for an extended time. Although correlations were relatively strong, results suggest that correction factors should be generated for the desired study species and may only allow coarse-scale comparisons between studies using different tissue types

The Roles of Large Top Predators in Coastal Ecosystems: New Insights from Long Term Ecological Research

During recent human history, human activities such as overhunting and habitat destruction have severely impacted many large top predator populations around the world. Studies from a variety of ecosystems show that loss or diminishment of top predator populations can have serious consequences for population and community dynamics and ecosystem stability. However, there are relatively few studies of the roles of large top predators in coastal ecosystems, so that we do not yet completely understand what could happen to coastal areas if large top predators are extirpated or significantly reduced in number. This lack of knowledge is surprising given that coastal areas around the globe are highly valued and densely populated by humans, and thus coastal large top predator populations frequently come into conflict with coastal human populations. This paper reviews what is known about the ecological roles of large top predators in coastal systems and presents a synthesis of recent work from three coastal eastern US Long Term Ecological Research (LTER) sites where long-term studies reveal what appear to be common themes relating to the roles of large top predators in coastal systems. We discuss three specific themes: (1) large top predators acting as mobile links between disparate habitats, (2) large top predators potentially affecting nutrient and biogeochemical dynamics through localized behaviors, and (3) individual specialization of large top predator behaviors. We also discuss how research within the LTER network has led to enhanced understanding of the ecological roles of coastal large top predators. Highlighting this work is intended to encourage further investigation of the roles of large top predators across diverse coastal aquatic habitats and to better inform researchers and ecosystem managers about the importance of large top predators for coastal ecosystem health and stability

The Roles of Large Top Predators in Coastal Ecosystems: New Insights from long Term Ecological Research

Abstract: During recent human history, human activities such as overhunting and habitat destruction have severely impacted many large top predator populations around the world. Studies from a variety of ecosystems show that loss or diminishment of top predator populations can have serious consequences for population and community dynamics and ecosystem stability. However, there are relatively few studies of the roles of large top predators in coastal ecosystems, so that we do not yet completely understand what could happen to coastal areas if large top predators are extirpated or significantly reduced in number. This lack of knowledge is surprising given that coastal areas around the globe are highly valued and densely populated by humans, and thus coastal large top predator populations frequently come into conflict with coastal human populations. This paper reviews what is known about the ecological roles of large top predators in coastal systems and presents a synthesis of recent work from three coastal eastern US Long Term Ecological Research (LTER) sites where long-term studies reveal what appear to be common themes relating to the roles of large top predators in coastal systems. We discuss three specific themes: (1) large top predators acting as mobile links between disparate habitats, (2) large top predators potentially affecting nutrient and biogeochemical dynamics through localized behaviors, and (3) individual specialization of large top predator behaviors. We also discuss how research within the LTER network has led to enhanced understanding of the ecological roles of coastal large top predators. Highlighting this work is intended to encourage further investigation of the roles of large top predators across diverse coastal aquatic habitats and to better inform researchers and ecosystem managers about the importance of large top predators for coastal ecosystem health and stability.Keywords: Individual specialization, Morone saxatilis, Migratory striped bass, Sea otters, Bottoom up control, Alligator holes, Trophic cascades, Food webs, Kelp forests, EvergladesThis is the publisher’s final pdf. The published article is copyrighted by the Oceanography Society and can be found at: http://www.tos.org/oceanography/

A global perspective on the trophic geography of sharks

Sharks are a diverse group of mobile predators that forage across varied spatial scales and have the potential to influence food web dynamics. The ecological consequences of recent declines in shark biomass may extend across broader geographic ranges if shark taxa display common behavioural traits. By tracking the original site of photosynthetic fixation of carbon atoms that were ultimately assimilated into muscle tissues of 5,394 sharks from 114 species, we identify globally consistent biogeographic traits in trophic interactions between sharks found in different habitats. We show that populations of shelf-dwelling sharks derive a substantial proportion of their carbon from regional pelagic sources, but contain individuals that forage within additional isotopically diverse local food webs, such as those supported by terrestrial plant sources, benthic production and macrophytes. In contrast, oceanic sharks seem to use carbon derived from between 30° and 50° of latitude. Global-scale compilations of stable isotope data combined with biogeochemical modelling generate hypotheses regarding animal behaviours that can be tested with other methodological approaches.This research was conducted as part of C.S.B.’s Ph.D dissertation, which was funded by the University of Southampton and NERC (NE/L50161X/1), and through a NERC Grant-in-Kind from the Life Sciences Mass Spectrometry Facility (LSMSF; EK267-03/16). We thank A. Bates, D. Sims, F. Neat, R. McGill and J. Newton for their analytical contributions and comments on the manuscripts.Peer reviewe