Energetic connectivity of diverse elasmobranch populations - implications for ecological resilience.

Understanding the factors shaping patterns of ecological resilience is critical for mitigating the loss of global biodiversity. Throughout aquatic environments, highly mobile predators are thought to serve as important vectors of energy between ecosystems thereby promoting stability and resilience. However, the role these predators play in connecting food webs and promoting energy flow remains poorly understood in most contexts. Using carbon and nitrogen isotopes, we quantified the use of several prey resource pools (small oceanic forage, large oceanics, coral reef, and seagrass) by 17 species of elasmobranch fishes (n = 351 individuals) in The Bahamas to determine their functional diversity and roles as ecosystem links. We observed remarkable functional diversity across species and identified four major groups responsible for connecting discrete regions of the seascape. Elasmobranchs were responsible for promoting energetic connectivity between neritic, oceanic and deep-sea ecosystems. Our findings illustrate how mobile predators promote ecosystem connectivity, underscoring their functional significance and role in supporting ecological resilience. More broadly, strong predator conservation efforts in developing island nations, such as The Bahamas, are likely to yield ecological benefits that enhance the resilience of marine ecosystems to combat imminent threats such as habitat degradation and climate change.

Energetic consequences of resource use diversity in a marine carnivore.

Understanding how intraspecific variation in the use of prey resources impacts energy metabolism has strong implications for predicting long-term fitness and is critical for predicting population-to-community level responses to environmental change. Here, we examine the energetic consequences of variable prey resource use in a widely distributed marine carnivore, juvenile sand tiger sharks (Carcharias taurus). We used carbon and nitrogen isotope analysis to identify three primary prey resource pools-demersal omnivores, pelagic forage, and benthic detritivores and estimated the proportional assimilation of each resource using Bayesian mixing models. We then quantified how the utilization of these resource pools impacted the concentrations of six plasma lipids and how this varied by ontogeny. Sharks exhibited variable reliance on two of three predominant prey resource pools: demersal omnivores and pelagic forage. Resource use variation was a strong predictor of energetic condition, whereby individuals more reliant upon pelagic forage exhibited higher blood plasma concentrations of very low-density lipoproteins, cholesterol, and triglycerides. These findings underscore how intraspecific variation in resource use may impact the energy metabolism of animals, and more broadly, that natural and anthropogenically driven fluctuations in prey resources could have longer term energetic consequences.

Delineation of blacktip shark (Carcharhinus limbatus) nursery habitats in the north-western Gulf of Mexico.

Coevolution with predators leads to the use of low-risk habitats by many prey species, which promotes survival during early developmental phases. These nurseries are valued by conservation and management agencies because of their contributions to adult populations. However, the physical and geographic characteristics, like shallow depths and isolation from other marine habitats, that restrict access to predators and thereby reduce risk to juvenile animals can also limit scientific research. Consequently, many nursery habitats are still unidentified and understudied. Here we used gillnet monitoring from 1982 to 2018 to delineate blacktip shark (Carcharhinus limbatus) nurseries in the north-western Gulf of Mexico and elucidated their physical, environmental and biological characteristics. Nursery habitats within estuaries (<2% of spatial area) were proximate to the Gulf of Mexico and exhibited significantly lower variability in salinity than non-nurseries. However, relative abundances of predators and prey were not significant delineators of nursery habitats. As such, food and risk may not influence juvenile blacktip habitat use as expected. Alternatively, reduced osmoregulatory stress attributed to predictable environments likely provides advantageous conditions for blacktips to develop foraging and antipredator tactics, which is vital prior to the winter migration of juvenile sharks into the Gulf of Mexico.

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.

New insights into the trophic ecology of blacktip sharks (Carcharhinus limbatus) from a subtropical estuary in the western Gulf of Mexico.

As environmental change persists, understanding resource use patterns is of value to predict the consequences of shifting trophic structures. While many sharks are opportunistic predators, some exhibit prey selectivity, putting them at higher risk compared to species with greater trophic plasticity. In the Gulf of Mexico (GOM), Clupeids and Sciaenids comprise 69% of blacktip shark (Carcharhinus limbatus) diets, which is consequential considering potential responses of these prey groups to disturbance and over harvesting. We assessed if blacktips exhibit selectivity for Clupeids and Sciaenids in the western GOM based on stomach contents from sharks in coastal Texas. Clupeids comprised <2% of diets, while striped mullet (Mugil cephalus) and red drum (Sciaenops ocellatus) comprised >70% of identifiable prey. Ontogenetic shifts from smaller (Clupeids, small Sciaenids) to larger, higher trophic level (Ariidae, Elasmobranchii) prey fits our understanding of foraging among coastal sharks, and suggests our regional understanding of blacktip trophic ecology may be limited by the sizes of sampled sharks. Observed increases in blacktip densities coupled with declines in prey (Mugilids, Sciaenids) is concerning if blacktips have limited diet plasticity. Yet GOM blacktips may be more generalized than previously thought, which is promising for conservation and management.

Studying animal niches using bulk stable isotope ratios: an updated synthesis.

The development of the isotopic niche, an n-dimensional hypervolume (with n being the number of isotopes) occupied by a population in delta space, has revolutionized the study of animal interactions in wild populations. While the isotopic niche offers a useful means to understand interactions at many ecological resolutions (e.g., individual, population, community, ecosystem), a variety of intrinsic and extrinsic factors drive isotopic variability and influence the ultimate geometry of observed niche dimensions. Here, we provide an updated synthesis to guide the application of bulk stable isotope ratios to study ecological niches. We summarize progress in the application of bulk stable isotope ratios for evaluating niches to synthesize a formal definition of the isotopic niche. We identify six broad categories to describe drivers of isotopic variance introduced by the animal, its environment, and the researcher, and provide recommendations to account for such variations before, during, and after sample collection and data analyses. Our synthesis illustrates the considerations that should be made before employing the isotopic niche to broader ecological contexts, and offers guidance for the use and interpretation of isotopic niche dynamics in future studies.

Inter-individual differences in ontogenetic trophic shifts among three marine predators.

Ontogenetic niche shifts are widespread. However, individual differences in size at birth, morphology, sex, and personalities can cause variability in behavior. As such, inherent inter-individual differences within populations may lead to context-dependent changes in behavior with animal body size, which is of concern for understanding population dynamics and optimizing ecological monitoring. Using stable carbon and nitrogen isotope values from concurrently sampled tissues, we quantified the direction and magnitude of intraspecific variation in trophic shifts among three shark species, and how these changed with body size: spurdogs (Squalus spp.) in deep-sea habitats off La Réunion, bull sharks (Carcharhinus leucas) in estuarine habitats of the Florida Everglades, and blacktip reef sharks (Carcharhinus melanopterus) in coral reef ecosystems of Moorea, French Polynesia. Intraspecific variation in trophic shifts was limited among spurdogs, and decreased with body size, while bull sharks exhibited greater individual differences in trophic shifts, but also decreased in variability through ontogeny. In contrast, blacktip reef sharks exhibited increased intraspecific variation in trophic interactions with body size. Variability in trophic interactions and ontogenetic shifts are known to be associated with changes in energetic requirements, but can vary with ecological context. Our results suggest that environmental stability may affect variability within populations, and ecosystems with greater spatial and/or temporal variability in environmental conditions, and those with more diverse food webs may facilitate greater individual differences in trophic interactions, and thus ontogenetic trophic shifts. In light of concerns over environmental disturbance, elucidating the contexts that promote or dampen phenotypic variability is invaluable for predicting population- and community-level responses to environmental changes.

Effects of anticoagulants on stable-isotope values (δ13 C and δ15 N) of shark blood components.

The effects of anticoagulant EDTA and sodium heparin (SH) on stable carbon δ13 C and nitrogen δ15 N isotopic values of red blood cells (RBC) and blood plasma in juvenile blacktip reef sharks Carcharhinus melanopterus were analysed. Plasma preserved with anticoagulants was not isotopically distinct from plasma stored in no-additive control tubes but RBC δ15 N values exhibited small enrichments when preserved with EDTA and SH. Results suggest EDTA and SH are viable anticoagulants for stable isotopic analyses of blood fractions but further studies are advised to validate results.

Individual variation in ontogenetic niche shifts in habitat use and movement patterns of a large estuarine predator (Carcharhinus leucas).

Ontogenetic niche shifts are common among animals, yet most studies only investigate niche shifts at the population level, which may overlook considerable differences among individuals in the timing and dynamics of these shifts. Such divergent behaviors within size-/age-classes have important implications for the roles a population-and specific age-classes-play in their respective ecosystem(s). Using acoustic telemetry, we tracked the movements of juvenile bull sharks in the Shark River Estuary of Everglades National Park, Florida, and found that sharks increased their use of marine microhabitats with age to take advantage of more abundant resources, but continued to use freshwater and estuarine microhabitats as refuges from marine predators. Within this population-level ontogenetic niche shift, however, movement patterns varied among individual sharks, with 47 % of sharks exhibiting condition-dependent habitat use and 53 % appearing risk-averse regardless of body condition. Among sharks older than age 0, fifty percent made regular movements between adjacent regions of the estuary, while the other half made less predictable movements that often featured long-term residence in specific regions. Individual differences were apparently shaped by both intrinsic and extrinsic factors, including individual responses to food-risk trade-offs and body condition. These differences appear to develop early in the lives of bull sharks, and persist throughout their residencies in nursery habitats. The widespread occurrence of intraspecific variation in behavior among mobile taxa suggests it is important in shaping population dynamics of at least some species, and elucidating the contexts and timing in which it develops and persists is important for understanding its role within communities.

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.

Warming waters lead to increased habitat suitability for juvenile bull sharks (Carcharhinus leucas).

Coastal ecosystems are highly vulnerable to the impacts of climate change and other stressors, including urbanization and overfishing. Consequently, distributions of coastal fish have begun to change, particularly in response to increasing temperatures linked to climate change. However, few studies have evaluated how natural and anthropogenic disturbances can alter species distributions in conjunction with geophysical habitat alterations, such as changes to land use and land cover (LU/LC). Here, we examine the spatiotemporal changes in the distribution of juvenile bull sharks (Carcharhinus leucas) using a multi-decadal fishery-independent survey of coastal Alabama. Using a boosted regression tree (BRT) modeling framework, we assess the covariance of environmental conditions (sea surface temperature, depth, salinity, dissolved oxygen, riverine discharge, Chl-a) as well as historic changes to LU/LC to the distribution of bull sharks. Species distribution models resultant from BRTs for early (2003-2005) and recent (2018-2020) monitoring periods indicated a mean increase in habitat suitability (i.e., probability of capture) for juvenile bull sharks from 0.028 to 0.082, concomitant with substantial increases in mean annual temperature (0.058°C/yr), Chl-a (2.32 mg/m3), and urbanization (increased LU/LC) since 2000. These results align with observed five-fold increases in the relative abundance of juvenile bull sharks across the study period and demonstrate the impacts of changing environmental conditions on their distribution and relative abundance. As climate change persists, coastal communities will continue to change, altering the structure of ecological communities and the success of nearshore fisheries.

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.

Grow fast, die young: Does compensatory growth reduce survival of juvenile blacktip sharks (Carcharhinus limbatus) in the western Gulf of Mexico?

Effective conservation and management necessitate an understanding of the ecological mechanisms that shape species life histories in order to predict how variability in natural and anthropogenic impacts will alter growth rates, recruitment, and survival. Among these mechanisms, the interaction between parturition timing and prey availability frequently influences offspring success, particularly when postnatal care is absent. Here, we assess how parturition timing and nursery conditions, including prey abundance and environmental conditions, influence the growth and potential survival of blacktip sharks (Carcharhinus limbatus) in western Gulf of Mexico (GOM) estuaries over their first year. Catch data from long-term gillnet monitoring allowed for clear delineation of cohorts based on size frequency distribution plots, and showed that late parturition cohorts born in estuaries with fewer prey resources exhibited more rapid growth than early parturition cohorts that experienced more abundant prey. Compensatory behaviors that promoted accelerated growth led to reduced second year residency, likely due to reduced survival resultant from greater risk taking and potentially due to reduced site fidelity attributed to larger body size. Water temperatures influenced blacktip growth rates through physiological increases in metabolism and potential premigratory foraging cues associated with cooling temperatures. Gradual warming of the GOM (0.03°C year-1) was also correlated with earlier parturition across the study period (1982-2017), similar to other migratory species. Considering current trends in climate and associated phenological shifts in many animals, testing hypotheses assessing compensatory growth-risk trade-offs is important moving forward to predict changes in life histories and associated recruitment in concert with current and future conservation actions, like wildlife management.

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.

Population structure, connectivity, and demographic history of an apex marine predator, the bull shark Carcharhinus leucas.

Knowledge of population structure, connectivity, and effective population size remains limited for many marine apex predators, including the bull shark Carcharhinus leucas. This large-bodied coastal shark is distributed worldwide in warm temperate and tropical waters, and uses estuaries and rivers as nurseries. As an apex predator, the bull shark likely plays a vital ecological role within marine food webs, but is at risk due to inshore habitat degradation and various fishing pressures. We investigated the bull shark's global population structure and demographic history by analyzing the genetic diversity of 370 individuals from 11 different locations using 25 microsatellite loci and three mitochondrial genes (CR, nd4, and cytb). Both types of markers revealed clustering between sharks from the Western Atlantic and those from the Western Pacific and the Western Indian Ocean, with no contemporary gene flow. Microsatellite data suggested low differentiation between the Western Indian Ocean and the Western Pacific, but substantial differentiation was found using mitochondrial DNA. Integrating information from both types of markers and using Bayesian computation with a random forest procedure (ABC-RF), this discordance was found to be due to a complete lack of contemporary gene flow. High genetic connectivity was found both within the Western Indian Ocean and within the Western Pacific. In conclusion, these results suggest important structuring of bull shark populations globally with important gene flow occurring along coastlines, highlighting the need for management and conservation plans on regional scales rather than oceanic basin scale.

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.

Species co-occurrence affects the trophic interactions of two juvenile reef shark species in tropical lagoon nurseries in Moorea (French Polynesia).

Food web structure is shaped by interactions within and across trophic levels. As such, understanding how the presence and absence of predators, prey, and competitors affect species foraging patterns is important for predicting the consequences of changes in species abundances, distributions, and behaviors. Here, we used plasma δ13C and δ15N values from juvenile blacktip reef sharks (Carcharhinus melanopterus) and juvenile sicklefin lemon sharks (Negaprion acutidens) to investigate how species co-occurrence affects their trophic interactions in littoral waters of Moorea, French Polynesia. Co-occurrence led to isotopic niche partitioning among sharks within nurseries, with significant increases in δ15N values among sicklefin lemon sharks, and significant decreases in δ15N among blacktip reef sharks. Niche segregation likely promotes coexistence of these two predators during early years of growth and development, but data do not suggest coexistence affects life history traits, such as body size, body condition, and ontogenetic niche shifts. Plasticity in trophic niches among juvenile blacktip reef sharks and sicklefin lemon sharks also suggests these predators are able to account for changes in community structure, resource availability, and intra-guild competition, and may fill similar functional roles in the absence of the other species, which is important as environmental change and human impacts persist in coral reef ecosystems.

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.