Michael R. Heithaus

Predicting ecological consequences of marine top predator declines

Recent studies document unprecedented declines in marine top predators that can initiate trophic cascades. Predicting the wider ecological consequences of these declines requires understanding how predators influence communities by inflicting mortality on prey and inducing behavioral modifications (risk effects). Both mechanisms are important in marine communities, and a sole focus on the effects of predator-inflicted mortality might severely underestimate the importance of predators. We outline direct and indirect consequences of marine predator declines and propose an integrated predictive framework that includes risk effects, which appear to be strongest for long-lived prey species and when resources are abundant. We conclude that marine predators should be managed for the maintenance of both density- and risk-driven ecological processes, and not demographic persistence alone.

Biology of sharks and their relatives

Phylogeny and Zoogeography The Origin and Relationships of Early Chondrichthyans Eileen D. Grogan, Richard Lund, and Emily Greenfest-Allen Elasmobranch Phylogeny: A Mitochondrial Estimate Based on 595 Species Gavin J.P. Naylor, Janine N. Caira, Kirsten Jensen, Kerri A.M. Rosana, Nicolas Straube, and Clemens Lakner Phylogeny of Batoidea Neil C. Aschliman, Kerin M. Claeson, and John D. McEachran Phylogeny, Biology, and Classification of Extant Holocephalans Dominique A. Didier, Jenny M. Kemper, and David A. Ebert Form, Function, and Physiological Processes Biomechanics of Locomotion in Sharks, Rays, and Chimeras Anabela M.R. Maia, Cheryl A.D. Wilga, and George V. Lauder Prey Capture Behavior and Feeding Mechanics of Elasmobranchs Philip J. Motta and Daniel R. Huber Energetics, Metabolism, and Endothermy in Sharks and Rays Diego Bernal, John K. Carlson, Kenneth J. Goldman, and Christopher G. Lowe Food Consumption and Feeding Habits Bradley M. Wetherbee, Enric Cortes, and Joseph J. Bizzarro Integrative Multisensor Tagging: Emerging Techniques to Link Elasmobranch Behavior, Physiology, and Ecology Nicholas M. Whitney, Yannis P. Papastamatiou, Adrian C. Gleiss Reproductive Biology of Elasmobranchs Christina L. Conrath and John A. Musick Hormonal Regulation of Elasmobranch Physiology James Gelsleichter and Andrew N. Evans Sensory Physiology and Behavior of Elasmobranchs Jayne M. Gardiner, Robert E. Hueter, Karen P. Maruska, Joseph A. Sisneros, Brandon M. Casper, David A. Mann, Leo S. Demski Recent Advances in Elasmobranch Immunology Carl A. Luer, Catherine J. Walsh, and Ashby B. Bodine Ecology and Life History Assessing the Age and Growth of Chondrichthyan Fishes Kenneth J. Goldman, Gregor M. Cailliet, Allen H. Andrews, and Lisa J. Natanson Population Dynamics, Demography, and Stock Assessment Enric Cortes, Elizabeth N. Brooks, and Todd Gedamke Genetics of Sharks, Skates, and Rays Edward J. Heist Predator-Prey Interactions Michael R. Heithaus and Jeremy J. Vaudo An Updated Look at Elasmobranchs as Hosts of Metazoan Parasites Janine N. Caira, Claire J. Healy, and Kirsten Jensen Assessing Habitat Use and Movement Colin A. Simpfendorfer and Michelle R. Heupel Index

Patterns and ecosystem consequences of shark declines in the ocean.

Whereas many land predators disappeared before their ecological roles were studied, the decline of marine apex predators is still unfolding. Large sharks in particular have experienced rapid declines over the last decades. In this study, we review the documented changes in exploited elasmobranch communities in coastal, demersal, and pelagic habitats, and synthesize the effects of sharks on their prey and wider communities. We show that the high natural diversity and abundance of sharks is vulnerable to even light fishing pressure. The decline of large predatory sharks reduces natural mortality in a range of prey, contributing to changes in abundance, distribution, and behaviour of small elasmobranchs, marine mammals, and sea turtles that have few other predators. Through direct predation and behavioural modifications, top-down effects of sharks have led to cascading changes in some coastal ecosystems. In demersal and pelagic communities, there is increasing evidence of mesopredator release, but cascading effects are more hypothetical. Here, fishing pressure on mesopredators may mask or even reverse some ecosystem effects. In conclusion, large sharks can exert strong top-down forces with the potential to shape marine communities over large spatial and temporal scales. Yet more empirical evidence is needed to test the generality of these effects throughout the ocean.

BEHAVIORALLY MEDIATED INDIRECT INTERACTIONS IN MARINE COMMUNITIES AND THEIR CONSERVATION IMPLICATIONS

The importance of density-mediated indirect effects (e.g., keystone predators) in marine communities has been widely recognized. Behaviorally mediated indirect interactions (BMIIs) may be equally important in marine systems, but have received relatively little attention. BMIIs occur when a change in an “initiator” species causes a behavioral shift in a “transmitter” species that, in turn, affects a “receiver” species. BMIIs between initiator and receiver species can be described by the ecological relationships between initiator and transmitter, and between transmitter and receiver (i.e., predator and prey, competitors, or no relationship), and the nature of the indirect effect on the receiver (i.e., positive or negative). We review published examples of BMIIs in marine communities, showing that BMIIs may create, enhance, ameliorate, or even reverse the sign of the direct interactions between species. Models that only include direct interactions or density-mediated indirect ones cannot predict some of thes...

Predator–prey and competitive interactions between sharks (order Selachii) and dolphins (suborder Odontoceti): a review

The importance of interactions between sharks and cetaceans has been a subject of much conjecture, but few studies have addressed these interactions. Sharks (order Selachii) have been hypothesized to be important predators on dolphins and porpoises (suborder Odontoceti). Unfortunately, there are often few data to back up claims that certain shark species are major threats to cetaceans. To help identify potential shark predators in specific locations, available data on interactions with odontocetes for all shark species that may include cetaceans in their diet are reviewed. Shark species are categorized into groups based on predatory interactions with dolphins and porpoises (regular predators, occasional predators, potential predators, ectoparasites and insufficient data). Several shark species that have been overlooked in the cetacean literature are identified as potentially important predators while others that have been suspected to be important predators are probably at most occasional predators. How shark predation can influence dolphin populations, habitat use, group size and behaviour is discussed. How risk of shark predation can vary with habitat attributes in both nearshore and pelagic waters is also discussed. Predator–prey interactions have been the focus of most studies of shark–dolphin interaction, but competitive interactions may also occur. The first analysis of shark–dolphin dietary overlap is presented, which shows it to be significant between common dolphins and several species of sharks, including species that prey upon these dolphins.

Superalliance of bottlenose dolphins

It is quite common to find several levels of nested male alliances in human political organization, but these are extremely rare in other species. Yet we found that male bottlenose dolphins (Tursiops sp.) at Shark Bay, Western Australia, form two levels of alliance within a social network of more than 400 individuals. Fourteen of the males formed highly labile alliances, rather than the more typical stable ones, and joined forces in a large ‘superalliance’ that competed directly with smaller teams of stable alliances.

The Biology of Tiger Sharks, Galeocerdo Cuvier, in Shark Bay, Western Australia: Sex Ratio, Size Distribution, Diet, and Seasonal Changes in Catch Rates

Tiger sharks, Galeocerdo cuvier, are apex predators in a variety of nearshore ecosystems throughout the world. This study investigates the biology of tiger sharks in the shallow seagrass ecosystem of Shark Bay, Western Australia. Tiger sharks (n = 252) were the most commonly caught species (94%) compared to other large sharks. Tiger sharks ranged from 148–407 cm TL. The overall sex ratio was biased towards females (1.8 : 1), but the sex ratio of mature animals (> 300 cm TL) did not differ from 1 : 1. Contrary to previous accounts, tiger sharks were caught more often in all habitats during daylight hours than at night. Tiger shark catch rates were highly correlated with water temperature and were highest when water temperatures were above 19°C. The seasonal abundance of tiger sharks is correlated to both water temperature and the occurrence of their main prey: sea snakes and dugongs, Dugong dugon. Stomach contents analysis indicated that sea turtles and smaller elasmobranchs were also common prey. The importance of major seagrass grazers (dugongs and green sea turtles, Chelonia mydas) in the diet of tiger sharks suggests the possibility that these sharks are keystone predators in this ecosystem.

Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics

1. Risk effects of predators can profoundly affect community dynamics, but the nature of these effects is context dependent. 2. Although context dependence has hindered the development of a general framework for predicting the nature and extent of risk effects, recent studies suggest that such a framework is attainable if the factors that shape anti-predator behaviour, and its effectiveness, in natural communities are well understood. 3. One of these factors, the interaction of prey escape tactics and landscape features, has been largely overlooked. 4. We tested whether this interaction gives rise to interspecific variation in habitat-use patterns of sympatric large marine vertebrates at risk of tiger shark (Galeocerdo cuvier Peron and LeSueur, 1822) predation. Specifically, we tested the a priori hypothesis that pied cormorants (Phalacrocorax varius Gmelin, 1789) would modify their use of shallow seagrass habitats in a manner opposite to that of previously studied dolphins (Tursiops aduncus Ehrenberg, 1833), dugongs (Dugong dugon Müller, 1776), and green turtles (Chelonia mydas Linnaeus, 1758) because, unlike these species, the effectiveness of cormorant escape behaviour does not vary spatially. 5. As predicted, cormorants used interior and edge portions of banks proportional to the abundance of their potential prey when sharks were absent but shifted to interior portions of banks to minimize encounters with tiger sharks as predation risk increased. Other shark prey, however, shift to edge microhabitats when shark densities increase to take advantage of easier escape despite higher encounter rates with sharks. 6. The interaction of landscape features and escape ability likely is important in diverse communities. 7. When escape probabilities are high in habitats with high predator density, risk effects of predators can reverse the direction of commonly assumed indirect effects of top predators. 8. The interaction between landscape features and prey escape tactics can result in a single predator species having differential effects on their sympatric prey that could cascade through ecosystems and should be incorporated into a general framework for context dependence of risk effects.

Key Questions in Marine Megafauna Movement Ecology

It is a golden age for animal movement studies and so an opportune time to assess priorities for future work. We assembled 40 experts to identify key questions in this field, focussing on marine megafauna, which include a broad range of birds, mammals, reptiles, and fish. Research on these taxa has both underpinned many of the recent technical developments and led to fundamental discoveries in the field. We show that the questions have broad applicability to other taxa, including terrestrial animals, flying insects, and swimming invertebrates, and, as such, this exercise provides a useful roadmap for targeted deployments and data syntheses that should advance the field of movement ecology.

Why Do Dolphins Carry Sponges

Tool use is rare in wild animals, but of widespread interest because of its relationship to animal cognition, social learning and culture. Despite such attention, quantifying the costs and benefits of tool use has been difficult, largely because if tool use occurs, all population members typically exhibit the behavior. In Shark Bay, Australia, only a subset of the bottlenose dolphin population uses marine sponges as tools, providing an opportunity to assess both proximate and ultimate costs and benefits and document patterns of transmission. We compared sponge-carrying (sponger) females to non-sponge-carrying (non-sponger) females and show that spongers were more solitary, spent more time in deep water channel habitats, dived for longer durations, and devoted more time to foraging than non-spongers; and, even with these potential proximate costs, calving success of sponger females was not significantly different from non-spongers. We also show a clear female-bias in the ontogeny of sponging. With a solitary lifestyle, specialization, and high foraging demands, spongers used tools more than any non-human animal. We suggest that the ecological, social, and developmental mechanisms involved likely (1) help explain the high intrapopulation variation in female behaviour, (2) indicate tradeoffs (e.g., time allocation) between ecological and social factors and, (3) constrain the spread of this innovation to primarily vertical transmission.