Steven T. Kessel

Aquatic animal telemetry: A panoramic window into the underwater world

A brave new world with a wider view Researchers have long attempted to follow animals as they move through their environment. Until relatively recently, however, such efforts were limited to short distances and times in species large enough to carry large batteries and transmitters. New technologies have opened up new frontiers in animal tracking remote data collection. Hussey et al. review the unique directions such efforts have taken for marine systems, while Kays et al. review recent advances for terrestrial species. We have entered a new era of animal ecology, where animals act as both subjects and samplers of their environments. Science, this issue 10.1126/science.1255642, 10.1126/science.aaa2478 BACKGROUND Global aquatic environments are changing profoundly as a result of human actions; consequently, so too are the ways in which organisms are distributing themselves through space and time. Our ability to predict organism and community responses to these alterations will be dependent on knowledge of animal movements, interactions, and how the physiological and environmental processes underlying them shape species distributions. These patterns and processes ultimately structure aquatic ecosystems and provide the wealth of ecosystem services upon which humans depend. Until recently, the vast size, opacity, and dynamic nature of the aquatic realm have impeded our efforts to understand these ecosystems. With rapid technological advancement over the past several decades, a suite of electronic tracking devices (e.g., acoustic and satellite transmitters) that can remotely monitor animals in these challenging environments are now available. Aquatic telemetry technology is rapidly accelerating our ability to observe animal behavior and distribution and, as a consequence, is fundamentally altering our understanding of the structure and function of global aquatic ecosystems. These advances provide the toolbox to define how future global aquatic management practices must evolve. ADVANCES Aquatic telemetry has emerged through technological advances in miniaturization, battery engineering, and software and hardware development, allowing the monitoring of organisms whose habitats range from the poles to the tropics and the photic zone to the abyssal depths. This is enabling the characterization of the horizontal and vertical movements of individuals, populations, and entire communities over scales of meters to tens of thousands of kilometers and over time frames of hours to years and even over the entire lifetimes of individuals. Electronic tags can now be equipped with sensors that measure ambient physical parameters (depth, temperature, conductivity, fluorescence), providing simultaneous monitoring of animals’ environments. By linking telemetry with biologgers (e.g., jaw-motion sensors), it is possible to monitor individual feeding events. In addition, other devices on instrumented animals can communicate with one another, providing insights into predator-prey interactions and social behavior. Coupling telemetry with minute nonlethal biopsy allows understanding of how trophic dynamics, population connectivity, and gene-level basis for organismal health and condition relate to movement. These advances are revolutionizing the scope and scales of questions that can be addressed on the causes and consequences of animal distribution and movement. OUTLOOK Aquatic animal telemetry has advanced rapidly, yet new challenges present themselves in coordination of monitoring across large-spatial scales (ocean basins), data sharing, and data assimilation. The continued advancement of aquatic telemetry lies in establishing and maintaining accessible and cost-effective infrastructure and in promoting multidisciplinary tagging approaches to maximize cost benefits. A united global network and centralized database will provide the mechanism for global telemetry data and will promote a transparent environment for data sharing that will, in turn, increase global communication, scope for collaboration, intellectual advancement, and funding opportunities. An overarching global network will realize the potential of telemetry, which is essential for advancing scientific knowledge and effectively managing globally shared aquatic resources and their ecosystems in the face of mounting human pressures and environmental change. Aquatic telemetry in action. A southern rock lobster (Jasus edwardsii) (A) and a lemon shark (Negaprion brevirostris) (D) fitted with acoustic tags are detected and logged by moored receivers (D) or mobile receivers attached to opportunistic platforms or carried by large animals (C). A juvenile green turtle (Chelonia mydas) (B) fitted with a satellite tag is monitored in real time via orbiting satellites. A grey seal (Halichoerus grypus) “bioprobe” (C), fitted with intercommunicating acoustic and satellite transmitters, transmits and receives data on animal interactions and ocean conditions. The distribution and interactions of aquatic organisms across space and time structure our marine, freshwater, and estuarine ecosystems. Over the past decade, technological advances in telemetry have transformed our ability to observe aquatic animal behavior and movement. These advances are now providing unprecedented ecological insights by connecting animal movements with measures of their physiology and environment. These developments are revolutionizing the scope and scale of questions that can be asked about the causes and consequences of movement and are redefining how we view and manage individuals, populations, and entire ecosystems. The next advance in aquatic telemetry will be the development of a global collaborative effort to facilitate infrastructure and data sharing and management over scales not previously possible.

Two decades of genetic profiling yields first evidence of natal philopatry and long‐term fidelity to parturition sites in sharks

Sharks are a globally threatened group of marine fishes that often breed in their natal region of origin. There has even been speculation that female sharks return to their exact birthplace to breed (‘natal philopatry’), which would have important conservation implications. Genetic profiling of lemon sharks (Negaprion brevirostris) from 20 consecutive cohorts (1993–2012) at Bimini, Bahamas, showed that certain females faithfully gave birth at this site for nearly two decades. At least six females born in the 1993–1997 cohorts returned to give birth 14–17 years later, providing the first direct evidence of natal philopatry in the chondrichthyans. Long‐term fidelity to specific nursery sites coupled with natal philopatry highlights the merits of emerging spatial and local conservation efforts for these threatened predators.

First record of living Manta alfredi × Manta birostris hybrid

Following a recent taxonomic revision, two manta species (Manta alfredi and Manta birostris ) have been advocated based on meristic and morphological characteristics (Marshall et al. 2009). Subsequent genetic analyses of the two species using mitochondrial and nuclear markers confirmed two distinguishable genetic groups (Kashiwagi et al. 2012). Using the above taxonomic and genetic criteria, we provide evidence for the first record of a living Manta alfredi ×Manta birostris hybrid. The Manta individual (Fig. 1a, b) was non-lethally sampled from a known manta aggregation site in Dunganab Bay, Sudan, Red Sea, in October 2012. The individual was identified in the field as Manta alfredi based on distinguishing morphological criteria: dorsoventral colouration/spot patterns, mouth and pectoral fin colouration, and absence of remnant spine (Fig. 1b; Marshall et al. 2009). DNA was recovered from a fin clip using standard molecular genetic protocols. The mitochondrial gene ND5 (1,154 bp) and nuclear gene RAG1 (646 bp) were amplified following Kashiwagi et al. (2012), and sequenced. Recovered sequences (GenBank accession nos. KF574269-KF574270) were aligned with those previously reported (Kashiwagi et al. 2012) and a haplotype network was constructed in TCS 1.21 (Clement et al. 2000). TheManta specimen was confirmed to carry a newManta alfredi mtDNA haplotype (red in Fig. 1). However, the RAG1 sequence indicates that this individual is an interspecific hybrid. The twoManta species are reciprocally monophyletic at the RAG1 locus, which contains two species-specific single nucleotide polymorphisms (SNPs): at position 73 (M . alfredi : G; M . birostris : A) and position 507 (M . alfredi : A; M . birostris : C) following Kashiwagi et al. (2012). The hybrid individual is heterozygous at both SNPs (see inset chromatograms). Heterozygosity was confirmed by sequencing this individual in triplicate in both forward and reverse directions at RAG1 . Our finding indicates that reproductive isolation among M . alfredi and M . birostris may be less complete than previously thought, or alternatively, that species-specific taxonomic and genetic differentiation is not as unambiguous as currently suggested. Given the designation of the two discrete species as vulnerable on the IUCN Red List and their recent listing on CITES appendix II following concern over increasing global R. P. Walter (*) : S. T. Kessel :A. T. Fisk :D. D. Heath : N. E. Hussey University of Windsor – GLIER, Windsor, Canada e-mail: rwalter@uwindsor.ca

Envisioning the Future of Aquatic Animal Tracking: Technology, Science, and Application

Electronic tags are significantly improving our understanding of aquatic animal behavior and are emerging as key sources of information for conservation and management practices. Future aquatic integrative biology and ecology studies will increasingly rely on data from electronic tagging. Continued advances in tracking hardware and software are needed to provide the knowledge required by managers and policymakers to address the challenges posed by the worlds changing aquatic ecosystems. We foresee multiplatform tracking systems for simultaneously monitoring the position, activity, and physiology of animals and the environment through which they are moving. Improved data collection will be accompanied by greater data accessibility and analytical tools for processing data, enabled by new infrastructure and cyberinfrastructure. To operationalize advances and facilitate integration into policy, there must be parallel developments in the accessibility of education and training, as well as solutions to key governance and legal issues.

Aerial Survey as a Tool to Estimate Abundance and Describe Distribution of a Carcharhinid Species, the Lemon Shark, Negaprion brevirostris

Aerial survey provides an important tool to assess the abundance of both terrestrial and marine vertebrates. To date, limited work has tested the effectiveness of this technique to estimate the abundance of smaller shark species. In Bimini, Bahamas, the lemon shark (Negaprion brevirostris) shows high site fidelity to a shallow sandy lagoon, providing an ideal test species to determine the effectiveness of localised aerial survey techniques for a Carcharhinid species in shallow subtropical waters. Between September 2007 and September 2008, visual surveys were conducted from light aircraft following defined transects ranging in length between 8.8 and 4.4 km. Count results were corrected for “availability”, “perception”, and “survey intensity” to provide unbiased abundance estimates. The abundance of lemon sharks was greatest in the central area of the lagoon during high tide, with a change in abundance distribution to the east and western regions of the lagoon with low tide. Mean abundance of sharks was estimated at 49 (±8.6) individuals, and monthly abundance was significantly positively correlated with mean water temperature. The successful implementation of the aerial survey technique highlighted the potential of further employment for shark abundance assessments in shallow coastal marine environments.

The Conservation of the Greenland Shark (Somniosus microcephalus): Setting Scientific, Law, and Policy Coordinates for Avoiding a Species at Risk

Sharks are among the most ancient predators on Earth, having roamed the oceans for more than 400 million years. Previously abundant and widespread, many populations have dwindled to a small fractio...

Risky business for a juvenile marine predator? Testing the influence of foraging strategies on size and growth rate under natural conditions

Mechanisms driving selection of body size and growth rate in wild marine vertebrates are poorly understood, thus limiting knowledge of their fitness costs at ecological, physiological and genetic scales. Here, we indirectly tested whether selection for size-related traits of juvenile sharks that inhabit a nursery hosting two dichotomous habitats, protected mangroves (low predation risk) and exposed seagrass beds (high predation risk), is influenced by their foraging behaviour. Juvenile sharks displayed a continuum of foraging strategies between mangrove and seagrass areas, with some individuals preferentially feeding in one habitat over another. Foraging habitat was correlated with growth rate, whereby slower growing, smaller individuals fed predominantly in sheltered mangroves, whereas larger, faster growing animals fed over exposed seagrass. Concomitantly, tracked juveniles undertook variable movement behaviours across both the low and high predation risk habitat. These data provide supporting evidence for the hypothesis that directional selection favouring smaller size and slower growth rate, both heritable traits in this shark population, may be driven by variability in foraging behaviour and predation risk. Such evolutionary pathways may be critical to adaptation within predator-driven marine ecosystems.

Conservation of reef manta rays (Manta alfredi) in a UNESCO World Heritage Site : large-scale island development or sustainable tourism?

A large reef manta ray (Manta alfredi) aggregation has been observed off the north Sudanese Red Sea coast since the 1950s. Sightings have been predominantly within the boundaries of a marine protected area (MPA), which was designated a UNESCO World Heritage Site in July 2016. Contrasting economic development trajectories have been proposed for the area (small-scale ecotourism and large-scale island development). To examine space-use, Wildlife Computers® SPOT 5 tags were secured to three manta rays. A two-state switching Bayesian state space model (BSSM), that allowed movement parameters to switch between resident and travelling, was fit to the recorded locations, and 50% and 95% kernel utilization distributions (KUD) home ranges calculated. A total of 682 BSSM locations were recorded between 30 October 2012 and 6 November 2013. Of these, 98.5% fell within the MPA boundaries; 99.5% for manta 1, 91.5% for manta 2, and 100% for manta 3. The BSSM identified that all three mantas were resident during 99% of transmissions, with 50% and 95% KUD home ranges falling mainly within the MPA boundaries. For all three mantas combined (88.4%), and all individuals (manta 1–92.4%, manta 2–64.9%, manta 3–91.9%), the majority of locations occurred within 15 km of the proposed large-scale island development. Results indicated that the MPA boundaries are spatially appropriate for manta rays in the region, however, a close association to the proposed large-scale development highlights the potential threat of disruption. Conversely, the focused nature of spatial use highlights the potential for reliable ecotourism opportunities.

Transcoelomic expulsion of an ingested foreign object by a carcharhinid shark

A wild lemon shark (Negaprion brevirostris) was observed to expel an ingested foreign object through its body wall, over a minimum period of 435 days. We observed this lemon shark at a recreational diving feeding site off the coast of Juno Beach (FL, USA) on 12 occasions between 6 December 2014 and 14 December 2016. At the final observation, following expulsion, we observed this lemon shark with scar tissue and in apparent healthy condition. At minimum, this lemon shark was able to survive for over 1 year under perforation of its stomach lining, coelom and body wall. This account provides further evidence for the resilience and recovery capabilities of elasmobranch fish.