Kim N. Holland

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.

Movement Patterns, Habitat Utilization, Home Range Size and Site Fidelity of Whitesaddle Goatfish, Parupeneus Porphyreus, In a Marine Reserve

Suitability of small (< 1 km2) marine reserves for protecting a commercially important endemic Hawaiian goatfish, Parupeneus porphyreus, was examined by quantifying goatfish habitat use, home range size and site fidelity in an existing marine reserve (Coconut Island in Kaneohe Bay, Hawaii). Five goatfish equipped with acoustic transmitters were tracked for up to 93 h each over 3–14 days. Daytime habitat use patterns of two of these fish were continuously monitored for one month using a fixed hydrophone hardwired to an onshore computer. Acoustically tagged fish showed consistent diel patterns of behavior, refuging in holes in the reef by day and moving over extensive areas of sand and coral rubble habitat at night. Remote monitoring of daytime habitat use by two goatfish revealed that the same daytime refuge was used by both fish for at least one month (the battery life of the transmitters). Home ranges of all fish were within the boundaries of the Coconut Island reserve suggesting that even small areas containing suitable habitat can make effective reserves for this species. A relatively low abundance of reproductive size P. porphyreus at Coconut Island in comparison with deeper areas may indicate an ontogenetic shift to deeper habitat in this species.

Movements and dispersal patterns of blue trevally (Caranx melampygus) in a fisheries conservation zone

Abstract The short- and long-term movement patterns of blue trevally (Caranx melampygus) were monitored using a combination of sonic tracking and tag-and-release techniques. All fish were captured and released on the patch reef surrounding Coconut Island in Kaneohe Bay, Oahu, Hawaii, which has been a no-fishing conservation zone for over 30 years. Sonic tracking produced fine-scale movement data from five fish for periods spanning up to 18 days. All fish displayed diel movement patterns within consistent home ranges, which encompassed different parts of the reef during the night than during the day. Movements were predominantly along the walls of the patch reef, with occasional forays to nearby sections of adjacent reefs. Four hundred and ten fish were tagged and released on the Coconut Island reef, and the recapture sites of 85 recaptured fish indicated that most did not move far from their point of release; 75.5% were recaptured within 0.5 km of their release points. Time at liberty ranged from 4 to 454 days, and distance between release and recapture sites was not related to time at liberty. Some fish were observed many times in the same areas over periods of several months. Both the tracking and recapture data indicate strong site fidelity in this species and low occurrence of long distance emigration. These behavioral traits suggest that successful husbandry of this species may be accomplished through the use of management practices such as establishing no-fishing zones.

Movement patterns, home range size and habitat utilization of the bluespine unicornfish, Naso unicornis (Acanthuridae) in a Hawaiian marine reserve

SynopsisWe quantified bluespine unicornfish, Naso unicornis, movement patterns, home range size and habitat preferences in a small Hawaiian marine reserve. Bluespine unicornfish were site-attached to home ranges situated within the reserve boundaries and their movements were aligned with topographic features. Two different diel movement patterns (‘commuting’ and ‘foraying’) were observed. Commuters made crepuscular migrations of several hundred meters between daytime foraging areas and nighttime refuge holes. Foraying fish did not partake in crepuscular migrations and utilized refuge holes both day and night. Two bluespine unicornfish were also nocturnally active. There was little direct evidence of dispersal from the reserve but differences in bluespine unicornfish abundance and size among reef habitat zones were consistent with ontogenetic habitat shifts. The influence of habitat topography on bluespine unicornfish movements suggests that gross habitat characteristics could be used to predict reef fish movements. This could provide a simple method for setting marine reserve boundaries at sites for which empirical fish movement data are unavailable.

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.

Daily movements, habitat use, and submergence intervals of normal and tumor-bearing juvenile green turtles (Chelonia mydas L.) within a foraging area in the Hawaiian islands

Depth-sensitive ultrasonic transmitters monitored the horizontal and vertical movements of 12 juvenile (<65 cm carapace length) green turtles (Chelonia mydas L.) in Kaneohe Bay, Oahu (Hawaii, USA). This site was chosen because of its accessibility, its importance as a foraging area, and the high incidence (≈50%) of fibropapillomatosis, a tumor disease of unknown etiology. Our objectives were to determine the daily movements, habitat use, and submergence intervals of normal and tumor-bearing animals. The presence of tumors had no obvious effects on movement patterns or habitat use. All turtles remained within a small portion of the bay where patch reefs and shallow coral-covered areas are common, and algal growth most abundant. During daylight, two normal and two tumor-bearing animals remained within known feeding areas, all other turtles studied stayed within deep mud bottom channels or within crevices on the sides of reefs. All, except one tumor-bearing turtle, moved up on to shallow patch reefs or shallow coral-covered areas at night. Submergence intervals for both groups were short (over 90% were 33 min or less and none exceeded 66 min) compared to maximum breath-hold times (up to 5 h) measured in the laboratory by earlier workers. Juvenile green turtles in Hawaii, therefore, most likely maintain aerobic metabolism while submerged and surface before oxygen stores are significantly depleted. Tumor-bearing turtles had a higher frequency of longer submergence intervals during the night, indicating they may have been somewhat less active at night. Normal turtles showed no such day-night difference.

Global phylogeography with mixed-marker analysis reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini).

Background The scalloped hammerhead shark, Sphyrna lewini, is a large endangered predator with a circumglobal distribution, observed in the open ocean but linked ontogenetically to coastal embayments for parturition and juvenile development. A previous survey of maternal (mtDNA) markers demonstrated strong genetic partitioning overall (global ΦST = 0.749) and significant population separations across oceans and between discontinuous continental coastlines. Methodology/Principal Findings We surveyed the same global range with increased sample coverage (N = 403) and 13 microsatellite loci to assess the male contribution to dispersal and population structure. Biparentally inherited microsatellites reveal low or absent genetic structure across ocean basins and global genetic differentiation (F ST = 0.035) over an order of magnitude lower than the corresponding measures for maternal mtDNA lineages (ΦST = 0.749). Nuclear allelic richness and heterozygosity are high throughout the Indo-Pacific, while genetic structure is low. In contrast, allelic diversity is low while population structure is higher for populations at the ends of the range in the West Atlantic and East Pacific. Conclusions/Significance These data are consistent with the proposed Indo-Pacific center of origin for S. lewini, and indicate that females are philopatric or adhere to coastal habitats while males facilitate gene flow across oceanic expanses. This study includes the largest sampling effort and the most molecular loci ever used to survey the complete range of a large oceanic predator, and findings emphasize the importance of incorporating mixed-marker analysis into stock assessments of threatened and endangered shark species.

Scales of orientation, directed walks and movement path structure in sharks

1. Animal search patterns reflect sensory perception ranges combined with memory and knowledge of the surrounding environment. 2. Random walks are used when the locations of resources are unknown, whereas directed walks should be optimal when the location of favourable habitats is known. However, directed walks have been quantified for very few species. 3. We re-analysed tracking data from three shark species to determine whether they were using directed walks, and if so, over which spatial scales. Fractal analysis was used to quantify how movement structure varied with spatial scale and determine whether the sharks were using patches. 4. Tiger sharks performed directed walks at large spatial scales (at least 6-8 km). Thresher sharks also showed directed movement (at scales of 400-1900 m), and adult threshers were able to orient at greater scales than juveniles, which may suggest that learning improves the ability to perform directed walks. Blacktip reef sharks had small home ranges, high site fidelity and showed no evidence of oriented movements at large scales. 5. There were inter- and intraspecific differences in path structure and patch size, although most individuals showed scale-dependent movements. Furthermore, some individuals of each species performed movements similar to a correlated random walk. 6. Sharks can perform directed walks over large spatial scales, with scales of movements reflecting site fidelity and home range size. Understanding when and where directed walks occur is crucial for developing more accurate population-level dispersal models.

Sharks can detect changes in the geomagnetic field

We used behavioural conditioning to demonstrate that sharks can detect changes in the geomagnetic field. Captive sharks were conditioned by pairing activation of an artificial magnetic field with presentation of food over a target. Conditioned sharks subsequently converged on the target when the artificial magnetic field was activated but no food reward was presented thereby demonstrating that they were able to sense the altered magnetic field. This strong response provides a robust behavioural assay that could be used to determine how sharks detect magnetic fields and to measure detection thresholds.

Seasonal cycles and long-term trends in abundance and species composition of sharks associated with cage diving ecotourism activities in Hawaii

Shark cage diving is both popular and controversial, with proponents citing educational value and non-extractive use of natural resources and opponents raising concerns about public safety and ecological impacts. Logbook data collected 2004–2008 from two Oahu (Hawaii) shark cage diving operations were analysed to determine whether such voluntary records provide useful insights into shark ecology or ecotourism impacts. Operators correctly identified common shark species and documented gross seasonal cycles and long-term trends in abundance of Galapagos ( Carcharhinus galapagensis ), sandbar ( Carcharhinus plumbeus ) and tiger sharks ( Galeorcerdo cuvier ). Annual cycles in shark abundance may indicate seasonal migrations, whereas long-term trends suggest gradual exclusion of smaller sandbar sharks from cage diving sites. Numerically dominant (> 98%) Galapagos and sandbar sharks are rarely implicated in attacks on humans. Negligible impact on public safety is supported by other factors such as: (1) remoteness of the sites, (2) conditioning stimuli that are specific to the tour operations and different from inshore recreational stimuli and (3) no increase in shark attacks on the north coast of Oahu since cage diving started. Tracking studies are required to validate logbook data and to determine whether sharks associated with offshore cage diving travel into inshore areas used for in-water recreation.