Diel vertical migration is a widespread behavioral phenomenon where organisms migrate through the water column and may modify behavior relative to changing environmental conditions based on ...physiological tolerances. Here, we combined a novel suite of biologging technologies to examine the thermal physiology (intramuscular temperature), fine-scale swimming behavior and activity (overall dynamic body acceleration as a proxy for energy expenditure) of bluntnose sixgill sharks (Hexanchus griseus) in response to environmental changes (depth, water temperature, dissolved oxygen) experienced during diel vertical migrations. In the subtropical waters off Hawai'i, sixgill sharks undertook pronounced diel vertical migrations and spent considerable amounts of time in cold (5-7°C), low oxygen conditions (10-25% saturation) during their deeper daytime distribution. Further, sixgill sharks spent the majority of their deeper daytime distribution with intramuscular temperatures warmer than ambient water temperatures, thereby providing them with a significant thermal advantage over non-vertically migrating and smaller-sized prey. Sixgill sharks exhibited relatively high rates of activity during both shallow (night) and deep (day) phases and contrary to our predictions, did not reduce activity levels during their deeper daytime distribution while experiencing low temperature and dissolved oxygen levels. This demonstrates an ability to tolerate the low oxygen conditions occurring within the local oxygen minimum zone. The novel combination of biologging technologies used here enabled innovative in situ deep-sea natural experiments and provided significant insight into the behavioral and physiological ecology of an ecologically important deepwater species.
The use of fish aggregating devices (FADs) by purse seine fisheries has come under increasing criticism for its potential deleterious impacts on tuna stocks, for high levels of by‐catch and threats ...to the biodiversity of tropical pelagic ecosystems. Here, we review the current state of scientific knowledge of this fishing technique and current management strategies. Our intent is to encourage objective discussion of the topic and highlight areas worthy of future research. We show that catching juvenile tuna around FADs does not necessarily result in overfishing of stocks, although more selective fishing techniques would likely help obtain higher yield. Levels of non‐tuna by‐catch are comparable to or less than in other commercial tuna fisheries and are primarily comprised of species that are not considered threatened. Accordingly, to minimize impacts on ecosystem balance, there is merit in considering that all species captured in purse seine fisheries (excluding vulnerable species such as turtles and sharks) should be retained, but the consequences of such a measure should be carefully examined before implementation. The take of vulnerable species could be further reduced by introduction of additional mitigation measures, but their potential benefits would be limited without parallel efforts with other gears. Finally, there is no unequivocal empirical evidence that FADs represent an ‘ecological trap’ that inherently disrupts tuna biology although further research should focus on this issue. We encourage RFMOs to expand and improve their FAD management plans. Under appropriate management regimes, FAD fishing could be an ecologically and economically sensible fishing method.
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.
Animals are often faced with complex movement decisions, particularly those that involve long‐distance dispersal. Partial migrations, ubiquitous among all groups of vertebrates, are a form of ...long‐distance movement that occurs when only some of the animals in a population migrate. The decision to migrate or to be a resident can be dependent on many factors, but these factors are rarely quantified in fishes, particularly top predators, even though partial migrations may have important implications for ecosystem dynamics and conservation. We utilized passive acoustic telemetry, with a Brownian bridge movement model and generalized additive mixed models, to explore the factors regulating partial migration in a large marine predator, the tiger shark, throughout the Hawaiian Islands. Although sharks tended to utilize a particular “core” island, they also demonstrated inter‐island movements, particularly mature females that would swim from the northwestern Hawaiian Islands to the main Hawaiian Islands (MHI). Immigration to another island was a function of season, sea surface temperature (SST), and chlorophyll a concentration. Our results predict that 25% of mature females moved from remote French Frigate Shoals atoll to the MHI during late summer/early fall, potentially to give birth. Females with core home ranges within the MHI showed limited movements to the NWHI, and immigration to an island was better explained by SST and chlorophyll a concentration, suggesting a foraging function. Dispersal patterns in tiger sharks are complex but can be considered a mix of skipped‐breeding partial migration by mature females and individual‐based inter‐island movements potentially linked to foraging. Therefore, sharks appear to use a conditional strategy based on fixed intrinsic and flexible extrinsic states. The application of Brownian bridge movement models to electronic presence/absence data provides a new technique for assessing the influence of habitat and environmental conditions on patterns of movement for fish populations.
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 world’s 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.
We equipped individual tiger (Galeocerdo cuvier Péron and Lesueur, 1822) and Galapagos (Carcharhinus galapagensis Snodgrass and Heller, 1905) sharks with both acoustic and satellite transmitters to ...quantify their long-term movements in the Papahanaumokuakea Marine National Monument (Northwestern Hawaiian Islands). Tiger sharks exhibited two broad patterns of behavior. Some individuals were detected at French Frigate Shoals (FFS) year round, whereas others visited FFS atoll in summer to forage on fledging albatross, then swam thousands of kilometers along the Hawaiian chain, or out into open ocean to the North Pacific transition zone chlorophyll front, before returning to FFS in subsequent years. These patterns suggest tiger sharks may use cognitive maps to navigate between distant foraging areas. Different patterns of spatial behavior may arise because cognitive maps are built up through individual exploration, and each tiger shark learns a unique combination of foraging sites. Galapagos shark detections were all associated with FFS, suggesting these sharks may be more resident around oceanic islands. Both Galapagos and tiger sharks primarily used the mixed layer (<100 m depth) and made occasional deeper dives through the thermocline down to 680 m. Results show reef-associated sharks utilize a wide variety of habitats ranging from shallow atoll lagoons to deep reefs and open ocean and may provide important trophic links between these habitats.
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 Φ(ST) = 0.749) and significant population separations across oceans and between discontinuous continental coastlines.
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 (Φ(ST) = 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.
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.
Identification of nursery habitats and knowledge of the trophic ecology and habitat use of juvenile fishes within these habitats are fundamental in developing sound management and conservation ...strategies. The brown stingray Dasyatis lata is a large benthic predator that inhabits the coastal waters of Hawai'i. Although abundant in these ecosystems, little is known about its basic ecology. Stomach content, bulk and amino acid stable isotope analyses were used to assess diet and habitat use of juvenile brown stingrays and to examine the possibility of competitive interactions with juvenile scalloped hammerhead sharks Sphyrna lewini that are sympatric with brown stingrays in Kane'ohe Bay, Oahu. Based on stomach contents, brown stingrays fed almost exclusively on crustaceans. An ontogenetic shift in stingray diet and an increase in relative trophic position (TP) were apparent from stomach content and stable isotope analysis. Stingray bulk delta super(13)C and delta super(15)N values indicated long-term foraging fidelity to subregions of the bay. Use of Kane'ohe Bay as a nursery habitat was supported by nitrogen isotopic analysis of individual amino acids from stingray muscle samples. Our results clearly demonstrated that stingrays foraged within the bay for the majority of their juvenile lives then shifted to offshore habitats with the onset of sexual maturity. Trophic enrichment factors used to estimate TPs from amino acid analysis in previous studies may underestimate TPs in elasmobranchs owing to urea retention for osmoregulation. Potential prey resources were partitioned between stingrays and juvenile scalloped hammerhead sharks, and TP estimates from each analytical method indicated that juvenile scalloped hammerhead sharks forage on higher TP prey than do juvenile brown stingrays. These results show that the study of foraging ecology and habitat use of marine animals can greatly benefit from integrating traditional stomach content and bulk stable isotopic analyses with nitrogen isotopic analyses of individual amino acids.
Tiger sharks (Galecerdo cuvier) are apex predators characterized by their broad diet, large size and rapid growth. Tiger shark maximum size is typically between 380 & 450 cm Total Length (TL), with a ...few individuals reaching 550 cm TL, but the maximum size of tiger sharks in Hawaii waters remains uncertain. A previous study suggested tiger sharks grow rather slowly in Hawaii compared to other regions, but this may have been an artifact of the method used to estimate growth (unvalidated vertebral ring counts) compounded by small sample size and narrow size range. Since 1993, the University of Hawaii has conducted a research program aimed at elucidating tiger shark biology, and to date 420 tiger sharks have been tagged and 50 recaptured. All recaptures were from Hawaii except a single shark recaptured off Isla Jacques Cousteau (24°13'17″N 109°52'14″W), in the southern Gulf of California (minimum distance between tag and recapture sites = approximately 5,000 km), after 366 days at liberty (DAL). We used these empirical mark-recapture data to estimate growth rates and maximum size for tiger sharks in Hawaii. We found that tiger sharks in Hawaii grow twice as fast as previously thought, on average reaching 340 cm TL by age 5, and attaining a maximum size of 403 cm TL. Our model indicates the fastest growing individuals attain 400 cm TL by age 5, and the largest reach a maximum size of 444 cm TL. The largest shark captured during our study was 464 cm TL but individuals >450 cm TL were extremely rare (0.005% of sharks captured). We conclude that tiger shark growth rates and maximum sizes in Hawaii are generally consistent with those in other regions, and hypothesize that a broad diet may help them to achieve this rapid growth by maximizing prey consumption rates.
We report the results of a series of experiments to test the utility of acceleration data-loggers for determining the energy expenditure of juvenile hammerhead sharks (
Sphyrna lewini). In one ...experiment, three sharks were instrumented with miniature acceleration data-loggers and swum in a Brett-style respirometer at a range of speeds. For all three sharks, significant linear relationships were obtained between mean oxygen consumption (M
·o
2) and Partial Dynamic Body Acceleration in the lateral and dorso-ventral axes (PDBA
y,
z
) with high predictive power (
r
2
>
0.71). In a second experiment, PDBA was measured for sharks swimming freely in circular tanks. The free-swimming sharks exhibited wide ranges of PDBA
y,
z
; routine swimming was characterised by low PDBA
y,
z
(0.01–0.12
g) whereas unsteady swimming, (especially fast-start swimming of >
1
g) was characterised by high PDBA
y,
z
. Despite initial evidence of linearity in the oxygen consumption vs. PDBA relationship, incorporating previous estimates of standard metabolic rate of hammerhead sharks suggests a non-linear fit. Further work is needed to establish the exact shape of the relationship beyond the narrow range of speeds that hammerhead pups could be exercised in this study, particularly the low swimming speeds which are frequently observed in free-swimming animals.
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