John F. Kocik

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.

A Vulnerability Assessment of Fish and Invertebrates to Climate Change on the Northeast U.S. Continental Shelf.

Climate change and decadal variability are impacting marine fish and invertebrate species worldwide and these impacts will continue for the foreseeable future. Quantitative approaches have been developed to examine climate impacts on productivity, abundance, and distribution of various marine fish and invertebrate species. However, it is difficult to apply these approaches to large numbers of species owing to the lack of mechanistic understanding sufficient for quantitative analyses, as well as the lack of scientific infrastructure to support these more detailed studies. Vulnerability assessments provide a framework for evaluating climate impacts over a broad range of species with existing information. These methods combine the exposure of a species to a stressor (climate change and decadal variability) and the sensitivity of species to the stressor. These two components are then combined to estimate an overall vulnerability. Quantitative data are used when available, but qualitative information and expert opinion are used when quantitative data is lacking. Here we conduct a climate vulnerability assessment on 82 fish and invertebrate species in the Northeast U.S. Shelf including exploited, forage, and protected species. We define climate vulnerability as the extent to which abundance or productivity of a species in the region could be impacted by climate change and decadal variability. We find that the overall climate vulnerability is high to very high for approximately half the species assessed; diadromous and benthic invertebrate species exhibit the greatest vulnerability. In addition, the majority of species included in the assessment have a high potential for a change in distribution in response to projected changes in climate. Negative effects of climate change are expected for approximately half of the species assessed, but some species are expected to be positively affected (e.g., increase in productivity or move into the region). These results will inform research and management activities related to understanding and adapting marine fisheries management and conservation to climate change and decadal variability.

Visibility of Visual Implant Elastomer Tags in Atlantic Salmon Reared for Two Years in Marine Net-Pens

Abstract We evaluated detectability of visual implant elastomer (VIE) tags in individual Atlantic salmon Salmo salar reared from smolts to adults in commercial marine net-pens. A total of 9,000 individual smolts were marked (adipose eye, lower jaw, or both) with colored VIE tags. During the period from March 1998 to December 2000 (2–28 months after tagging) a total of 3,220 fish were visually inspected for VIE tags. Tag detection rates remained high (>90%) for the first 17 months after tagging but then declined sharply, particularly for VIEs in the jaw. Use of a UV light significantly increased detection of both eye and jaw VIE tags. We conclude that VIE tags are optimal for use in Atlantic salmon when recovery of fish occurs within 17 months of tagging.

Linking Behavior, Physiology, and Survival of Atlantic Salmon Smolts During Estuary Migration

Abstract Decreased marine survival is identified as a component driver of continued declines of Atlantic Salmon Salmo salar. However, estimates of marine mortality often incorporate loss incurred during estuary migration that may be mechanistically distinct from factors affecting marine mortality. We examined movements and survival of 941 smolts (141 wild and 800 hatchery-reared fish) released in freshwater during passage through the Penobscot River estuary, Maine, from 2005 to 2013. We related trends in estuary arrival date, movement rate, and survival to fish characteristics, migratory history, and environmental conditions in the estuary. Fish that experienced the warmest thermal history arrived in the estuary 8 d earlier than those experiencing the coolest thermal history during development. Estuary arrival date was 10 d later for fish experiencing high flow than for fish experiencing low flow. Fish released furthest upstream arrived in the estuary 3 d later than those stocked further downstream but moved 0.5 km/h faster through the estuary. Temporally, movement rate and survival in the estuary both peaked in mid-May. Spatially, movement rate and survival both decreased from freshwater to the ocean. Wild smolts arrived in the estuary later than hatchery fish, but we observed no change in movement rate or survival attributable to rearing history. Fish with the highest gill Na+, K+-ATPase activity incurred 25% lower mortality through the estuary than fish with the lowest gill Na+, K+-ATPase activity. Smolt survival decreased (by up to 40%) with the increasing number of dams passed (ranging from two to nine) during freshwater migration. These results underscore the importance of physiological preparedness on performance and the delayed, indirect effects of dams on survival of Atlantic Salmon smolts during estuary migration, ultimately affecting marine survival estimates.

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.

Use of Riffle and Run Habitats with Aquatic Vegetation by Juvenile Atlantic Salmon

Abstract We examined the use of riffle and run habitats with varying aquatic macrophyte coverage by juvenile Atlantic salmon Salmo salar in the Narraguagus River, Maine, via electrofishing and individual fish observations. At the site level, large and small parr were more abundant in riffle habitats than in run habitats, and the abundance of small parr was lower at sites with heavy aquatic vegetation. At the individual-fish level, parr use of moderately vegetated areas was significantly higher than expected based on availability of such habitats, and use of heavily vegetated areas was lower than expected. The use of vegetated areas was not independent of dominant substrate type. Use of moderately vegetated habitats exceeded expectations for gravel- and sand-dominated areas; for cobble-dominated areas, use of sites with little or no vegetation exceeded expectations. Approximately 95% of the observed parr were found in the vicinity of a discrete cover item (i.e., cobble, vegetation, or other). Parr typicall...

Collaboration between Atlantic and Pacific salmon biologists to enhance recovery of endangered salmon in North America

Salmon hold an iconic status along the Atlantic and Pacific coasts of North America, historically providing critical ecosystem services and substantial economic benefits to these regions. Overharvest, fish passage barriers and habitat destruction, in combination with other factors, have resulted in extirpation of approximately 30 % of Pacific (Oncorhynchus spp.) and 90 % of Atlantic salmon (Salmo salar) populations in the contiguous United States (Parrish et al. 1998; Gustafson et al. 2007). Many of the remaining native populations of Atlantic salmon, and Pacific salmon are protected under the U.S. Endangered Species Act (Ford 2011). Significant population declines are also occurring on both coasts in southern Canada (Irvine et al. 2005), where conservation actions are ongoing. This conservation crisis has resulted in extensive research to inform management decisions associated with recovery of endangered salmon populations. Collectively, there is a large and productive research effort in North America focused on conservation of endangered salmon populations. Numerous partnerships are in place to facilitate collaborations among researchers within each of the respective Pacific and Atlantic salmon research communities. In contrast, opportunities for sharing information across these two communities are less structured and usually occur on a small scale—e.g., at international meetings. Publications from these international meetings have typically been collections of concept papers each focused on Atlantic salmon or Pacific salmon (e.g., Lynch et al. 2002; Waples and Hendry 2008). Our goal was to help establish new collaborations between these highly productive research communities by teaming up Atlantic and Pacific salmon biologists. We organized a ‘‘Teaming Up’’ symposium that was held at the 2012 Annual Meeting of the American Fisheries Society in St. Paul, Minnesota, USA. This meeting helped connect scientists with similar interests and it was the catalyst for many new collaborative papers in this special issue. These new teams of Pacific and Atlantic salmon biologists identified areas where collaboration between these research communities W. R. Ardren (&) U.S. Fish and Wildlife Service, Western New England Complex, 11 Lincoln St., Essex Junction, VT 05452, USA e-mail: william_ardren@fws.gov