Joanna Mills Flemming

ROBUST STATE–SPACE MODELING OF ANIMAL MOVEMENT DATA

Remotely sensed tracking data collected on animal movement is vastly un- derutilized due to a lack of statistical tools for appropriate analysis. Features of such data that make analysis particularly challenging include the presence of estimation errors that are non-Gaussian and vary in time, observations that occur irregularly in time, and com- plexity in the underlying behavioral processes. We develop a state-space framework that simultaneously deals with these features and demonstrate our method by analyzing three seal pathway data sets. We show how known information regarding error distributions can be used to improve inference of the underlying process(es) and demonstrate that our frame- work provides a powerful and flexible method for fitting different behavioral models to tracking data.

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.

META‐ANALYSIS OF ANIMAL MOVEMENT USING STATE‐SPACE MODELS

The study of animal movement and behavior is being revolutionized by technology, such as satellite tags and harmonic radar, that allows us to track the movements of individual animals. However, our ability to analyze and model such data has lagged behind the sophisticated collection methods. We review problems with current methods and suggest a more powerful and flexible approach, state-space modeling, and we illustrate how these models can be posed in a meta-analytic framework so that information from individual trajectories may be combined optimally. State-space models enable us to deal with the complexity of modeling animals interacting with their environment but, unlike other methods, they allow simultaneous estimation of measurement error and process noise that are inherent in animal-trajectory data. A Bayesian framework allows us to incorporate important prior information when available and also allows meta-analytic techniques to be incorporated in a straightforward fashion. Meta-analysis enables both individual and broader-level inference from observations of multiple individual pathways. Our approach is powerful because it allows researchers to test hypotheses regarding animal movement, to connect theoretical models to data, and to use modern likelihood-based estimation techniques, all under a single statistical framework.

Rapid Global Expansion of Invertebrate Fisheries: Trends, Drivers, and Ecosystem Effects

Background Worldwide, finfish fisheries are receiving increasing assessment and regulation, slowly leading to more sustainable exploitation and rebuilding. In their wake, invertebrate fisheries are rapidly expanding with little scientific scrutiny despite increasing socio-economic importance. Methods and Findings We provide the first global evaluation of the trends, drivers, and population and ecosystem consequences of invertebrate fisheries based on a global catch database in combination with taxa-specific reviews. We also develop new methodologies to quantify temporal and spatial trends in resource status and fishery development. Since 1950, global invertebrate catches have increased 6-fold with 1.5 times more countries fishing and double the taxa reported. By 2004, 34% of invertebrate fisheries were over-exploited, collapsed, or closed. New fisheries have developed increasingly rapidly, with a decrease of 6 years (3 years) in time to peak from the 1950s to 1990s. Moreover, some fisheries have expanded further and further away from their driving market, encompassing a global fishery by the 1990s. 71% of taxa (53% of catches) are harvested with habitat-destructive gear, and many provide important ecosystem functions including habitat, filtration, and grazing. Conclusions Our findings suggest that invertebrate species, which form an important component of the basis of marine food webs, are increasingly exploited with limited stock and ecosystem-impact assessments, and enhanced management attention is needed to avoid negative consequences for ocean ecosystems and human well-being.

Overestimating Fish Counts by Non-Instantaneous Visual Censuses: Consequences for Population and Community Descriptions

Background Increasingly, underwater visual censuses (UVC) are used to assess fish populations. Several studies have demonstrated the effectiveness of protected areas for increasing fish abundance or provided insight into the natural abundance and structure of reef fish communities in remote areas. Recently, high apex predator densities (>100,000 individuals·km−2) and biomasses (>4 tonnes·ha−1) have been reported for some remote islands suggesting the occurrence of inverted trophic biomass pyramids. However, few studies have critically evaluated the methods used for sampling conspicuous and highly mobile fish such as sharks. Ideally, UVC are done instantaneously, however, researchers often count animals that enter the survey area after the survey has started, thus performing non-instantaneous UVC. Methodology/Principal Findings We developed a simulation model to evaluate counts obtained by divers deploying non-instantaneous belt-transect and stationary-point-count techniques. We assessed how fish speed and survey procedure (visibility, diver speed, survey time and dimensions) affect observed fish counts. Results indicate that the bias caused by fish speed alone is huge, while survey procedures had varying effects. Because the fastest fishes tend to be the largest, the bias would have significant implications on their biomass contribution. Therefore, caution is needed when describing abundance, biomass, and community structure based on non-instantaneous UVC, especially for highly mobile species such as sharks. Conclusions/Significance Based on our results, we urge that published literature state explicitly whether instantaneous counts were made and that survey procedures be accounted for when non-instantaneous counts are used. Using published density and biomass values of communities that include sharks we explore the effect of this bias and suggest that further investigation may be needed to determine pristine shark abundances and the existence of inverted biomass pyramids. Because such studies are used to make important management and conservation decisions, incorrect estimates of animal abundance and biomass have serious and significant implications.

Recovery Trends in Marine Mammal Populations

Marine mammals have greatly benefitted from a shift from resource exploitation towards conservation. Often lauded as symbols of conservation success, some marine mammal populations have shown remarkable recoveries after severe depletions. Others have remained at low abundance levels, continued to decline, or become extinct or extirpated. Here we provide a quantitative assessment of (1) publicly available population-level abundance data for marine mammals worldwide, (2) abundance trends and recovery status, and (3) historic population decline and recent recovery. We compiled 182 population abundance time series for 47 species and identified major data gaps. In order to compare across the largest possible set of time series with varying data quality, quantity and frequency, we considered an increase in population abundance as evidence of recovery. Using robust log-linear regression over three generations, we were able to classify abundance trends for 92 spatially non-overlapping populations as Significantly Increasing (42%), Significantly Decreasing (10%), Non-Significant Change (28%) and Unknown (20%). Our results were comparable to IUCN classifications for equivalent species. Among different groupings, pinnipeds and other marine mammals (sirenians, polar bears and otters) showed the highest proportion of recovering populations, likely benefiting from relatively fast life histories and nearshore habitats that provided visibility and protective management measures. Recovery was less frequent among cetaceans, but more common in coastal than offshore populations. For marine mammals with available historical abundance estimates (n = 47), larger historical population declines were associated with low or variable recent recoveries so far. Overall, our results show that many formerly depleted marine mammal populations are recovering. However, data-deficient populations and those with decreasing and non-significant trends require attention. In particular, increased study of populations with major data gaps, including offshore small cetaceans, cryptic species, and marine mammals in low latitudes and developing nations, is needed to better understand the status of marine mammal populations worldwide.

Shifting elasmobranch community assemblage at Cocos Island—an isolated marine protected area

Fishing pressure has increased the extinction risk of many elasmobranch (shark and ray) species. Although many countries have established no-take marine reserves, a paucity of monitoring data means it is still unclear if reserves are effectively protecting these species. We examined data collected by a small group of divers over the past 21 years at one of the worlds oldest marine protected areas (MPAs), Cocos Island National Park, Costa Rica. We used mixed effects models to determine trends in relative abundance, or probability of occurrence, of 12 monitored elasmobranch species while accounting for variation among observers and from abiotic factors. Eight of 12 species declined significantly over the past 2 decades. We documented decreases in relative abundance for 6 species, including the iconic scalloped hammerhead shark (Sphyrna lewini) (-45%), whitetip reef shark (Triaenodon obesus) (-77%), mobula ray (Mobula spp.) (-78%), and manta ray (Manta birostris) (-89%), and decreases in the probability of occurrence for 2 other species. Several of these species have small home ranges and should be better protected by an MPA, which underscores the notion that declines of marine megafauna will continue unabated in MPAs unless there is adequate enforcement effort to control fishing. In addition, probability of occurrence at Cocos Island of tiger (Galeocerdo cuvier), Galapagos (Carcharhinus galapagensis), blacktip (Carcharhinus limbatus), and whale (Rhincodon typus) sharks increased significantly. The effectiveness of MPAs cannot be evaluated by examining single species because population responses can vary depending on life history traits and vulnerability to fishing pressure.

Trends in the exploitation of South Atlantic shark populations

Approximately 25% of globally reported shark catches occur in Atlantic pelagic longline fisheries. Strong declines in shark populations have been detected in the North Atlantic, whereas in the South Atlantic the situation is less clear, although fishing effort has been increasing in this region since the late 1970s. We synthesized information on shark catch rates (based on 871,177 sharks caught on 86,492 longline sets) for the major species caught by multiple fleets in the South Atlantic between 1979 and 2011. We complied records from fishing logbooks of fishing companies, fishers, and onboard observers that were supplied to Brazilian institutions. By using exploratory data analysis and literature sources, we identified 3 phases of exploitation in these data (Supporting Information). From 1979 to 1997 (phase A), 5 fleets (40 vessels) fished mainly for tunas. From 1998 to 2008 (phase B), 20 fleets (100 vessels) fished for tunas, swordfishes, and sharks. From 2008 to 2011 (phase C), 3 fleets (30 vessels) fished for multiple species, but restrictive measures were implemented. We used generalized linear models to standardize catch rates and identify trends in each of these phases. Shark catch rates increased from 1979 to 1997, when fishing effort was low, decreased from 1998 to 2008, when fishing effort increased substantially, and remained stable or increased from 2008 to 2011, when fishing effort was again low. Our results indicate that most shark populations affected by longlines in the South Atlantic are currently depleted, but these populations may recover if fishing effort is reduced accordingly. In this context, it is problematic that comprehensive data collection, monitoring, and management of these fisheries ceased after 2012. Concurrently with the fact that Brazil is newly identified by FAO among the largest (and in fastest expansion) shark sub-products consumer market worldwide.

Fast fitting of non‐Gaussian state‐space models to animal movement data via Template Model Builder

State-space models (SSM) are often used for analyzing complex ecological processes that are not observed directly, such as marine animal movement. When outliers are present in the measurements, special care is needed in the analysis to obtain reliable location and process estimates. Here we recommend using the Laplace approximation combined with automatic differentiation (as implemented in the novel R package Template Model Builder; TMB) for the fast fitting of continuous-time multivariate non-Gaussian SSMs. Through Argos satellite tracking data, we demonstrate that the use of continuous-time t-distributed measurement errors for error-prone data is more robust to outliers and improves the location estimation compared to using discretized-time t-distributed errors (implemented with a Gibbs sampler) or using continuous-time Gaussian errors (as with the Kalman filter). Using TMB, we are able to estimate additional parameters compared to previous methods, all without requiring a substantial increase in computational time. The model implementation is made available through the R package argosTrack.

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.