Managing the effects of multiple stressors on wildlife populations in their ecosystems: developing a cumulative risk approach.

Assessing cumulative effects of human activities on ecosystems is required by many jurisdictions, but current science cannot meet regulatory demands. Regulations define them as effect(s) of one human action combined with other actions. Here we argue for an approach that evaluates the cumulative risk of multiple stressors for protected wildlife populations within their ecosystems. Monitoring effects of each stressor is necessary but not sufficient to estimate how multiple stressors interact to affect wildlife populations. Examining the mechanistic pathways, from cellular to ecological, by which stressors affect individuals can help prioritize stressors and interpret how they interact. Our approach uses health indicators to accumulate the effects of stressors on individuals and to estimate changes in vital rates, driving population status. We advocate using methods well-established in human health and integrating them into ecosystem-based management to protect the health of commercially and culturally important wildlife populations and to protect against risk of extinction for threatened species. Our approach will improve abilities to conserve and manage ecosystems but will also demand significant increases in research and monitoring effort. We advocate for increased investment proportional to the economic scale of human activities in the Anthropocene and their pervasive effects on ecology and biodiversity.

Understanding the combined effects of multiple stressors: A new perspective on a longstanding challenge.

Wildlife populations and their habitats are exposed to an expanding diversity and intensity of stressors caused by human activities, within the broader context of natural processes and increasing pressure from climate change. Estimating how these multiple stressors affect individuals, populations, and ecosystems is thus of growing importance. However, their combined effects often cannot be predicted reliably from the individual effects of each stressor, and we lack the mechanistic understanding and analytical tools to predict their joint outcomes. We review the science of multiple stressors and present a conceptual framework that captures and reconciles the variety of existing approaches for assessing combined effects. Specifically, we show that all approaches lie along a spectrum, reflecting increasing assumptions about the mechanisms that regulate the action of single stressors and their combined effects. An emphasis on mechanisms improves analytical precision and predictive power but could introduce bias if the underlying assumptions are incorrect. A purely empirical approach has less risk of bias but requires adequate data on the effects of the full range of anticipated combinations of stressor types and magnitudes. We illustrate how this spectrum can be formalised into specific analytical methods, using an example of North Atlantic right whales feeding on limited prey resources while simultaneously being affected by entanglement in fishing gear. In practice, case-specific management needs and data availability will guide the exploration of the stressor combinations of interest and the selection of a suitable trade-off between precision and bias. We argue that the primary goal for adaptive management should be to identify the most practical and effective ways to remove or reduce specific combinations of stressors, bringing the risk of adverse impacts on populations and ecosystems below acceptable thresholds.

Understanding the population consequences of disturbance.

Managing the nonlethal effects of disturbance on wildlife populations has been a long-term goal for decision makers, managers, and ecologists, and assessment of these effects is currently required by European Union and United States legislation. However, robust assessment of these effects is challenging. The management of human activities that have nonlethal effects on wildlife is a specific example of a fundamental ecological problem: how to understand the population-level consequences of changes in the behavior or physiology of individual animals that are caused by external stressors. In this study, we review recent applications of a conceptual framework for assessing and predicting these consequences for marine mammal populations. We explore the range of models that can be used to formalize the approach and we identify critical research gaps. We also provide a decision tree that can be used to select the most appropriate model structure given the available data. Synthesis and applications: The implementation of this framework has moved the focus of discussion of the management of nonlethal disturbances on marine mammal populations away from a rhetorical debate about defining negligible impact and toward a quantitative understanding of long-term population-level effects. Here we demonstrate the framework's general applicability to other marine and terrestrial systems and show how it can support integrated modeling of the proximate and ultimate mechanisms that regulate trait-mediated, indirect interactions in ecological communities, that is, the nonconsumptive effects of a predator or stressor on a species' behavior, physiology, or life history.

The political biogeography of migratory marine predators.

During their migrations, marine predators experience varying levels of protection and face many threats as they travel through multiple countries' jurisdictions and across ocean basins. Some populations are declining rapidly. Contributing to such declines is a failure of some international agreements to ensure effective cooperation by the stakeholders responsible for managing species throughout their ranges, including in the high seas, a global commons. Here we use biologging data from marine predators to provide quantitative measures with great potential to inform local, national and international management efforts in the Pacific Ocean. We synthesized a large tracking data set to show how the movements and migratory phenology of 1,648 individuals representing 14 species-from leatherback turtles to white sharks-relate to the geopolitical boundaries of the Pacific Ocean throughout species' annual cycles. Cumulatively, these species visited 86% of Pacific Ocean countries and some spent three-quarters of their annual cycles in the high seas. With our results, we offer answers to questions posed when designing international strategies for managing migratory species.

Essential ocean variables for global sustained observations of biodiversity and ecosystem changes.

Sustained observations of marine biodiversity and ecosystems focused on specific conservation and management problems are needed around the world to effectively mitigate or manage changes resulting from anthropogenic pressures. These observations, while complex and expensive, are required by the international scientific, governance and policy communities to provide baselines against which the effects of human pressures and climate change may be measured and reported, and resources allocated to implement solutions. To identify biological and ecological essential ocean variables (EOVs) for implementation within a global ocean observing system that is relevant for science, informs society, and technologically feasible, we used a driver-pressure-state-impact-response (DPSIR) model. We (1) examined relevant international agreements to identify societal drivers and pressures on marine resources and ecosystems, (2) evaluated the temporal and spatial scales of variables measured by 100+ observing programs, and (3) analysed the impact and scalability of these variables and how they contribute to address societal and scientific issues. EOVs were related to the status of ecosystem components (phytoplankton and zooplankton biomass and diversity, and abundance and distribution of fish, marine turtles, birds and mammals), and to the extent and health of ecosystems (cover and composition of hard coral, seagrass, mangrove and macroalgal canopy). Benthic invertebrate abundance and distribution and microbe diversity and biomass were identified as emerging EOVs to be developed based on emerging requirements and new technologies. The temporal scale at which any shifts in biological systems will be detected will vary across the EOVs, the properties being monitored and the length of the existing time-series. Global implementation to deliver useful products will require collaboration of the scientific and policy sectors and a significant commitment to improve human and infrastructure capacity across the globe, including the development of new, more automated observing technologies, and encouraging the application of international standards and best practices.

Free-swimming northern elephant seals have low field metabolic rates that are sensitive to an increased cost of transport.

Widely ranging marine predators often adopt stereotyped, energy-saving behaviours to minimize the energetic cost of transport while maximizing energy gain. Environmental and anthropogenic disturbances can disrupt energy balance by prompting avoidance behaviours that increase transport costs, thereby decreasing foraging efficiency. We examined the ability of 12 free-ranging, juvenile northern elephant seals (Mirounga angustirostris) to mitigate the effects of experimentally increased transport costs by modifying their behaviour and/or energy use in a compensatory manner. Under normal locomotion, elephant seals had low energy requirements (106.5±28.2 kJ kg(-1) day(-1)), approaching or even falling below predictions of basal requirements. Seals responded to a small increase in locomotion costs by spending more time resting between dives (149±44 s) compared with matched control treatments (102±11 s; P<0.01). Despite incurred costs, most other dive and transit behaviours were conserved across treatments, including fixed, rhythmic swimming gaits. Because of this, and because each flipper stroke had a predictable effect on total costs (P<0.001), total energy expenditure was strongly correlated with time spent at sea under both treatments (P<0.0001). These results suggest that transiting elephant seals have a limited capacity to modify their locomotory behaviour without increasing their transport costs. Based on this, we conclude that elephant seals and other ocean predators occupying similar niches may be particularly sensitive to increased transport costs incurred when avoiding unanticipated disturbances.

Estimating resource acquisition and at-sea body condition of a marine predator.

1. Body condition plays a fundamental role in many ecological and evolutionary processes at a variety of scales and across a broad range of animal taxa. An understanding of how body condition changes at fine spatial and temporal scales as a result of interaction with the environment provides necessary information about how animals acquire resources. 2. However, comparatively little is known about intra- and interindividual variation of condition in marine systems. Where condition has been studied, changes typically are recorded at relatively coarse time-scales. By quantifying how fine-scale interaction with the environment influences condition, we can broaden our understanding of how animals acquire resources and allocate them to body stores. 3. Here we used a hierarchical Bayesian state-space model to estimate the body condition as measured by the size of an animal's lipid store in two closely related species of marine predator that occupy different hemispheres: northern elephant seals (Mirounga angustirostris) and southern elephant seals (Mirounga leonina). The observation model linked drift dives to lipid stores. The process model quantified daily changes in lipid stores as a function of the physiological condition of the seal (lipid:lean tissue ratio, departure lipid and departure mass), its foraging location, two measures of behaviour and environmental covariates. 4. We found that physiological condition significantly impacted lipid gain at two time-scales - daily and at departure from the colony - that foraging location was significantly associated with lipid gain in both species of elephant seals and that long-term behavioural phase was associated with positive lipid gain in northern and southern elephant seals. In northern elephant seals, the occurrence of short-term behavioural states assumed to represent foraging were correlated with lipid gain. Lipid gain was a function of covariates in both species. Southern elephant seals performed fewer drift dives than northern elephant seals and gained lipids at a lower rate. 5. We have demonstrated a new way to obtain time series of body condition estimates for a marine predator at fine spatial and temporal scales. This modelling approach accounts for uncertainty at many levels and has the potential to integrate physiological and movement ecology of top predators. The observation model we used was specific to elephant seals, but the process model can readily be applied to other species, providing an opportunity to understand how animals respond to their environment at a fine spatial scale.

Using energetic models to investigate the survival and reproduction of beaked whales (family Ziphiidae).

Mass stranding of several species of beaked whales (family Ziphiidae) associated with exposure to anthropogenic sounds has raised concern for the conservation of these species. However, little is known about the species' life histories, prey or habitat requirements. Without this knowledge, it becomes difficult to assess the effects of anthropogenic sound, since there is no way to determine whether the disturbance is impacting the species' physical or environmental requirements. Here we take a bioenergetics approach to address this gap in our knowledge, as the elusive, deep-diving nature of beaked whales has made it hard to study these effects directly. We develop a model for Ziphiidae linking feeding energetics to the species' requirements for survival and reproduction, since these life history traits would be the most likely to be impacted by non-lethal disturbances. Our models suggest that beaked whale reproduction requires energy dense prey, and that poor resource availability would lead to an extension of the inter-calving interval. Further, given current information, it seems that some beaked whale species require relatively high quality habitat in order to meet their requirements for survival and reproduction. As a result, even a small non-lethal disturbance that results in displacement of whales from preferred habitats could potentially impact a population if a significant proportion of that population was affected. We explored the impact of varying ecological parameters and model assumptions on survival and reproduction, and find that calf and fetus survival appear more readily affected than the survival of adult females.

Foraging behavior and success of a mesopelagic predator in the northeast Pacific Ocean: insights from a data-rich species, the northern elephant seal.

The mesopelagic zone of the northeast Pacific Ocean is an important foraging habitat for many predators, yet few studies have addressed the factors driving basin-scale predator distributions or inter-annual variability in foraging and breeding success. Understanding these processes is critical to reveal how conditions at sea cascade to population-level effects. To begin addressing these challenging questions, we collected diving, tracking, foraging success, and natality data for 297 adult female northern elephant seal migrations from 2004 to 2010. During the longer post-molting migration, individual energy gain rates were significant predictors of pregnancy. At sea, seals focused their foraging effort along a narrow band corresponding to the boundary between the sub-arctic and sub-tropical gyres. In contrast to shallow-diving predators, elephant seals target the gyre-gyre boundary throughout the year rather than follow the southward winter migration of surface features, such as the Transition Zone Chlorophyll Front. We also assessed the impact of added transit costs by studying seals at a colony near the southern extent of the species' range, 1,150 km to the south. A much larger proportion of seals foraged locally, implying plasticity in foraging strategies and possibly prey type. While these findings are derived from a single species, the results may provide insight to the foraging patterns of many other meso-pelagic predators in the northeast Pacific Ocean.

Latitudinal range influences the seasonal variation in the foraging behavior of marine top predators.

Non-migratory resident species should be capable of modifying their foraging behavior to accommodate changes in prey abundance and availability associated with a changing environment. Populations that are better adapted to change will have higher foraging success and greater potential for survival in the face of climate change. We studied two species of resident central place foragers from temperate and equatorial regions with differing population trends and prey availability associated to season, the California sea lion (Zalophus californianus) (CSL) whose population is increasing and the endangered Galapagos sea lion (Zalophus wollebaeki) (GSL) whose population is declining. To determine their response to environmental change, we studied and compared their diving behavior using time-depth recorders and satellite location tags and their diet by measuring C and N isotope ratios during a warm and a cold season. Based on latitudinal differences in oceanographic productivity, we hypothesized that the seasonal variation in foraging behavior would differ for these two species. CSL exhibited greater seasonal variability in their foraging behavior as seen in changes to their diving behavior, foraging areas and diet between seasons. Conversely, GSL did not change their diving behavior between seasons, presenting three foraging strategies (shallow, deep and bottom divers) during both. GSL exhibited greater dive and foraging effort than CSL. We suggest that during the warm and less productive season a greater range of foraging behaviors in CSL was associated with greater competition for prey, which relaxed during the cold season when resource availability was greater. GSL foraging specialization suggests that resources are limited throughout the year due to lower primary production and lower seasonal variation in productivity compared to CSL. These latitudinal differences influence their foraging success, pup survival and population growth reflected in contrasting population trends in which CSL are more successful and potentially more resilient to climate change.

Accuracy of ARGOS locations of Pinnipeds at-sea estimated using Fastloc GPS.

BACKGROUND: ARGOS satellite telemetry is one of the most widely used methods to track the movements of free-ranging marine and terrestrial animals and is fundamental to studies of foraging ecology, migratory behavior and habitat-use. ARGOS location estimates do not include complete error estimations, and for many marine organisms, the most commonly acquired locations (Location Class 0, A, B, or Z) are provided with no declared error estimate. METHODOLOGY/PRINCIPAL FINDINGS: We compared the accuracy of ARGOS Locations to those obtained using Fastloc GPS from the same electronic tags on five species of pinnipeds: 9 California sea lions (Zalophus californianus), 4 Galapagos sea lions (Zalophus wollebaeki), 6 Cape fur seals (Arctocephalus pusillus pusillus), 3 Australian fur seals (A. p. doriferus) and 5 northern elephant seals (Mirounga angustirostris). These species encompass a range of marine habitats (highly pelagic vs coastal), diving behaviors (mean dive durations 2-21 min) and range of latitudes (equator to temperate). A total of 7,318 ARGOS positions and 27,046 GPS positions were collected. Of these, 1,105 ARGOS positions were obtained within five minutes of a GPS position and were used for comparison. The 68(th) percentile ARGOS location errors as measured in this study were LC-3 0.49 km, LC-2 1.01 km, LC-1 1.20 km, LC-0 4.18 km, LC-A 6.19 km, LC-B 10.28 km. CONCLUSIONS/SIGNIFICANCE: The ARGOS errors measured here are greater than those provided by ARGOS, but within the range of other studies. The error was non-normally distributed with each LC highly right-skewed. Locations of species that make short duration dives and spend extended periods on the surface (sea lions and fur seals) had less error than species like elephant seals that spend more time underwater and have shorter surface intervals. Supplemental data (S1) are provided allowing the creation of density distributions that can be used in a variety of filtering algorithms to improve the quality of ARGOS tracking data.