Greg A. Breed

Tracking apex marine predator movements in a dynamic ocean

Pelagic marine predators face unprecedented challenges and uncertain futures. Overexploitation and climate variability impact the abundance and distribution of top predators in ocean ecosystems. Improved understanding of ecological patterns, evolutionary constraints and ecosystem function is critical for preventing extinctions, loss of biodiversity and disruption of ecosystem services. Recent advances in electronic tagging techniques have provided the capacity to observe the movements and long-distance migrations of animals in relation to ocean processes across a range of ecological scales. Tagging of Pacific Predators, a field programme of the Census of Marine Life, deployed 4,306 tags on 23 species in the North Pacific Ocean, resulting in a tracking data set of unprecedented scale and species diversity that covers 265,386 tracking days from 2000 to 2009. Here we report migration pathways, link ocean features to multispecies hotspots and illustrate niche partitioning within and among congener guilds. Our results indicate that the California Current large marine ecosystem and the North Pacific transition zone attract and retain a diverse assemblage of marine vertebrates. Within the California Current large marine ecosystem, several predator guilds seasonally undertake north–south migrations that may be driven by oceanic processes, species-specific thermal tolerances and shifts in prey distributions. We identify critical habitats across multinational boundaries and show that top predators exploit their environment in predictable ways, providing the foundation for spatial management of large marine ecosystems.

Spatial memory and animal movement

Memory is critical to understanding animal movement but has proven challenging to study. Advances in animal tracking technology, theoretical movement models and cognitive sciences have facilitated research in each of these fields, but also created a need for synthetic examination of the linkages between memory and animal movement. Here, we draw together research from several disciplines to understand the relationship between animal memory and movement processes. First, we frame the problem in terms of the characteristics, costs and benefits of memory as outlined in psychology and neuroscience. Next, we provide an overview of the theories and conceptual frameworks that have emerged from behavioural ecology and animal cognition. Third, we turn to movement ecology and summarise recent, rapid developments in the types and quantities of available movement data, and in the statistical measures applicable to such data. Fourth, we discuss the advantages and interrelationships of diverse modelling approaches that have been used to explore the memory-movement interface. Finally, we outline key research challenges for the memory and movement communities, focusing on data needs and mathematical and computational challenges. We conclude with a roadmap for future work in this area, outlining axes along which focused research should yield rapid progress.

Sex-specific, seasonal foraging tactics of adult grey seals (Halichoerus grypus) revealed by state-space analysis

In many large pelagic animals, observing behavior is limited to observation by radio or satellite telemetry. In many cases, discriminating different behaviors from telemetry data has been a key, but often elusive, goal. Here we use state-space models (SSMs) to fit a correlated random walk (CRW) model that switches between two unobserved behavioral states (nominally foraging and traveling) to 41 male and 43 female adult grey seal (Halichoerus grypus) satellite telemetry tracks. The SSM results reveal markedly different spatial behavior between the sexes, fitting well with sexual size dimorphism and known dietary differences, suggesting that the sexes deal with seasonal prey availability and reproductive costs differently. From these results we were also able to produce behaviorally informed habitat use maps, showing a complex and dynamic network of small, intensely used foraging areas. Our flexible SSM approach clearly demonstrates sex-related behavioral differences, fine scale spatial and temporal foraging patterns, and a clearer picture of grey seal ecology and role in the Scotian Shelf ecosystem.

Sexual segregation of seasonal foraging habitats in a non-migratory marine mammal

Many animal species segregate by sex. Such segregation may be social in nature, or ecological, or both. Grey seals (Halichoerus grypus), like many large mammals, are sexually size dimorphic. In size dimorphic species, allometric differences in morphology, metabolic rate and reproductive costs are likely. Such differences may require the sexes to use different foraging strategies or different habitats. To investigate sexual segregation of habitat in grey seals, we used satellite tracks from 95 (male 46; female 49) adults breeding at Sable Island, Nova Scotia (44 °N, 60 °W) collected from 1995 to 2005. Location estimates were made from satellite fixes using a state-space movement model to estimate true locations and regularize them in time. Location estimates were used to calculate home range kernels of male and female habitat use each month. Month by sex kernel home ranges revealed striking differences and dynamics in habitat use between males and females on spatial scales broader than most terrestrial examples and at temporal and spatial resolutions rarely available for marine species. Differences were most pronounced just before (October–December) and immediately after breeding (February–March). During both periods, males primarily used areas along the continental shelf break, while females mainly used mid-shelf regions. Coupled with previously identified sex-specific seasonal patterns of energy storage, diving and diet, our findings suggest that males and females differ profoundly in their spatial foraging strategies. These differences may serve to maximize fitness by reducing intersexual competition during key foraging periods.

Cumulative human impacts on marine predators

Stressors associated with human activities interact in complex ways to affect marine ecosystems, yet we lack spatially explicit assessments of cumulative impacts on ecologically and economically key components such as marine predators. Here we develop a metric of cumulative utilization and impact (CUI) on marine predators by combining electronic tracking data of eight protected predator species (n=685 individuals) in the California Current Ecosystem with data on 24 anthropogenic stressors. We show significant variation in CUI with some of the highest impacts within US National Marine Sanctuaries. High variation in underlying species and cumulative impact distributions means that neither alone is sufficient for effective spatial management. Instead, comprehensive management approaches accounting for both cumulative human impacts and trade-offs among multiple stressors must be applied in planning the use of marine resources.

An Organic Carbon Budget for the Mississippi River Turbidity Plume and Plume Contributions to Air-sea CO2 Fluxes and Bottom Water Hypoxia

We investigated seasonal variability in organic carbon (OC) budgets using a physical-biological model for the Mississippi River turbidity plume. Plume volume was calculated from mixed layer depth and area in each of four salinity subregions based on an extensive set of cruise data and satellite-derived suspended sediment distributions. These physical measurements were coupled with an existing food web model to determine seasonally dependent budgets for labile (reactive on time scales of days to weeks) OC in each salinity subregion. Autochthonous gross primary production (GPP) equaled 1.3×1012 g C yr−1 and dominated labile OC inputs (88% of the budget) because riverine OC was assumed mostly refractory (nonreactive). For perspective, riverine OC inputs amounted to 3.9×1012 g C yr−1, such that physical inputs were 3 times greater than biological inputs to the plume. Annually, microbial respiration (R) accounted for 65% of labile OC losses and net metabolism (GPP—R) for the entire plume was, autotrophic, equaling 5.1×1011 g C yr−1. Smaller losses of labile OC occurred via sedimentation (20%), advection (10%), and export to higher trophic levels (5%). In our present model, annual losses of labile OC are 10% higher than inputs, indicating future improvements are required. Application of our model to estimate air-sea carbon dioxide (CO2) fluxes indicated the plume was a net sink of 2.0×109 mol CO2 yr−1, of which 90% of the total drawdown was from biotic factors. In all seasons, low salinity waters were a source of CO2 (pCO2=560–890 μatm), and intermediate to high salinity waters were a sink of CO2 (pCO2=200–370 μatm). Our model was also used to calculate O2 demand for the development, of regional hypoxia, and our spring and early summer budgets indicated that sedimentation of autochthonous OC from the immediate plume contributed 23% of the O2 demand necessary for establishment of hypoxia in the region.

Using satellite tracking to optimize protection of long-lived marine species: olive ridley sea turtle conservation in Central Africa.

Tractable conservation measures for long-lived species require the intersection between protection of biologically relevant life history stages and a socioeconomically feasible setting. To protect breeding adults, we require knowledge of animal movements, how movement relates to political boundaries, and our confidence in spatial analyses of movement. We used satellite tracking and a switching state-space model to determine the internesting movements of olive ridley sea turtles (Lepidochelys olivacea) (n = 18) in Central Africa during two breeding seasons (2007-08, 2008-09). These movements were analyzed in relation to current park boundaries and a proposed transboundary park between Gabon and the Republic of Congo, both created to reduce unintentional bycatch of sea turtles in marine fisheries. We additionally determined confidence intervals surrounding home range calculations. Turtles remained largely within a 30 km radius from the original nesting site before departing for distant foraging grounds. Only 44.6 percent of high-density areas were found within the current park but the proposed transboundary park would incorporate 97.6 percent of high-density areas. Though tagged individuals originated in Gabon, turtles were found in Congolese waters during greater than half of the internesting period (53.7 percent), highlighting the need for international cooperation and offering scientific support for a proposed transboundary park. This is the first comprehensive study on the internesting movements of solitary nesting olive ridley sea turtles, and it suggests the opportunity for tractable conservation measures for female nesting olive ridleys at this and other solitary nesting sites around the world. We draw from our results a framework for cost-effective protection of long-lived species using satellite telemetry as a primary tool.

Biogeochemical Characteristics of the Lower Mississippi River, USA, During June 2003

During June 2003, a period of mid level discharge (17,400 m−3 s−1), a parcel of water in the lower Mississippi River was sampled every 2 h during its 4-d transit from river km 362 near Baton Rouge to km 0 at Head of Passes, Louisiana, United States. Properties measured at the surface during each of the 48 stations were temperature, salinity, dissolved organic carbon (DOC), total dissolved nitrogen, dissolved macronutrients (NO3+NO2, PO4, Si(OH)4), chlorophylla (chla; three size fractions: < 5 μm, 5–20 μm, and > 20 μm) pigment composition by HPLC, total suspended matter (TSM), particulate organic carbon (POC), and particulate nitrogen (PN). Air-water CO2 flux was calculated from surface water dissolved inorganic carbon and pH. During the 4 d transit, large particles appeared to be settling out of the surface water. Concentrations of chla containing particles > 20 μm declined 37%, TSM declined 43%, POC declined 42% and PN declined 57%. Concentrations of the smaller chla containing particles did not change suggesting only large particulate materials were settling. There was no measurable loss of dissolved NO3, PO4, or Si(OH)4, consistent with the observation that chla did not increase during the 4-d transit. DOC declined slightly (3%). These data indicate there was little autotrophic or heterotrophic activity in the lower Mississippi River at this time, but the system was slightly net heterotrophic.

Electronic tracking tag programming is critical to data collection for behavioral time-series analysis

Electronic tracking tags are major tools of ecological research and management, but programming sophisticated tags can be challenging. We discovered that a common programming scheme can negatively affect the quality of tracks collected by Argos tags. Here we describe the problem and how it occurred. We then simulated a series of tracks with different data collection schemes to investigate how spatial precision and temporal frequency affect the overall quality of tracking data. Tracks were simulated using a two-state composite correlated random walk (CCRW). Tracks were simulated with two spatial scales, using parameters estimated from northern elephant seal (large scale) and California sea lion (small scale) tracking data. Onto each simulated track, observations of varying precision, frequency, and censoring were imposed. We then fit the CCRW in a state-space model (SSM) to the simulated observations in order to assess how data quality and frequency affected recovery of known behavioral state and location. We show that when movement scales are small, regular observations were critical to recover behavior and location. In addition, tracks with frequent regular locations (increasing N) overcame low spatial accuracy (e.g., Argos) to detect small-scale movement patterns, suggesting frequently collected Argos locations may be as good as infrequently collected GPS in some circumstances. From these results and our experience tracking animals generally, we produce a set of guidelines for those manufacturing, programming, and deploying electronic tracking tags to maximize the utility of the data they produce.

Incorrect Likelihood Methods Were Used to Infer Scaling Laws of Marine Predator Search Behaviour

Background Ecologists are collecting extensive data concerning movements of animals in marine ecosystems. Such data need to be analysed with valid statistical methods to yield meaningful conclusions. Principal Findings We demonstrate methodological issues in two recent studies that reached similar conclusions concerning movements of marine animals (Nature 451∶1098; Science 332∶1551). The first study analysed vertical movement data to conclude that diverse marine predators (Atlantic cod, basking sharks, bigeye tuna, leatherback turtles and Magellanic penguins) exhibited “Lévy-walk-like behaviour”, close to a hypothesised optimal foraging strategy. By reproducing the original results for the bigeye tuna data, we show that the likelihood of tested models was calculated from residuals of regression fits (an incorrect method), rather than from the likelihood equations of the actual probability distributions being tested. This resulted in erroneous Akaike Information Criteria, and the testing of models that do not correspond to valid probability distributions. We demonstrate how this led to overwhelming support for a model that has no biological justification and that is statistically spurious because its probability density function goes negative. Re-analysis of the bigeye tuna data, using standard likelihood methods, overturns the original result and conclusion for that data set. The second study observed Lévy walk movement patterns by mussels. We demonstrate several issues concerning the likelihood calculations (including the aforementioned residuals issue). Re-analysis of the data rejects the original Lévy walk conclusion. Conclusions We consequently question the claimed existence of scaling laws of the search behaviour of marine predators and mussels, since such conclusions were reached using incorrect methods. We discourage the suggested potential use of “Lévy-like walks” when modelling consequences of fishing and climate change, and caution that any resulting advice to managers of marine ecosystems would be problematic. For reproducibility and future work we provide R source code for all calculations.