Biologging, Remotely-Sensed Oceanography and the Continuous Plankton Recorder Reveal the Environmental Determinants of a Seabird Wintering Hotspot

Marine environments are greatly affected by climate change, and understanding how this perturbation affects marine vertebrates is a major issue. In this context, it is essential to identify the environmental drivers of animal distribution. Here, we focused on the little auk (Alle alle), one of the world’s most numerous seabirds and a major component in Arctic food webs. Using a multidisciplinary approach, we show how little auks adopt specific migratory strategies and balance environmental constraints to optimize their energy budgets. Miniature electronic loggers indicate that after breeding, birds from East Greenland migrate .2000 km to overwinter in a restricted area off Newfoundland. Synoptic data available from the Continuous Plankton Recorder (CPR) indicate that this region harbours some of the highest densities of the copepod Calanus finmarchicus found in the North Atlantic during winter. Examination of large-scale climatic and oceanographic data suggests that little auks favour patches of high copepod abundance in areas where air temperature ranges from 0uC to 5uC. These results greatly advance our understanding of animal responses to extreme environmental constraints, and highlight that information on habitat preference is key to identifying critical areas for marine conservation.

New frontiers in biologging science

The term ‘biologging’ refers to the use of miniaturized animal-attached tags for logging and/or relaying of data about an animal's movements, behaviour, physiology and/or environment. Biologging technology substantially extends our abilities to observe, and take measurements from, free-ranging, undisturbed subjects, providing much scope for advancing both basic and applied biological research. Here, we review highlights from the third international conference on biologging science, which was held in California, USA, from 1 to 5 September 2008. Over the last few years, considerable progress has been made with a range of recording technologies as well as with the management, visualization, integration and analysis of increasingly large and complex biologging datasets. Researchers use these techniques to study animal biology with an unprecedented level of detail and across the full range of ecological scales—from the split-second decision making of individuals to the long-term dynamics of populations, and even entire communities. We conclude our report by suggesting some directions for future research.

Identifying predictable foraging habitats for a wide-ranging marine predator using ensemble ecological niche models

Aim: Ecological niche modelling can provide valuable insight into species' environmental preferences and aid the identification of key habitats for populations of conservation concern. Here, we integrate biologging, satellite remote-sensing and ensemble ecological niche models (EENMs) to identify predictable foraging habitats for a globally important population of the grey-headed albatross (GHA) Thalassarche chrysostoma. Location: Bird Island, South Georgia; Southern Atlantic Ocean. Methods: GPS and geolocation-immersion loggers were used to track at-sea movements and activity patterns of GHA over two breeding seasons (n = 55; brood-guard). Immersion frequency (landings per 10-min interval) was used to define foraging events. EENM combining Generalized Additive Models (GAM), MaxEnt, Random Forest (RF) and Boosted Regression Trees (BRT) identified the biophysical conditions characterizing the locations of foraging events, using time-matched oceanographic predictors (Sea Surface Temperature, SST; chlorophyll a, chl-a; thermal front frequency, TFreq; depth). Model performance was assessed through iterative cross-validation and extrapolative performance through cross-validation among years. Results: Predictable foraging habitats identified by EENM spanned neritic (<500 m), shelf break and oceanic waters, coinciding with a set of persistent biophysical conditions characterized by particular thermal ranges (3–8 °C, 12–13 °C), elevated primary productivity (chl-a > 0.5 mg m−3) and frequent manifestation of mesoscale thermal fronts. Our results confirm previous indications that GHA exploit enhanced foraging opportunities associated with frontal systems and objectively identify the APFZ as a region of high foraging habitat suitability. Moreover, at the spatial and temporal scales investigated here, the performance of multi-model ensembles was superior to that of single-algorithm models, and cross-validation among years indicated reasonable extrapolative performance. Main conclusions: EENM techniques are useful for integrating the predictions of several single-algorithm models, reducing potential bias and increasing confidence in predictions. Our analysis highlights the value of EENM for use with movement data in identifying at-sea habitats of wide-ranging marine predators, with clear implications for conservation and management.

Identifying predictable foraging habitats for a wide-ranging marine predator using ensemble ecological niche models

Aim: Ecological niche modelling can provide valuable insight into species' environmental preferences and aid the identification of key habitats for populations of conservation concern. Here, we integrate biologging, satellite remote-sensing and ensemble ecological niche models (EENMs) to identify predictable foraging habitats for a globally important population of the grey-headed albatross (GHA) Thalassarche chrysostoma. Location: Bird Island, South Georgia; Southern Atlantic Ocean. Methods: GPS and geolocation-immersion loggers were used to track at-sea movements and activity patterns of GHA over two breeding seasons (n = 55; brood-guard). Immersion frequency (landings per 10-min interval) was used to define foraging events. EENM combining Generalized Additive Models (GAM), MaxEnt, Random Forest (RF) and Boosted Regression Trees (BRT) identified the biophysical conditions characterizing the locations of foraging events, using time-matched oceanographic predictors (Sea Surface Temperature, SST; chlorophyll a, chl-a; thermal front frequency, TFreq; depth). Model performance was assessed through iterative cross-validation and extrapolative performance through cross-validation among years. Results: Predictable foraging habitats identified by EENM spanned neritic (<500 m), shelf break and oceanic waters, coinciding with a set of persistent biophysical conditions characterized by particular thermal ranges (3–8 °C, 12–13 °C), elevated primary productivity (chl-a > 0.5 mg m−3) and frequent manifestation of mesoscale thermal fronts. Our results confirm previous indications that GHA exploit enhanced foraging opportunities associated with frontal systems and objectively identify the APFZ as a region of high foraging habitat suitability. Moreover, at the spatial and temporal scales investigated here, the performance of multi-model ensembles was superior to that of single-algorithm models, and cross-validation among years indicated reasonable extrapolative performance. Main conclusions: EENM techniques are useful for integrating the predictions of several single-algorithm models, reducing potential bias and increasing confidence in predictions. Our analysis highlights the value of EENM for use with movement data in identifying at-sea habitats of wide-ranging marine predators, with clear implications for conservation and management.

Persistence in diving American mink

Background American mink forage on land and in water, with aquatic prey often constituting a large proportion of their diet. Their long, thin body shape and relatively poor insulation make them vulnerable to heat loss, particularly in water, yet some individuals dive over 100 times a day. At the level of individual dives, previous research found no difference in dive depth or duration, or the total number of dives per day between seasons, but mink did appear to make more dives per active hour in winter than in summer. There was also no difference in the depth or duration of individual dives between the sexes, but there was some evidence that females made more dives per day than males. However, because individual mink dives tend to be extremely short in duration, persistence (quantified as the number of consecutive dives performed) may be a more appropriate metric with which to compare diving behaviour under different scenarios. Results Mink performed up to 28 consecutive dives, and dived continually for up to 36 min. Periods of more loosely aggregated diving (termed ‘aquatic activity sessions’) comprised up to 80 dives, carried out over up to 162.8 min. Contrary to our predictions, persistence was inversely proportional to body weight, with small animals more persistent than large ones, and (for females, but not for males) increased with decreasing temperature. For both sexes, persistence was greater during the day than during the night. Conclusions The observed body weight effect may point to inter-sexual niche partitioning, since in mink the smallest animals are females and the largest are males. The results may equally point to individual specialism’s, since persistence was also highly variable among individuals. Given the energetic costs involved, the extreme persistence of some animals observed in winter suggests that the costs of occasional prolonged activity in cold water are outweighed by the energetic gains. Analysing dive persistence can provide information on an animal’s physical capabilities for performing multiple dives and may reveal how such behaviour is affected by different conditions. Further development of monitoring and biologging methodology to allow quantification of hunting success, and thus the rewards obtained under alternative scenarios, would be insightful.

Individual foraging strategies in Australasian gannets (Morus serrator)

The individual foraging behaviour of Australasian gannets (Morus serrator) was studied using GPS and time-depth recorders. Gannets were found to forage at average maximum distances of 49 km (± 39 km) from the colony, with total foraging path lengths of 143 km (± 108 km) and foraging trip durations of 13.9 h (± 11 h). During foraging trips gannets spent on average 48.7% (± 17.6) of the time flying and made 37 (± 30.4) dives per trip, with an average maximum depth of 3.6 m (± 1 m). However, considerable variation in individual foraging strategies were recorded and these will be discussed in relation to individuals age, breeding experience and sex.

Global patterns for upper ceilings on migration distance in sea turtles and comparisons with fish, birds and mammals

1. Some animals migrate huge distances in search of resources with locomotory mode (flying/swimming/walking) thought to drive the upper ceilings on migration distance. Yet in cross-taxa comparisons, upper ceilings on migration distance have been ignored for one important group, sea turtles. 2. Using migration distances recorded for 407 adult and 4715 juvenile sea turtles across five species, we show that for adult cheloniid turtles, the upper ceiling on species migration distances between breeding and foraging habitats (1050–2850 km across species) is similar to that predicted for equivalent-sized marine mammals and fish. 3. In contrast, by feeding in the open ocean, adult leatherback turtles (Dermochelys coriacea) and juveniles of all turtle species can travel around 12 000 km from their natal regions, travelling across the widest ocean basins. For juvenile turtles, this puts their maximum migration distances well beyond those expected for equivalent-sized marine mammals and fish, but not those found in some similar sized birds. 4. Post-hatchling turtles perform these long-distance migrations to juvenile foraging sites only once in their lifetime, while adult turtles return to their breeding sites every few (generally ?2) years. Our results highlight the important roles migration periodicity and foraging mode can play in driving the longest migrations, and the implications for Marine Protected Area planning are considered in terms of sea turtle conservation.

High activity and Levy searches : jellyfish can search the water column like fish

Over-fishing may lead to a decrease in fish abundance and a proliferation of jellyfish. Active movements and prey search might be thought to provide a competitive advantage for fish, but here we use data-loggers to show that the frequently occurring coastal jellyfish (Rhizostoma octopus) does not simply passively drift to encounter prey. Jellyfish (327 days of data from 25 jellyfish with depth collected every 1 min) showed very dynamic vertical movements, with their integrated vertical movement averaging 619.2 m d−1, more than 60 times the water depth where they were tagged. The majority of movement patterns were best approximated by exponential models describing normal random walks. However, jellyfish also showed switching behaviour from exponential patterns to patterns best fitted by a truncated Lévy distribution with exponents (mean μ = 1.96, range 1.2–2.9) close to the theoretical optimum for searching for sparse prey (μopt ≈ 2.0). Complex movements in these ‘simple’ animals may help jellyfish to compete effectively with fish for plankton prey, which may enhance their ability to increase in dominance in perturbed ocean systems.

Time-in-area represents foraging activity in a wide-ranging pelagic forager

Successful Marine Spatial Planning depends upon the identification of areas with high importance for particular species, ecosystems or processes. For seabirds, advancements in biologging devices have enabled us to identify these areas through the detailed study of at-sea behaviour. However, in many cases, only positional data are available and the presence of local biological productivity and hence seabird foraging behaviour is inferred from these data alone, under the untested assumption that foraging activity is more likely to occur in areas where seabirds spend more time. We fitted GPS devices and accelerometers to northern gannets Morus bassanus and categorised the behaviour of individuals outside the breeding colony as plunge diving, surface foraging, floating and flying. We then used the locations of foraging events to test the efficiency of 2 approaches: time-in-area and kernel density (KD) analyses, which are widely employed to detect highly-used areas and interpret foraging behaviour from positional data. For KD analyses, the smoothing parameter (h) was calculated using the ad hoc method (KDad hoc), and KDh=9.1, where h = 9.1 km, to designate core foraging areas from location data. A high proportion of foraging events occurred in core foraging areas designated using KDad hoc, KDh=9.1, and time-in-area. Our findings demonstrate that foraging activity occurs in areas where seabirds spend more time, and that both KD analysis and the time-in-area approach are equally efficient methods for this type of analysis. However, the time-in-area approach is advantageous in its simplicity, and in its ability to provide the shapes commonly used in planning. Therefore, the time-in-area approach can be used as a simple way of using seabirds to identify ecologically important locations from both tracking and survey data.

Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion

Despite global declines in the abundance of marine predators, knowledge of foraging ecology, necessary to predict the ecological consequences of large changes in marine predator abundance, remains enigmatic for many species. Given that populations suffering severe declines are of conservation concern, we examined the foraging ecology of southern sea lions (SSL) (Otaria flavescens)-one of the least studied otariids (fur seal and sea lions)-which have declined by over 90 % at the Falkland Islands since the 1930s. Using a combination of biologging devices and stable isotope analysis of vibrissae, we redress major gaps in the knowledge of SSL ecology and quantify patterns of individual specialization. Specifically, we revealed two discrete foraging strategies, these being inshore (coastal) and offshore (outer Patagonian Shelf). The majority of adult female SSL (72 % or n = 21 of 29 SSL) foraged offshore. Adult female SSL that foraged offshore travelled further (92 ± 20 vs. 10 ± 4 km) and dived deeper (75 ± 23 vs. 21 ± 8 m) when compared to those that foraged inshore. Stable isotope analysis revealed long-term fidelity (years) to these discrete foraging habitats. In addition, we found further specialization within the offshore group, with adult female SSL separated into two clusters on the basis of benthic or mixed (benthic and pelagic) dive behavior (benthic dive proportion was 76 ± 9 vs. 51 ± 8 %, respectively). We suggest that foraging specialization in depleted populations such as SSL breeding at the Falkland Islands, are influenced by foraging site fidelity, and could be independent of intraspecific competition. Finally, the behavioral differences we describe are crucial to understanding population-level dynamics, impediments to population recovery, and threats to population persistence.

Utility of biological sensor tags in animal conservation

Electronic tags (both biotelemetry and biologging platforms) have informed conservation and resource management policy and practice by providing vital information on the spatial ecology of animals and their environments. However, the extent of the contribution of biological sensors (within electronic tags) that measure an animal's state (e.g., heart rate, body temperature, and details of locomotion and energetics) is less clear. A literature review revealed that, despite a growing number of commercially available state sensor tags and enormous application potential for such devices in animal biology, there are relatively few examples of their application to conservation. Existing applications fell under 4 main themes: quantifying disturbance (e.g., ecotourism, vehicular and aircraft traffic), examining the effects of environmental change (e.g., climate change), understanding the consequences of habitat use and selection, and estimating energy expenditure. We also identified several other ways in which sensor tags could benefit conservation, such as determining the potential efficacy of management interventions. With increasing sensor diversity of commercially available platforms, less invasive attachment techniques, smaller device sizes, and more researchers embracing such technology, we suggest that biological sensor tags be considered a part of the necessary toolbox for conservation. This approach can measure (in real time) the state of free-ranging animals and thus provide managers with objective, timely, relevant, and accurate data to inform policy and decision making.

Navigating uncertain waters: a critical review of inferring foraging behaviour from location and dive data in pinnipeds

In the last thirty years, the emergence and progression of biologging technology has led to great advances in marine predator ecology. Large databases of location and dive observations from biologging devices have been compiled for an increasing number of diving predator species (such as pinnipeds, sea turtles, seabirds and cetaceans), enabling complex questions about animal activity budgets and habitat use to be addressed. Central to answering these questions is our ability to correctly identify and quantify the frequency of essential behaviours, such as foraging. Despite technological advances that have increased the quality and resolution of location and dive data, accurately interpreting behaviour from such data remains a challenge, and analytical methods are only beginning to unlock the full potential of existing datasets. This review evaluates both traditional and emerging methods and presents a starting platform of options for future studies of marine predator foraging ecology, particularly from location and two-dimensional (time-depth) dive data. We outline the different devices and data types available, discuss the limitations and advantages of commonly-used analytical techniques, and highlight key areas for future research. We focus our review on pinnipeds - one of the most studied taxa of marine predators - but offer insights that will be applicable to other air-breathing marine predator tracking studies. We highlight that traditionally-used methods for inferring foraging from location and dive data, such as first-passage time and dive shape analysis, have important caveats and limitations depending on the nature of the data and the research question. We suggest that more holistic statistical techniques, such as state-space models, which can synthesise multiple track, dive and environmental metrics whilst simultaneously accounting for measurement error, offer more robust alternatives. Finally, we identify a need for more research to elucidate the role of physical oceanography, device effects, study animal selection, and developmental stages in predator behaviour and data interpretation.

Context dependency of trait repeatability and its relevance for management and conservation of fish populations

Repeatability of behavioural and physiological traits is increasingly a focus for animal researchers, for which fish have become important models. Almost all of this work has been done in the context of evolutionary ecology, with few explicit attempts to apply repeatability and context dependency of trait variation toward understanding conservation-related issues. Here, we review work examining the degree to which repeatability of traits (such as boldness, swimming performance, metabolic rate and stress responsiveness) is context dependent. We review methods for quantifying repeatability (distinguishing between within-context and across-context repeatability) and confounding factors that may be especially problematic when attempting to measure repeatability in wild fish. Environmental factors such temperature, food availability, oxygen availability, hypercapnia, flow regime and pollutants all appear to alter trait repeatability in fishes. This suggests that anthropogenic environmental change could alter evolutionary trajectories by changing which individuals achieve the greatest fitness in a given set of conditions. Gaining a greater understanding of these effects will be crucial for our ability to forecast the effects of gradual environmental change, such as climate change and ocean acidification, the study of which is currently limited by our ability to examine trait changes over relatively short time scales. Also discussed are situations in which recent advances in technologies associated with electronic tags (biotelemetry and biologging) and respirometry will help to facilitate increased quantification of repeatability for physiological and integrative traits, which so far lag behind measures of repeatability of behavioural traits.

New insights: animal-borne cameras and accelerometers reveal the secret lives of cryptic species

Logging cameras and accelerometers have opened our eyes to the secret lives of many enigmatic species. Here some of the new opportunities provided by this technology are reviewed. Recent discoveries are highlighted including the observation of selective feeding on energy-rich parts of prey. As such, biologging cameras provide new opportunities for consideration of selective feeding within the same sort of theoretical framework (marginal value theory/optimal foraging) that exploitation of prey patches has been examined. A recent study with the world's largest bony fish, the ocean sunfish (Mola mola), is highlighted where animal-borne cameras allowed the ground-truthing of data sets collected with depth recorders and accelerometers. This synergistic use of a range of biologging approaches will help drive an holistic understanding of the free-living behaviour of a range of species.

Testing optimal foraging theory models on benthic divers

Empirical testing of optimal foraging models on diving air-breathing animals is limited due to difficulties in quantifying the prey field through direct observations. Here we used accelerometers to detect rapid head movements during prey encounter events (PEE) of free-ranging benthic-divers, Australian fur seals, Arctocephalus pusillus doriferus. PEE signals from accelerometer data were validated by simultaneous video data. We then used PEEs as a measure of patch quality to test several optimal foraging model predictions. Seals had longer bottom durations in unfruitful dives (no PEE) than those with some foraging success (PEE. ≥. 1). However, when examined in greater detail, seals had longer bottom durations in dives with more PEEs, but shorter bottom durations in bouts (sequences of dives) with more PEEs. Our results suggest that seals were generally maximizing bottom durations in all foraging dives, characteristic of benthic divers. However, successful foraging dives might be more energetically costly (e.g. digestive costs), thus resulting in shorter bottom durations at the larger scale of bouts. Our study provides a case study of how the foraging behaviour of a central place forager foraging in a fairly homogeneous environment, with relatively high travel costs, may deviate from current foraging models under different situations. Future foraging models should aim to integrate other aspects (e.g. diet) of the foraging process for more accurate predictions.