Environmental Drivers of Growth and Oxidative Status during Early Life in a Long-Lived Antarctic Seabird, the Adélie Penguin.

AbstractIn vertebrates, developmental conditions can have long-term effects on individual performance. It is increasingly recognized that oxidative stress could be one physiological mechanism connecting early-life experience to adult phenotype. Accordingly, markers of oxidative status could be useful for assessing the developmental constraints encountered by offspring. Although some studies have demonstrated that developmental constraints are associated with high levels of oxidative stress in offspring, it remains unclear how growth, parental behavior, and brood competition may altogether affect oxidative stress in long-lived species in the wild. Here, we investigated this question in a long-lived Antarctic bird species by testing the impact of brood competition (e.g., brood size and hatching order) on body mass and on two markers of oxidative damage in Adélie penguin chicks. We also examined the influence of parental effort (i.e., foraging trip duration) and parental body condition on chick body mass and oxidative damage. First, we found that brood competition and parental traits had significant impacts on chick body mass. Second, we found that chick age and, to a lesser extent, chick body mass were two strong determinants of the levels of oxidative damage in Adélie penguin chicks. Finally, and importantly, we also found that brood competition significantly increased the levels of one marker of oxidative damage and was associated with a lower survival probability. However, parental effort and parental condition were not significantly linked to chick levels of oxidative damage. Overall, our study demonstrates that sibling competition can generate an oxidative cost even for this long-lived Antarctic species with a limited brood size (maximum of two chicks).

Elephant seal foraging success is enhanced in Antarctic coastal polynyas.

Antarctic polynyas are persistent open water areas which enable early and large seasonal phytoplankton blooms. This high primary productivity, boosted by iron supply from coastal glaciers, attracts organisms from all trophic levels to form a rich and diverse community. How the ecological benefit of polynya productivity is translated to the highest trophic levels remains poorly resolved. We studied 119 southern elephant seals feeding over the Antarctic shelf and demonstrated that: (i) 96% of seals foraging here used polynyas, with individuals spending on average 62% of their time there; (ii) the seals exhibited more area-restricted search behaviour when in polynyas; and (iii) these seals gained more energy (indicated by increased buoyancy from greater fat stores) when inside polynyas. This higher-quality foraging existed even when ice was not present in the study area, indicating that these are important and predictable foraging grounds year-round. Despite these energetic advantages from using polynyas, not all the seals used them extensively. Factors other than food supply may influence an individual's choice in their use of feeding grounds, such as exposure to predation or the probability of being able to return to distant sub-Antarctic breeding sites.

Horizontal-vertical movement relationships: Adélie penguins forage continuously throughout provisioning trips.

BACKGROUND: Diving marine predators forage in a three-dimensional environment, adjusting their horizontal and vertical movement behaviour in response to environmental conditions and the spatial distribution of prey. Expectations regarding horizontal-vertical movements are derived from optimal foraging theories, however, inconsistent empirical findings across a range of taxa suggests these behavioural assumptions are not universally applicable. METHODS: Here, we examined how changes in horizontal movement trajectories corresponded with diving behaviour and marine environmental conditions for a ubiquitous Southern Ocean predator, the Adélie penguin. Integrating extensive telemetry-based movement and environmental datasets for chick-rearing Adélie penguins at Béchervaise Island, we tested the relationships between horizontal move persistence (continuous scale indicating low ['resident'] to high ['directed'] movement autocorrelation), vertical dive effort and environmental variables. RESULTS: Penguins dived continuously over the course of their foraging trips and lower horizontal move persistence corresponded with less intense foraging activity, likely indicative of resting behaviour. This challenges the traditional interpretation of horizontal-vertical movement relationships based on optimal foraging models, which assumes increased residency within an area translates to increased foraging activity. Movement was also influenced by different environmental conditions during the two stages of chick-rearing: guard and crèche. These differences highlight the strong seasonality of foraging habitat for chick-rearing Adélie penguins at Béchervaise Island. CONCLUSIONS: Our findings advance our understanding of the foraging behaviour for this marine predator and demonstrates the importance of integrating spatial location and behavioural data before inferring habitat use.

Bacterial epibiont communities of panmictic Antarctic krill are spatially structured.

Antarctic krill (Euphausia superba) are amongst the most abundant animals on Earth, with a circumpolar distribution in the Southern Ocean. Genetic and genomic studies have failed to detect any population structure for the species, suggesting a single panmictic population. However, the hyper-abundance of krill slows the rate of genetic differentiation, masking potential underlying structure. Here we use high-throughput sequencing of bacterial 16S rRNA genes to show that krill bacterial epibiont communities exhibit spatial structuring, driven mainly by distance rather than environmental factors, especially for strongly krill-associated bacteria. Estimating the ecological processes driving bacterial community turnover indicated this was driven by bacterial dispersal limitation increasing with geographic distance. Furthermore, divergent epibiont communities generated from a single krill swarm split between aquarium tanks under near-identical conditions suggests physical isolation in itself can cause krill-associated bacterial communities to diverge. Our findings show that Antarctic krill-associated bacterial communities are geographically structured, in direct contrast with the lack of structure observed for krill genetic and genomic data.

Finding mesopelagic prey in a changing Southern Ocean.

Mesopelagic fish and squid occupy ocean depths extending below the photic zone and their vertical migrations represent a massive pathway moving energy and carbon through the water column. Their spatio-temporal distribution is however, difficult to map across remote regions particularly the vast Southern Ocean. This represents a key gap in understanding biogeochemical processes, marine ecosystem structure, and how changing ocean conditions will affect marine predators, which depend upon mesopelagic prey. We infer mesopelagic prey vertical distribution and relative abundance in the Indian sector of the Southern Ocean (20° to 130°E) with a novel approach using predator-derived indices. Fourteen years of southern elephant seal tracking and dive data, from the open ocean between the Antarctic Polar Front and the southern Antarctic Circumpolar Current front, clearly show that the vertical distribution of mesopelagic prey is influenced by the physical hydrographic processes that structure their habitat. Mesopelagic prey have a more restricted vertical migration and higher relative abundance closer to the surface where Circumpolar Deep Water rises to shallower depths. Combining these observations with a future projection of Southern Ocean conditions we show that changes in the coupling of surface and deep waters will potentially redistribute mesopelagic prey. These changes are small overall, but show important spatial variability: prey will increase in relative abundance to the east of the Kerguelen Plateau but decrease to the west. The consequences for deep-diving specialists such as elephant seals and whales over this time scale will likely be minor, but the changes in mesoscale vertical energy flow have implications for predators that forage within the mesopelagic zone as well as the broader pelagic ecosystem.

New insights into prime Southern Ocean forage grounds for thriving Western Australian humpback whales.

Humpback whale populations migrate extensively between winter breeding grounds and summer feeding grounds, however known links to remote Antarctic feeding grounds remain limited in many cases. New satellite tracks detail humpback whale migration pathways from Western Australia into the Southern Ocean. These highlight a focal feeding area during austral spring and early summer at the southern Kerguelen plateau, in a western boundary current where a sharp northward turn and retroflection of ocean fronts occurs along the eastern plateau edge. The topographic steering of oceanographic features here likely supports a predictable, productive and persistent forage ground. The spatial distribution of whaling catches and Discovery era mark-recaptures confirms the importance of this region to Western Australian humpback whales since at least historical times. Movement modelling discriminates sex-related behaviours, with females moving faster during both transit and resident periods, which may be a consequence of size or indicate differential energetic requirements. Relatively short and directed migratory pathways overall, together with high-quality, reliable forage resources may provide a partial explanation for the ongoing strong recovery demonstrated by this population. The combination of new oceanographic information and movement data provides enhanced understanding of important biological processes, which are relevant within the context of the current spatial management and conservation efforts in the Southern Ocean.

A quantitative, hierarchical approach for detecting drift dives and tracking buoyancy changes in southern elephant seals.

Foraging behaviour of marine predators inferred from the analysis of horizontal or vertical movements commonly lack quantitative information about foraging success. Several marine mammal species are known to perform dives where they passively drift in the water column, termed "drift" dives. The drift rate is determined by the animal's buoyancy, which can be used to make inference regarding body condition. Long term dive records retrieved via satellite uplink are often summarized before transmission. This loss of resolution hampers identification of drift dives. Here, we develop a flexible, hierarchically structured approach to identify drift dives and estimate the drift rate from the summarized time-depth profiles that are increasingly available to the global research community. Based on high-resolution dive data from southern elephant seals, we classify dives as drift/non-drift and apply a summarization algorithm. We then (i) automatically generate dive groups based on inflection point ordering using a 'Reverse' Broken-Stick Algorithm, (ii) develop a set of threshold criteria to apply across groups, ensuring non-drift dives are most efficiently rejected, and (iii) finally implement a custom Kalman filter to retain the remaining dives that are within the seals estimated drifting time series. Validation with independent data sets shows our method retains approximately 3% of all dives, of which 88% are true drift dives. The drift rate estimates are unbiased, with the upper 95% quantile of the mean squared error between the daily averaged summarized profiles using our method (SDDR) and the observed daily averaged drift rate (ODDR) being only 0.0015. The trend of the drifting time-series match expectations for capital breeders, showing the lowest body condition commencing foraging trips and a progressive improvement as they remain at sea. Our method offers sufficient resolution to track small changes in body condition at a fine temporal scale. This approach overcomes a long-term challenge for large existing and ongoing data collections, with potential application across other drift diving species. Enabling robust identification of foraging success at sea offers a rare and valuable opportunity for monitoring marine ecosystem productivity in space and time by tracking the success of a top predator.

A globally distributed Syndiniales parasite dominates the Southern Ocean micro-eukaryote community near the sea-ice edge.

Syndiniales (Dinophyceae, Alveolata) are a diverse parasitic group common in all marine environments, but their ecological role remains poorly understood. Here we show an unprecedented dominance of a single Syndiniales group I operational taxonomic unit (OTU) across 3000 km of Southern Ocean transects near the sea-ice edge. This super-abundant OTU consistently represented >20%, and in some locations >50%, of eukaryote 18S rDNA sequences. Identical 18S V4 sequences have been isolated from seven Northern Hemisphere locations, and the OTU's putative V9 rDNA sequence was detected at every station of the global Tara Oceans voyage. Although Syndiniales taxa display some host specificity, our identification of candidate Southern Ocean hosts suggests this OTU associates with distinct phyla in different parts of the world. Our results indicate Syndiniales are key players in surface waters near the vast and dynamic sea-ice edge in the world's most biologically productive ocean.

Otolith nucleus chemistry distinguishes Electrona antarctica in the westward-flowing Antarctic Slope Current and eastward-flowing Antarctic Circumpolar Current off East Antarctica.

Eastward transport in the Southern Ocean is concentrated in jets associated with fronts in the Antarctic Circumpolar Current (ACC), whereas flow along the Antarctic continental slope is strongly westward in the Antarctic Slope Current (ASC). The dominant mesopelagic fish endemic to the Southern Ocean, Electrona antarctica (Günther, 1878), has been linked to Circumpolar Deep Water (CDW) transported by the ACC, and a modified version of CDW associated with the ASC. In conjunction with a regional-scale hydrographic survey south of the Kerguelen Plateau, we sampled fish from the ACC and ASC across Princess Elizabeth Trough off East Antarctica, and examined their otolith chemistry. Material laid down in the nucleus during early life showed heterogeneity, arguing against a single homogeneous population. Instead, it suggested exposure to different environments after hatching, consistent with separate transport pathways along the ACC and ASC. Despite clear differences between stations documented in the survey, material laid down along the edge did not show heterogeneity, suggesting instead exposure to similar environments. Seasonal movement northward by ASC fish into the ACC may explain both these results, and potential physical mechanisms include circulation in the Australian-Antarctic Gyre; northward movement of slope waters along the eastern margin of Princess Elizabeth Trough; and seasonal extension of sea-ice into the ACC. Such meridional movement would expose fish to zonal flow, eastward in the ACC during winter and westward in the ASC during summer, promoting regional retention as well as creating opportunities for mixing with fish transported along the ACC.

Coastal polynyas: Winter oases for subadult southern elephant seals in East Antarctica.

Antarctic coastal polynyas are regions of persistent open water and are thought to be key bio-physical features within the sea-ice zone. However, their use by the upper trophic levels of ecosystems remains unclear. A unique bio-physical dataset recorded by southern elephant seals reveals that East Antarctic polynyas are a key winter foraging habitat for male seals. During their post-moult trips from Isles Kerguelen to the Antarctic continental shelf, a total of 18 out of 23 seals visited 9 different polynyas, spending on average 25 ± 20% (up to 75%) of their total trip time inside polynyas. Changes in seal foraging and diving behaviours are observed inside polynyas as compared to outside polynyas. Two polynya usages by seals are observed for the inactive and active polynya phases, pointing to different seasonal peaks in prey abundance. During the active polynya phase, we link seal foraging behaviour to changes in the physical stability of the water-column, which likely impact the seasonal biological dynamics within polynyas.

Bio-physical characterisation of polynyas as a key foraging habitat for juvenile male southern elephant seals (Mirounga leonina) in Prydz Bay, East Antarctica.

Antarctic coastal polynyas are persistent open water areas in the sea ice zone, and regions of high biological productivity thought to be important foraging habitat for marine predators. This study quantified southern elephant seal (Mirounga leonina) habitat use within and around the polynyas of the Prydz Bay region (63°E- 88°E) in East Antarctica, and examined the bio-physical characteristics structuring polynyas as foraging habitat. Output from a climatological regional ocean model was used to provide context for in situ temperature-salinity vertical profiles collected by tagged elephant seals and to characterise the physical properties structuring polynyas. Biological properties were explored using remotely-sensed surface chlorophyll (Chl-a) and, qualitatively, historical fish assemblage data. Spatially gridded residence time of seals was examined in relation to habitat characteristics using generalized additive mixed models. The results showed clear polynya usage during early autumn and increasingly concentrated usage during early winter. Bathymetry, Chl-a, surface net heat flux (representing polynya location), and bottom temperature were identified as significant bio-physical predictors of the spatio-temporal habitat usage. The findings from this study confirm that the most important marine habitats for juvenile male southern elephant seals within Prydz Bay region are polynyas. A hypothesis exists regarding the seasonal evolution of primary productivity, coupling from surface to subsurface productivity and supporting elevated rates of secondary production in the upper water column during summer-autumn. An advancement to this hypothesis is proposed here, whereby this bio-physical coupling is likely to extend throughout the water column as it becomes fully convected during autumn-winter, to also promote pelagic-benthic linkages important for benthic foraging within polynyas.

Decadal changes in habitat characteristics influence population trajectories of southern elephant seals.

Understanding divergent biological responses to climate change is important for predicting ecosystem level consequences. We use species habitat models to predict the winter foraging habitats of female southern elephant seals and investigate how changes in environmental variables within these habitats may be related to observed decreases in the Macquarie Island population. There were three main groups of seals that specialized in different ocean realms (the sub-Antarctic, the Ross Sea and the Victoria Land Coast). The physical and climate attributes (e.g. wind strength, sea surface height, ocean current strength) varied amongst the realms and also displayed different temporal trends over the last two to four decades. Most notably, sea ice extent increased on average in the Victoria Land realm while it decreased overall in the Ross Sea realm. Using a species distribution model relating mean residence times (time spent in each 50 × 50 km grid cell) to 9 climate and physical co-variates, we developed spatial predictions of residence time to identify the core regions used by the seals across the Southern Ocean from 120°E to 120°W. Population size at Macquarie Island was negatively correlated with ice concentration within the core habitat of seals using the Victoria Land Coast and the Ross Sea. Sea ice extent and concentration is predicted to continue to change in the Southern Ocean, having unknown consequences for the biota of the region. The proportion of Macquarie Island females (40%) utilizing the relatively stable sub-Antarctic region, may buffer this population against longer-term regional changes in habitat quality, but the Macquarie Island population has persistently decreased (-1.45% per annum) over seven decades indicating that environmental changes in the Antarctic are acting on the remaining 60% of the population to impose a long-term population decline in a top Southern Ocean predator.

Estimation and simulation of foraging trips in land-based marine predators.

The behavior of colony-based marine predators is the focus of much research globally. Large telemetry and tracking data sets have been collected for this group of animals, and are accompanied by many empirical studies that seek to segment tracks in some useful way, as well as theoretical studies of optimal foraging strategies. However, relatively few studies have detailed statistical methods for inferring behaviors in central place foraging trips. In this paper we describe an approach based on hidden Markov models, which splits foraging trips into segments labeled as "outbound", "search", "forage", and "inbound". By structuring the hidden Markov model transition matrix appropriately, the model naturally handles the sequence of behaviors within a foraging trip. Additionally, by structuring the model in this way, we are able to develop realistic simulations from the fitted model. We demonstrate our approach on data from southern elephant seals (Mirounga leonina) tagged on Kerguelen Island in the Southern Ocean. We discuss the differences between our 4-state model and the widely used 2-state model, and the advantages and disadvantages of employing a more complex model.

Putting the behavior into animal movement modeling: Improved activity budgets from use of ancillary tag information.

Animal movement research relies on biotelemetry, and telemetry-based locations are increasingly augmented with ancillary information. This presents an underutilized opportunity to enhance movement process models. Given tags designed to record specific behaviors, efforts are increasing to update movement models beyond reliance solely upon horizontal movement information to improve inference of space use and activity budgets. We present two state-space models adapted to incorporate ancillary data to inform three discrete movement states: directed, resident, and an activity state. These were developed for two case studies: (1) a "haulout" model for Weddell seals, and (2) an "activity" model for Antarctic fur seals which intersperse periods of diving activity and inactivity. The methodology is easily implementable with any ancillary data that can be expressed as a proportion (or binary) indicator. A comparison of the models augmented with ancillary information and unaugmented models confirmed that many behavioral states appeared mischaracterized in the latter. Important changes in subsequent activity budgets occurred. Haulout accounted for 0.17 of the overall Weddell seal time budget, with the estimated proportion of time spent in a resident state reduced from a posterior median of 0.69 (0.65-0.73; 95% HPDI) to 0.54 (0.50-0.58 HPDI). The drop was more dramatic in the Antarctic fur seal case, from 0.57 (0.52-0.63 HPDI) to 0.22 (0.20-0.25 HPDI), with 0.35 (0.31-0.39 HPDI) of time spent in the inactive (nondiving) state. These findings reinforce previously raised contentions about the drawbacks of behavioral states inferred solely from horizontal movements. Our findings have implications for assessing habitat requirements; estimating energetics and consumption; and management efforts such as mitigating fisheries interactions. Combining multiple sources of information within integrated frameworks should improve inference of relationships between movement decisions and fitness, the interplay between resource and habitat dependencies, and their changes at the population and landscape level.

Taking animal tracking to new depths: synthesizing horizontal--vertical movement relationships for four marine predators.

In animal ecology, a question of key interest for aquatic species is how changes in movement behavior are related in the horizontal and vertical dimensions when individuals forage. Alternative theoretical models and inconsistent empirical findings mean that this question remains unresolved. Here we tested expectations by incorporating the vertical dimension (dive information) when predicting switching between movement states ("resident" or "directed") within a state-space model. We integrated telemetry-based tracking and diving data available for four seal species (southern elephant, Weddell, antarctic fur, and crabeater) in East Antarctica. Where possible, we included dive variables derived from the relationships between (1) dive duration and depth (as a measure of effort), and (2) dive duration and the postdive surface interval (as a physiological measure of cost). Our results varied within and across species, but there was a general tendency for the probability of switching into "resident" state to be positively associated with shorter dive durations (for a given depth) and longer postdive surface intervals (for a given dive duration). Our results add to a growing body of literature suggesting that simplistic interpretations of optimal foraging theory based only on horizontal movements do not directly translate into the vertical dimension in dynamic marine environments. Analyses that incorporate at least two dimensions can test more sophisticated models of foraging behavior.

Integrative modelling of animal movement: incorporating in situ habitat and behavioural information for a migratory marine predator.

A fundamental goal in animal ecology is to quantify how environmental (and other) factors influence individual movement, as this is key to understanding responsiveness of populations to future change. However, quantitative interpretation of individual-based telemetry data is hampered by the complexity of, and error within, these multi-dimensional data. Here, we present an integrative hierarchical Bayesian state-space modelling approach where, for the first time, the mechanistic process model for the movement state of animals directly incorporates both environmental and other behavioural information, and observation and process model parameters are estimated within a single model. When applied to a migratory marine predator, the southern elephant seal (Mirounga leonina), we find the switch from directed to resident movement state was associated with colder water temperatures, relatively short dive bottom time and rapid descent rates. The approach presented here can have widespread utility for quantifying movement-behaviour (diving or other)-environment relationships across species and systems.

Predicting feeding success in a migratory predator: integrating telemetry, environment, and modeling techniques.

Foraging theory predicts that mobile predators should target high profitability areas with plentiful resources and minimize time spent moving between these areas. This has led to a focus in recent literature on the identification of "hotspots" important for migratory marine predators, i.e., regions where predators spend disproportionate amounts of time ostensibly due to high prey abundance; and determination of the environmental features characteristic of such areas. We investigated factors predicting foraging success in southern bluefin tuna (SBT; Thunnus maccoyii), by integrating telemetry-based feeding and movement data (n = 19 fish, length to caudal fork [LCF] = 99 +/- 3 cm) with environmental data over the scale of their annual oceanic migrations during 1998-2000. We used widely available statistical modeling techniques, generalized linear models, and generalized linear mixed models, formulated to represent feeding as a Markov process. The results showed increased feeding and predictability of feeding occurs in the coastal waters of southern Australia, providing some evidence that this area represents a fixed foraging "hotspot" for juvenile tuna during the austral summer. However, in oceanic waters southern bluefin tuna did not fit the common model of migration, but rather showed a pattern of relatively high foraging success throughout their migratory range, especially during periods of continuous travel. Interestingly, foraging "coldspots" (prolonged low-feeding periods) as well as "hotspots" were apparent across individual tracks, predicted most strongly by warm ocean temperatures. These results provide a new perspective on the ecology of large-scale feeding migrations within the context of the heterogeneous ocean environment, where the continuous and opportunistic feeding of generalist predators may be more common, particularly in predatory large pelagic fishes, than is currently documented.

Feeding ecology of wild migratory tunas revealed by archival tag records of visceral warming.

1. Seasonal long-distance migrations are often expected to be related to resource distribution, and foraging theory predicts that animals should spend more time in areas with relatively richer resources. Yet for highly migratory marine species, data on feeding success are difficult to obtain. We analysed the temporal feeding patterns of wild juvenile southern bluefin tuna from visceral warming patterns recorded by archival tags implanted within the body cavity. 2. Data collected during 1998-2000 totalled 6221 days, with individual time series (n = 19) varying from 141 to 496 days. These data span an annual migration circuit including a coastal summer residency within Australian waters and subsequent migration into the temperate south Indian Ocean. 3. Individual fish recommenced feeding between 5 and 38 days after tagging, and feeding events (n = 5194) were subsequently identified on 76.3 +/- 5.8% of days giving a mean estimated daily intake of 0.75 +/- 0.05 kg. 4. The number of feeding events varied significantly with time of day with the greatest number occurring around dawn (58.2 +/- 8.0%). Night feeding, although rare (5.7 +/- 1.3%), was linked to the full moon quarter. Southern bluefin tuna foraged in ambient water temperatures ranging from 4.9 degrees C to 22.9 degrees C and depths ranging from the surface to 672 m, with different targeting strategies evident between seasons. 5. No clear relationship was found between feeding success and time spent within an area. This was primarily due to high individual variability, with both positive and negative relationships observed at all spatial scales examined (grid ranges of 2 x 2 degrees to 10 x 10 degrees ). Assuming feeding success is proportional to forage density, our data do not support the hypothesis that these predators concentrate their activity in areas of higher resource availability. 6. Multiple-day fasting periods were recorded by most individuals. The majority of these (87.8%) occurred during periods of apparent residency within warmer waters (sea surface temperature > 15 degrees C) at the northern edge of the observed migratory range. These previously undocumented nonfeeding periods may indicate alternative motivations for residency. 7. Our results demonstrate the importance of obtaining information on feeding when interpreting habitat utilization from individual animal tracks.