Genomic evidence for homoploid hybrid speciation in a marine mammal apex predator.

Hybridization is widespread and constitutes an important source of genetic variability and evolution. In animals, its role in generating novel and independent lineages (hybrid speciation) has been strongly debated, with only a few cases supported by genomic data. The South American fur seal (SAfs) Arctocephalus australis is a marine apex predator of Pacific and Atlantic waters, with a disjunct set of populations in Peru and Northern Chile [Peruvian fur seal (Pfs)] with controversial taxonomic status. We demonstrate, using complete genome and reduced representation sequencing, that the Pfs is a genetically distinct species with an admixed genome that originated from hybridization between the SAfs and the Galapagos fur seal (Arctocephalus galapagoensis) ~400,000 years ago. Our results strongly support the origin of Pfs by homoploid hybrid speciation over alternative introgression scenarios. This study highlights the role of hybridization in promoting species-level biodiversity in large vertebrates.

Fatty acid profiles of more than 470 marine species from the Southern Hemisphere.

Lipid and fatty acid datasets are commonly used to assess the nutritional composition of organisms, trophic ecology, and ecosystem dynamics. Lipids and their fatty acid constituents are essential nutrients to all forms of life because they contribute to biological processes such as energy flow and metabolism. Assessment of total lipids in tissues of organisms provides information on energy allocation and life-history strategies and can be an indicator of nutritional condition. The analysis of an organism's fatty acids is a widely used technique for assessing nutrient and energy transfer, and dietary interactions in food webs. Although there have been many published regional studies that assessed lipid and fatty acid compositions, many only report the mean values of the most abundant fatty acids. There are limited individual records available for wider use in intercomparison or macro-scale studies. This dataset consists of 4856 records of individual and pooled samples of at least 470 different marine consumer species sampled from tropical, temperate, and polar regions around Australia and in the Southern, Indian, and Pacific Oceans from 1989 to 2018. This includes data for a diverse range of taxa (zooplankton, fish, cephalopods, chondrichthyans, and marine mammals), size ranges (0.02 cm to ~13 m), and that cover a broad range of trophic positions (2.0-4.6). When known, we provide a record of species name, date of sampling, sampling location, body size, relative (%) measurements of tissue-specific total lipid content and abundant fatty acids, and absolute content (mg 100 g-1 tissue) of eicosapentaenoic acid (EPA, 20:5n3) and docosahexaenoic acid (DHA, 22:6n3) as important long-chain (≥C20 ) polyunsaturated omega-3 fatty acids. These records form a solid basis for comparative studies that will facilitate a broad understanding of the spatial and temporal distribution of marine lipids globally. The dataset also provides reference data for future dietary assessments of marine predators and model assessments of potential impacts of climate change on the availability of marine lipids and fatty acids. There are 480 data records within our data file for which the providers have requested that permission for reuse be granted, with the likely condition that they are included as a coauthor on the reporting of the dataset. Records with this condition are indicated by a "yes" under "Conditions_of_data_use" in Data S1: Marineconsumer_FAdata.csv (see Table 2 in Metadata S1 for more details). For all other data records marked as "No" under "Conditions_of_data_use," there are no copyright restrictions for research and/or teaching purposes. We request that users acknowledge use of the data in publications, research proposals, websites, and other outlets via formal citation of this work and original data sources as applicable.

Potential for redistribution of post-moult habitat for Eudyptes penguins in the Southern Ocean under future climate conditions.

Anthropogenic climate change is resulting in spatial redistributions of many species. We assessed the potential effects of climate change on an abundant and widely distributed group of diving birds, Eudyptes penguins, which are the main avian consumers in the Southern Ocean in terms of biomass consumption. Despite their abundance, several of these species have undergone population declines over the past century, potentially due to changing oceanography and prey availability over the important winter months. We used light-based geolocation tracking data for 485 individuals deployed between 2006 and 2020 across 10 of the major breeding locations for five taxa of Eudyptes penguins. We used boosted regression tree modelling to quantify post-moult habitat preference for southern rockhopper (E. chrysocome), eastern rockhopper (E. filholi), northern rockhopper (E. moseleyi) and macaroni/royal (E. chrysolophus and E. schlegeli) penguins. We then modelled their redistribution under two climate change scenarios, representative concentration pathways RCP4.5 and RCP8.5 (for the end of the century, 2071-2100). As climate forcings differ regionally, we quantified redistribution in the Atlantic, Central Indian, East Indian, West Pacific and East Pacific regions. We found sea surface temperature and sea surface height to be the most important predictors of current habitat for these penguins; physical features that are changing rapidly in the Southern Ocean. Our results indicated that the less severe RCP4.5 would lead to less habitat loss than the more severe RCP8.5. The five taxa of penguin may experience a general poleward redistribution of their preferred habitat, but with contrasting effects in the (i) change in total area of preferred habitat under climate change (ii) according to geographic region and (iii) the species (macaroni/royal vs. rockhopper populations). Our results provide further understanding on the regional impacts and vulnerability of species to climate change.

Breeding Thin-Billed Prions Use Marine Habitats Ranging from Inshore to Distant Antarctic Waters.

Pelagic seabirds cover large distances efficiently and thus may reach a variety of marine habitats during breeding. Previous studies using stable isotope data and geolocators suggested that Thin-billed Prions breeding in the Falkland Islands in the Southwest Atlantic may forage in temperate waters over the Patagonian Shelf or cross the Drake Passage to forage in Antarctic waters south of the Polar Front. We deployed miniature GPS dataloggers to track Thin-billed prions in the Falkland Islands during incubation (3 seasons) and chick-rearing (2 seasons). Thin-billed Prions had a wide distribution during incubation, covering latitudes between 43 and 60° S, with trip lengths of ca. 2000 km over seven days, on average. Thin-billed Prions from two nearby sites (60 km apart) were spatially segregated in their incubation trips, with New Island Thin-billed Prions foraging over the Patagonian Shelf, compared to Thin-billed Prions from Bird Island, that foraged in the region of the Polar Front. During chick-rearing, Thin-billed Prions from New Island undertook both long trips to the Patagonian Shelf and south of the Polar Front (30% of trips were 5-11 days), and short trips (70% of trips were 1-4 days) when they foraged more locally, including in inshore waters around the Falkland Islands. Females carried out more trips to distant sites. Thus, Thin-billed showed a high flexibility in foraging areas, habitats and foraging trip durations, which enable them to benefit from both, temperate and Antarctic environments.

Overlap between marine predators and proposed Marine Managed Areas on the Patagonian Shelf.

Static (fixed-boundary) protected areas are key ocean conservation strategies, and marine higher predator distribution data can play a leading role toward identifying areas for conservation action. The Falkland Islands are a globally significant site for colonial breeding marine higher predators (i.e., seabirds and pinnipeds). However, overlap between marine predators and Falkland Islands proposed Marine Managed Areas (MMAs) has not been quantified. Hence, to provide information required to make informed decisions regarding the implementation of proposed MMAs, our aims were to objectively assess how the proposed MMA network overlaps with contemporary estimates of marine predator distribution. We collated tracking data (1999-2019) and used a combination of kernel density estimation and model-based predictions of spatial usage to quantify overlap between colonial breeding marine predators and proposed Falkland Islands MMAs. We also identified potential IUCN Key Biodiversity Areas (pKBAs) using (1) kernel density based methods originally designed to identify Important Bird and Biodiversity Areas (IBAs) and (2) habitat preference models. The proposed inshore MMA, which extends three nautical miles from the Falkland Islands, overlapped extensively with areas used by colonial breeding marine predators. This reflects breeding colonies being distributed throughout the Falklands archipelago, and use being high adjacent to colonies due to central-place foraging constraints. Up to 45% of pKBAs identified via kernel density estimation were located within the proposed MMAs. In particular, the proposed Jason Islands Group MMA overlapped with pKBAs for three marine predator species, suggesting it is a KBA hot spot. However, tracking data coverage was incomplete, which biased pKBAs identified using kernel density methods, to colonies tracked. Moreover, delineation of pKBA boundaries were sensitive to the choice of smoothing parameter used in kernel density estimation. Delineation based on habitat model predictions for both sampled and unsampled colonies provided less biased estimates, and revealed 72% of the Falkland Islands Conservation Zone was likely a KBA. However, it may not be practical to consider such a large area for fixed-boundary management. In the context of wide-ranging marine predators, emerging approaches such as dynamic ocean management could complement static management frameworks such as MMAs, and provide protection at relevant spatiotemporal scales.

Pelagic and benthic ecosystems drive differences in population and individual specializations in marine predators.

Individual specialization, which describes whether populations are comprised of dietary generalists or specialists, has profound ecological and evolutionary implications. However, few studies have quantified individual specialization within and between sympatric species that are functionally similar but have different foraging modes. We assessed the relationship between individual specialization, isotopic niche metrics and foraging behaviour of two marine predators with contrasting foraging modes: pelagic foraging female South American fur seals (Arctocephalus australis) and benthic foraging female southern sea lions (Otaria byronia). Stable isotope analysis of carbon and nitrogen was conducted along the length of adult female vibrissae to determine isotopic niche metrics and the degree of individual specialization. Vibrissae integrated time ranged between 1.1 and 5.5 years, depending on vibrissae length. We found limited overlap in dietary niche-space. Broader population niche sizes were associated with higher degrees of individual specialization, while narrower population niches with lower degrees of individual specialization. The degree of individual specialization was influenced by pelagic and benthic foraging modes. Specifically, South American fur seals, foraging in dynamic pelagic environments with abundant but similar prey, comprised specialist populations composed of generalist individuals. In contrast, benthic southern sea lions foraging in habitats with diverse but less abundant prey had more generalist populations composed of highly specialized individuals. We hypothesize that differences in specialization within and between populations were related to prey availability and habitat differences. Our study supports growing body of literature highlighting that individual specialization is a critical factor in shaping the ecological niche of higher marine predators.

Author Correction: Important At-Sea Areas of Colonial Breeding Marine Predators on the Southern Patagonian Shelf.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Important At-Sea Areas of Colonial Breeding Marine Predators on the Southern Patagonian Shelf.

The Patagonian Shelf Large Marine Ecosystem supports high levels of biodiversity and endemism and is one of the most productive marine ecosystems in the world. Despite the important role marine predators play in structuring the ecosystems, areas of high diversity where multiple predators congregate remains poorly known on the Patagonian Shelf. Here, we used biotelemetry and biologging tags to track the movements of six seabird species and three pinniped species breeding at the Falkland Islands. Using Generalized Additive Models, we then modelled these animals' use of space as functions of dynamic and static environmental indices that described their habitat. Based on these models, we mapped the predicted distribution of animals from both sampled and unsampled colonies and thereby identified areas where multiple species were likely to overlap at sea. Maximum foraging trip distance ranged from 79 to 1,325 km. However, most of the 1,891 foraging trips by 686 animals were restricted to the Patagonian Shelf and shelf slope, which highlighted a preference for these habitats. Of the seven candidate explanatory covariates used to predict distribution, distance from the colony was retained in models for all species and negatively affected the probability of occurrence. Predicted overlap among species was highest on the Patagonian Shelf around the Falkland Islands and the Burdwood Bank. The predicted area of overlap is consistent with areas that are also important habitat for marine predators migrating from distant breeding locations. Our findings provide comprehensive multi-species predictions for some of the largest marine predator populations on the Patagonian Shelf, which will contribute to future marine spatial planning initiatives. Crucially, our findings highlight that spatially explicit conservation measures are likely to benefit multiple species, while threats are likely to impact multiple species.

Habitat use and spatial fidelity of male South American sea lions during the nonbreeding period.

Conditions experienced during the nonbreeding period have profound long-term effects on individual fitness and survival. Therefore, knowledge of habitat use during the nonbreeding period can provide insights into processes that regulate populations. At the Falkland Islands, the habitat use of South American sea lions (Otaria flavescens) during the nonbreeding period is of particular interest because the population is yet to recover from a catastrophic decline between the mid-1930s and 1965, and nonbreeding movements are poorly understood. Here, we assessed the habitat use of adult male (n = 13) and juvenile male (n = 6) South American sea lions at the Falkland Islands using satellite tags and stable isotope analysis of vibrissae. Male South American sea lions behaved like central place foragers. Foraging trips were restricted to the Patagonian Shelf and were typically short in distance and duration (127 ± 66 km and 4.1 ± 2.0 days, respectively). Individual male foraging trips were also typically characterized by a high degree of foraging site fidelity. However, the isotopic niche of adult males was smaller than juvenile males, which suggested that adult males were more consistent in their use of foraging habitats and prey over time. Our findings differ from male South American sea lions in Chile and Argentina, which undertake extended movements during the nonbreeding period. Hence, throughout their breeding range, male South American sea lions have diverse movement patterns during the nonbreeding period that intuitively reflects differences in the predictability or accessibility of preferred prey. Our findings challenge the long-standing notion that South American sea lions undertake a winter migration away from the Falkland Islands. Therefore, impediments to South American sea lion population recovery likely originate locally and conservation measures at a national level are likely to be effective in addressing the decline and the failure of the population to recover.

Pup Vibrissae Stable Isotopes Reveal Geographic Differences in Adult Female Southern Sea Lion Habitat Use during Gestation.

Individuals within populations often differ substantially in habitat use, the ecological consequences of which can be far reaching. Stable isotope analysis provides a convenient and often cost effective means of indirectly assessing the habitat use of individuals that can yield valuable insights into the spatiotemporal distribution of foraging specialisations within a population. Here we use the stable isotope ratios of southern sea lion (Otaria flavescens) pup vibrissae at the Falkland Islands, in the South Atlantic, as a proxy for adult female habitat use during gestation. A previous study found that adult females from one breeding colony (Big Shag Island) foraged in two discrete habitats, inshore (coastal) or offshore (outer Patagonian Shelf). However, as this species breeds at over 70 sites around the Falkland Islands, it is unclear if this pattern is representative of the Falkland Islands as a whole. In order to characterize habitat use, we therefore assayed carbon (δ13C) and nitrogen (δ15N) ratios from 65 southern sea lion pup vibrissae, sampled across 19 breeding colonies at the Falkland Islands. Model-based clustering of pup isotope ratios identified three distinct clusters, representing adult females that foraged inshore, offshore, and a cluster best described as intermediate. A significant difference was found in the use of inshore and offshore habitats between West and East Falkland and between the two colonies with the largest sample sizes, both of which are located in East Falkland. However, habitat use was unrelated to the proximity of breeding colonies to the Patagonian Shelf, a region associated with enhanced biological productivity. Our study thus points towards other factors, such as local oceanography and its influence on resource distribution, playing a prominent role in inshore and offshore habitat use.

Regional variability in diving physiology and behavior in a widely distributed air-breathing marine predator, the South American sea lion (Otaria byronia).

Our understanding of how air-breathing marine predators cope with environmental variability is limited by our inadequate knowledge of their ecological and physiological parameters. Because of their wide distribution along both coasts of the sub-continent, South American sea lions (Otaria byronia) provide a valuable opportunity to study the behavioral and physiological plasticity of a marine predator in different environments. We measured the oxygen stores and diving behavior of South American sea lions throughout most of its range, allowing us to demonstrate that diving ability and behavior vary across its range. We found no significant differences in mass-specific blood volumes of sea lions among field sites and a negative relationship between mass-specific oxygen storage and size, which suggests that exposure to different habitats and geographical locations better explains oxygen storage capacities and diving capability in South American sea lions than body size alone. The largest animals in our study (individuals from Uruguay) were the shallowest and shortest duration divers, and had the lowest mass-specific total body oxygen stores, while the deepest and longest duration divers (individuals from southern Chile) had significantly larger mass-specific oxygen stores, despite being much smaller animals. Our study suggests that the physiology of air-breathing diving predators is not fixed, but that it can be adjusted, to a certain extent, depending on the ecological setting and or habitat. These adjustments can be thought of as a 'training effect': as the animal continues to push its physiological capacity through greater hypoxic exposure, its breath-holding capacity increases.

Dive characteristics can predict foraging success in Australian fur seals (Arctocephalus pusillus doriferus) as validated by animal-borne video.

Dive characteristics and dive shape are often used to infer foraging success in pinnipeds. However, these inferences have not been directly validated in the field with video, and it remains unclear if this method can be applied to benthic foraging animals. This study assessed the ability of dive characteristics from time-depth recorders (TDR) to predict attempted prey capture events (APC) that were directly observed on animal-borne video in Australian fur seals (Arctocephalus pusillus doriferus, n=11). The most parsimonious model predicting the probability of a dive with ≥1 APC on video included only descent rate as a predictor variable. The majority (94%) of the 389 total APC were successful, and the majority of the dives (68%) contained at least one successful APC. The best model predicting these successful dives included descent rate as a predictor. Comparisons of the TDR model predictions to video yielded a maximum accuracy of 77.5% in classifying dives as either APC or non-APC or 77.1% in classifying dives as successful verses unsuccessful. Foraging intensity, measured as either total APC per dive or total successful APC per dive, was best predicted by bottom duration and ascent rate. The accuracy in predicting total APC per dive varied based on the number of APC per dive with maximum accuracy occurring at 1 APC for both total (54%) and only successful APC (52%). Results from this study linking verified foraging dives to dive characteristics potentially opens the door to decades of historical TDR datasets across several otariid species.

From video recordings to whisker stable isotopes: a critical evaluation of timescale in assessing individual foraging specialisation in Australian fur seals.

Estimating the degree of individual specialisation is likely to be sensitive to the methods used, as they record individuals' resource use over different time-periods. We combined animal-borne video cameras, GPS/TDR loggers and stable isotope values of plasma, red cells and sub-sampled whiskers to investigate individual foraging specialisation in female Australian fur seals (Arctocephalus pusillus doriferus) over various timescales. Combining these methods enabled us to (1) provide quantitative information on individuals' diet, allowing the identification of prey, (2) infer the temporal consistency of individual specialisation, and (3) assess how different methods and timescales affect our estimation of the degree of specialisation. Short-term inter-individual variation in diet was observed in the video data (mean pairwise overlap = 0.60), with the sampled population being composed of both generalist and specialist individuals (nested network). However, the brevity of the temporal window is likely to artificially increase the level of specialisation by not recording the entire diet of seals. Indeed, the correlation in isotopic values was tighter between the red cells and whiskers (mid- to long-term foraging ecology) than between plasma and red cells (short- to mid-term) (R(2) = 0.93-0.73 vs. 0.55-0.41). δ(13)C and δ(15)N values of whiskers confirmed the temporal consistency of individual specialisation. Variation in isotopic niche was consistent across seasons and years, indicating long-term habitat (WIC/TNW = 0.28) and dietary (WIC/TNW = 0.39) specialisation. The results also highlight time-averaging issues (under-estimation of the degree of specialisation) when calculating individual specialisation indices over long time-periods, so that no single timescale may provide a complete and accurate picture, emphasising the benefits of using complementary methods.

Disentangling the cause of a catastrophic population decline in a large marine mammal.

Considerable uncertainties often surround the causes of long-term changes in population abundance. One striking example is the precipitous decline of southern sea lions (SSL; Otariaflavescens) at the Falkland Islands, from 80 555 pups in the mid 1930s to just 5506 pups in 1965. Despite an increase in SSL abundance over the past two decades, the population has not recovered, with the number of pups born in 2014 (minimum 4443 pups) less than 6% of the 1930s estimate. The order-of-magnitude decline is primarily attributed to commercial sealing in Argentina. Here, we test this established paradigm and alternative hypotheses by assessing (1) commercial sealing at the Falkland Islands, (2) winter migration of SSL from the Falkland Islands to Argentina, (3) whether the number of SSL in Argentina could have sustained the reported level of exploitation, and (4) environmental change. The most parsimonious hypothesis explaining the SSL population decline was environmental change. Specifically, analysis of 160 years of winter sea surface temperatures revealed marked changes, including a period of warming between 1930 and 1950 that was consistent with the period of SSL decline. Sea surface temperature changes likely influenced the distribution or availability of SSL prey and impacted its population dynamics. We suggest that historical harvesting may not always be the "smoking gun" as is often purported. Rather, our conclusions support the growing evidence for bottom-up forcing on the abundance of species at lower trophic levels (e.g., plankton and fish) and resulting impacts on higher trophic levels across a broad range of ecosystems.

Sexual Niche Segregation and Gender-Specific Individual Specialisation in a Highly Dimorphic Marine Mammal.

While sexual segregation is expected in highly dimorphic species, the local environment is a major factor driving the degree of resource partitioning within a population. Sexual and individual niche segregation was investigated in the Australian fur seal (Arctocephalus pusillus doriferus), which is a benthic foraging species restricted to the shallow continental shelf region of south-eastern Australia. Tracking data and the isotopic values of plasma, red blood cells and whiskers were combined to document spatial and dietary niche segregation throughout the year. Tracking data indicated that, in winter, males and females overlapped in their foraging habitat. All individuals stayed within central Bass Strait, relatively close (< 220 km) to the breeding colony. Accordingly, both genders exhibited similar plasma and red cell δ13C values. However, males exhibited greater δ13C intra-individual variation along the length of their whisker than females. This suggests that males exploited a greater diversity of foraging habitats throughout the year than their female counterparts, which are restricted in their foraging grounds by the need to regularly return to the breeding colony to suckle their pup. The degree of dietary sexual segregation was also surprisingly low, both sexes exhibiting a great overlap in their δ15N values. Yet, males displayed higher δ15N values than females, suggesting they fed upon a higher proportion of higher trophic level prey. Given that males and females exploit different resources (mainly foraging habitats), the degree of individual specialisation might differ between the sexes. Higher degrees of individual specialisation would be expected in males which exploit a greater range of resources. However, comparable levels of inter-individual variation in δ15N whisker values were found in the sampled males and females, and, surprisingly, all males exhibited similar seasonal and inter-annual variation in their δ13C whisker values, suggesting they all followed the same general dispersion pattern throughout the year.

Love thy neighbour or opposites attract? Patterns of spatial segregation and association among crested penguin populations during winter.

AIM: Competition for food among populations of closely related species and conspecifics that occur in both sympatry and parapatry can be reduced by interspecific and intraspecific spatial segregation. According to predictions of niche partitioning, segregation is expected to occur at habitat boundaries among congeners and within habitats among conspecifics, while negative relationships in the density of species or populations will occur in areas of overlap. We tested these predictions by modelling the winter distributions of two crested penguin species from three colonies in the south-western Atlantic. LOCATION: Penguins were tracked from two large colonies on the Falkland Islands and one in South Georgia, from where they dispersed through the South Atlantic, Southern Ocean and south-eastern Pacific. METHODS: Forty macaroni penguins (Eudyptes chrysolophus) from South Georgia and 82 southern rockhopper penguins (Eudyptes chrysocome chrysocome) from two colonies in the Falkland Islands were equipped with global location sensors which log time and light, allowing positions to be estimated twice-daily, from April to August in 2011. Positions were gridded and converted into maps of penguin density. Metrics of overlap were calculated and density was related to remote-sensed oceanographic variables and competitor density using generalized additive models. RESULTS: Macaroni penguins from western South Georgia and southern rockhopper penguins from Steeple Jason Island, Falkland Islands, were spatially segregated by differences in their habitat preferences thus supporting our first prediction regarding interspecific segregation. However, southern rockhopper penguins from Beauchêne Island showed a marked spatial overlap with macaroni penguins as the two had similar habitat preferences and strong mutual associations when controlling for habitat. Contrary to our predictions relating to intraspecific segregation, southern rockhopper penguins from Beauchêne Island and Steeple Jason Island were segregated by differences in habitat selection. MAIN CONCLUSIONS: Morphological differentiation probably allows macaroni penguins from South Georgia and southern rockhopper penguins from Beauchêne Island to coexist in areas of spatial overlap, whereas segregation of the two Falkland rockhopper penguin populations may have arisen from two distinct lineages retaining cultural fidelity to ancestral wintering areas.