Transcriptome of the dead: characterisation of immune genes and marker development from necropsy samples in a free-ranging marine mammal

Background Transcriptomes are powerful resources, providing a window on the expressed portion of the genome that can be generated rapidly and at low cost for virtually any organism. However, because many genes have tissue-specific expression patterns, developing a complete transcriptome usually requires a 'discovery pool' of individuals to be sacrificed in order to harvest mRNA from as many different types of tissue as possible. This hinders transcriptome development in large, charismatic and endangered species, many of which stand the most to gain from such approaches. To circumvent this problem in a model pinniped species, we 454 sequenced cDNA from testis, heart, spleen, intestine, kidney and lung tissues obtained from nine adult male Antarctic fur seals (Arctocephalus gazella) that died of natural causes at Bird Island, South Georgia. Results After applying stringent quality control criteria based on length and annotation, we obtained 12,397 contigs which, in combination with 454 data previously obtained from skin, gave a total of 23,096 unique contigs. Homology was found to 77.0% of dog (Canis lupus familiaris) transcripts, suggesting that the combined assembly represents a substantial proportion of this species' transcriptome. Moreover, only 0.5% of transcripts revealed sequence similarity to bacteria, implying minimal contamination, and the percentage of transcripts involved in cell death was low at 2.6%. Transcripts with immune-related annotations were almost five-fold enriched relative to skin and represented 13.2% of all spleen-specific contigs. By reference to the dog, we also identified transcripts revealing homology to five class I, ten class II and three class III genes of the Major Histocompatibility Complex and derived the putative genomic distribution of 17,121 contigs, 2,119 in silico mined microsatellites and 9,382 single nucleotide polymorphisms. Conclusions Our findings suggest that transcriptome development based on samples collected post mortem may greatly facilitate genomic studies, not only of marine mammals but also more generally of species that are of conservation concern

Linking extreme interannual changes in prey availability to foraging behaviour and breeding investment in a marine predator, the macaroni penguin

Understanding the mechanisms that link prey availability to predator behaviour and population change is central to projecting how a species may respond to future environmental pressures. We documented the behavioural responses and breeding investment of macaroni penguins Eudyptes chrysolophus across five breeding seasons where local prey density changed by five-fold; from very low to highly abundant. When prey availability was low, foraging trips were significantly longer and extended overnight. Birds also foraged farther from the colony, potentially in order to reach more distant foraging grounds and allow for increased search times. These extended foraging trips were also linked to a marked decrease in fledgling weights, most likely associated with reduced rates of provisioning. Furthermore, by comparing our results with previous work on this population, it appears that lowered first-year survival rates associated, at least partially, with fledging masses were also evident for this cohort. This study integrates a unique set of prey density, predator behaviour and predator breeding investment data to highlight a possible behavioural mechanism linking perturbations in prey availability to population demography

Combined influence of meso-scale circulation and bathymetry on the foraging behaviour of a diving predator, the king penguin (Aptenodytes patagonicus)

Investigating the responses of marine predators to environmental features is of key importance for understanding their foraging behaviour and reproductive success. In this study we examined the foraging behaviour of king penguins breeding at Kerguelen (southern Indian Ocean) in relation to oceanographic and bathymetric features within their foraging ambit. We used ARGOS and Global Positioning System tracking together with Time-Depth-Temperature-Recorders (TDR) to follow the at-sea movements of incubating and brooding king penguins. Combining the penguin behaviour with oceanographic data at the surface through satellite data and at depth through in-situ recordings by the TDRs enabled us to explore how these predators adjusted their horizontal and vertical foraging movements in response to their physical environment. Relating the observed behaviour and oceanographic patterns to local bathymetry lead to a comprehensive picture of the combined influence of bathymetry and meso-scale circulation on the foraging behaviour of king penguins. During both breeding stages king penguins foraged in the area to the south-east of Kerguelen, where they explored an influx of cold waters of southern origin interacting with the Kerguelen Plateau bathymetry. Foraging in the Polar Front and at the thermocline was associated with high prey capture rates. However, foraging trip orientation and water mass utilization suggested that bathymetrically entrained cold-water features provided the most favourable foraging locations. Our study explicitly reports the exploration of bathymetry-related oceanographic features by foraging king penguins. It confirms the presence of Areas of Ecological Significance for marine predators on the Kerguelen Plateau, and suggests the importance of further areas related to the cold-water flow along the shelf break of the Kerguelen Plateau

The roles of sex, mass and individual specialisation in partitioning foraging-depth niches of a pursuit-diving predator

Intra-specific foraging niche partitioning can arise due to gender differences or individual specialisation in behaviour or prey selection. These may in turn be related to sexual size dimorphism or individual variation in body size through allometry. These variables are often inter-related and challenging to separate statistically. We present a case study in which the effects of sex, body mass and individual specialisation on the dive depths of the South Georgia shag on Bird Island, South Georgia are investigated simultaneously using a linear mixed model. The nested random effects of trip within individual explained a highly significant amount of the variance. The effects of sex and body mass were both significant independently but could not be separated statistically owing to them being strongly interrelated. Variance components analysis revealed that 45.5% of the variation occurred among individuals, 22.6% among trips and 31.8% among Dives, while R2 approximations showed gender explained 31.4% and body mass 55.9% of the variation among individuals. Male dive depths were more variable than those of females at the levels of individual, trip and dive. The effect of body mass on individual dive depths was only marginally significant within sexes. The percentage of individual variation in dive depths explained by mass was trivial in males (0.8%) but substantial in females (24.1%), suggesting that differences in dive depths among males was largely due to them adopting different behavioural strategies whereas in females allometry played an additional role. Niche partitioning in the study population therefore appears to be achieved through the interactive effects of individual specialisation and gender upon vertical foraging patch selection, and has the potential to interact in complex ways with other axes of the niche hypervolume such as foraging locations, timing of foraging and diet

A dynamic framework for assessing and managing risks to ecosystems from fisheries: demonstration for conserving the krill-based food web in Antarctica

The ecosystem approach to fisheries has been discussed since the 1980s. It aims to reduce risks from fisheries to whole, or components of, ecosystems, not just to target species. Precautionary approaches further aim to keep the risk of damage to a low level. Here, we provide a dynamic framework for spreading the ecosystems risk of fisheries in space and time, a method that can be used from the outset of developing fisheries and continually updated as new knowledge becomes available. Importantly, this method integrates qualitative and quantitative approaches to assess risk and provides mechanisms to both spread the risk, including enabling closed areas to help offset risk, and adjust catch limits to keep regional risk to a baseline level. Also, the framework does not require uniform data standards across a region but can incorporate spatially and temporally heterogeneous data and knowledge. The approach can be coupled with the conservation of biodiversity in marine protected areas, addressing potential overlap of fisheries with areas of high conservation value. It accounts for spatial and temporal heterogeneity in ecosystems, including the different spatial and temporal scales at which organisms function. We develop the framework in the first section of the paper, including a simple illustration of its application. In the framework we include methods for using closed areas to offset risk or for conserving biodiversity of high conservation value. We also present methods that could be used to account for uncertainties in input data and knowledge. In the second section, we present a real-world illustration of the application of the framework to managing risks of food web effects of fishing for Antarctic krill in the Southern Ocean. Last, we comment on the wider application and development of the framework as information improves

Movements and activities of male black-tailed gulls in breeding and sabbatical years

Long-lived animals sometimes skip one or more breeding seasons; however, little is known about their movements and activities during such ‘sabbatical’ periods. Here we present novel data on year-round movements and activities of two male black-tailed gulls Larus crassirostris during a sabbatical year. We compare the data with those in a year when they bred and with those of two other breeding males. The year-round migration routes of two sabbatical males were consistent with those of the breeding males: they returned to the breeding area but did not visit the colony in the sabbatical year. They landed more frequently on water (a potential index of foraging effort) during the non-breeding autumn and winter prior to the sabbatical year than before breeding. Sabbatical gulls may forage more intensively to recover body condition immediately after breeding

Using habitat models for chinstrap penguins, Pygoscelis antarctica, to inform marine spatial management around the South Sandwich Islands during the penguin breeding season

If not carefully managed, harvesting of krill risks disturbing the ecological balance of many Antarctic and sub-Antarctic sites where krill-dependent predators feed. One of the least disturbed sites anywhere within the Southern Ocean and one where krill fishing has so far been virtually non-existent is the South Sandwich Islands volcanic archipelago. Some of the main krill predators breeding at the South Sandwich Islands are penguins, with five species breeding on the islands, the dominant species of which is the chinstrap penguin. In this paper we report on the results of ARGOS PTT deployments during the chinstrap penguin chick-rearing period, using the recorded foraging trips to develop habitat models. Foraging habitats used by chinstrap penguins during the chick-rearing period were best characterised by distance from the colony and sea surface temperature and, using these two covariates, we predicted foraging habitat use around all islands. We show that the provisions of the South Georgia and South Sandwich Islands Marine Protected Area ensure that chinstrap penguins, and other krill-dependent predators with similar foraging ranges, likely have robust protection during the summer. During the winter, when krill predators are likely to forage further offshore, seasonal sea ice provides a physical barrier to exclude the fishery, again ensuring the islands’ unique biodiversity receives strong protection. However, to the north of the marginal sea ice zone, competition between krill predators and the fishery could exist if the fishery were ever to explore new locations for resource extraction. We make a number of conclusions, including the need for winter tracking data to inform future management options

Wind field and sex constrain the flight speeds of central-place foraging albatrosses

By extracting energy from the highly dynamic wind and wave fields that typify pelagic habitats, albatrosses are able to proceed almost exclusively by gliding flight. Although energetic costs of gliding are low, enabling breeding albatrosses to forage hundreds to thousands of kilometers from their colonies, these and time costs vary with relative wind direction. This causes albatrosses in some areas to route provisioning trips to avoid headwind flight, potentially limiting habitat accessibility during the breeding season. In addition, because female albatrosses have lower wing loadings than males, it has been argued that they are better adapted to flight in light winds, leading to sexual segregation of foraging areas. We used satellite telemetry and immersion logger data to quantify the effects of relative wind speed, sex, breeding stage, and trip stage on the ground speeds (Vg) of four species of Southern Ocean albatrosses breeding at South Georgia. Vg was linearly related to the wind speed component in the direction of flight (Vwf), its effect being greatest on Wandering Albatrosses Diomedea exulans, followed by Black-browed Albatrosses Thalassarche melanophrys, Light-mantled Sooty Albatrosses Phoebatria palpebrata, and Gray-headed Albatrosses T. chrysostoma. Ground speeds at Vwf = 0 were similar to airspeeds predicted by aerodynamic theory and were higher in males than in females. However, we found no evidence that this led to sexual segregation, as males and females experienced comparable wind speeds during foraging trips. Black-browed, Gray-headed, and Light-mantled Sooty Albatrosses did not engage in direct, uninterrupted bouts of flight on moonless nights, but Wandering Albatrosses attained comparable Vg night and day, regardless of lunar phase. Relative flight direction was more important in determining Vg than absolute wind speed. When birds were less constrained in the middle stage of foraging trips, all species flew predominantly across the wind. However, in some instances, commuting birds encountered headwinds during outward trips and tail winds on their return, with the result that Vg was 1.0–3.4 m/s faster during return trips. This, we hypothesize, could result from constraints imposed by the location of prey resources relative to the colony at South Georgia or could represent an energy optimization strategy

Wintertime overlaps between female Antarctic fur seals (Arctocephalus gazella) and the krill fishery at South Georgia, South Atlantic

The diet of Antarctic fur seals (Arctocephalus gazella) at South Georgia is dominated by Antarctic krill (Euphausia superba). During the breeding season, foraging trips by lactating female fur seals are constrained by their need to return to land to provision their pups. Post-breeding, seals disperse in order to feed and recover condition; estimates indicate c.70% of females remain near to South Georgia, whilst others head west towards the Patagonian Shelf or south to the ice-edge. The krill fishery at South Georgia operates only during the winter, providing the potential for fur seal: fishery interaction during these months. Here we use available winter (May to September) tracking data from Platform Terminal Transmitter (PTT) tags deployed on female fur seals at Bird Island, South Georgia. We develop habitat models describing their distribution during the winters of 1999 and 2003 with the aim of visualising and quantifying the degree of spatial overlap between female fur seals and krill harvesting in South Georgia waters. We show that spatial distribution of fur seals around South Georgia is extensive, and that the krill fishery overlaps with small, highly localised areas of available fur seal habitat. From these findings we discuss the implications for management, and future work

A long-term study of gentoo penguin (Pygoscelis papua) population trends at a major Antarctic tourist site, Goudier Island, Port Lockroy

Gentoo penguins Pygoscelis papua breed at a number of sites at the West Antarctic Peninsula, including Goudier Island, Port Lockroy—the longest studied location for tourist-penguin interactions in the Antarctic. These penguins annually encounter some of the highest numbers of tourists in the whole of Antarctica. Using yearly count data from all ten colonies on Goudier Island, we report changes in long-term population size and breeding success over a 21 year period (1996/1997 to 2016/2017), documenting inter-annual variability in numbers of breeding pairs and chicks fledged (productivity). We found a 24.5% (1.4% per annum) decrease in breeding pairs; similar declines were evident in breeding pairs at six colonies visited by tourists as well as at four unvisited colonies. Breeding success also declined, with chick numbers declining in visited (53.7%, 3.8% per annum) and unvisited colonies (59.8%, 4.6% per annum). While gentoo penguin numbers are increasing regionally, we reveal a recent decline in the Goudier Island population occurring simultaneous with increases in tourist numbers from 262 in 1996/1997 to 19,688 in 2016/2017. Analyses suggest a complex situation with different possible drivers of change. There was a significant negative effect of increasing air temperature and shifts in sea ice variables on breeding pairs. However, similar statistical support showed a significant link existed between year and visitors, with higher numbers of visitors negatively affecting penguin numbers. Based on our results we recommend increased precaution in management at Goudier Island, and initiation of similar studies at other frequently visited penguin sites in Antarctica