Filipe R. Ceia

Sexual and individual foraging segregation in Gentoo penguins Pygoscelis papua from the Southern Ocean during an abnormal winter

Knowledge about sexual segregation and gender-specific, or indeed individual specialization, in marine organisms has improved considerably in the past decade. In this context, we tested the “Intersexual Competition Hypothesis” for penguins by investigating the feeding ecology of Gentoo penguins during their austral winter non-breeding season. We considered this during unusual environmental conditions (i.e. the year 2009 had observations of high sea surface and air temperatures) in comparison with the long term average at Bird Island, South Georgia. Through conventional (i.e. stomach contents) and stable isotopic values from red blood cells, plasma and feathers of both male and female Gentoo penguins, we showed that there were significant differences between sexes, with males feeding mainly on fish (54% by mass) followed by crustaceans (38%) whereas females fed mainly on crustaceans (89% by mass) followed by fish (4%). Themisto gaudichaudii was the most important crustacean prey for males (64% by mass; 82% by number; 53% by frequency of occurrence) and females (63% by mass; 77% by number; 89% by frequency of occurrence), contrasting with all previous studies that found Antarctic krill Euphausia superba were generally the main prey. Stable isotopic data showed that, in terms of habitat use (based on δ 13C), there were significant differences in short-term carbon signatures between males and females (based on plasma and red blood cells), suggesting that both sexes explored different habitats, with females exploring more offshore pelagic waters and males feeding more in coastal benthic waters. Based on δ 15N, males fed on significantly higher trophic level than females (based on plasma and red blood cells), in agreement with our diet results., Thus, Gentoo penguins behave in a similar manner to other non-breeding penguins species (e.g. king, macaroni and rockhopper penguins), albeit at a smaller spatial scale (as they do not disperse as these other penguins do), in that they have a wider habitat and trophic niche during the Antarctic Winter (in comparison to Summer). We also detected individual specialization in feeding/trophic levels for each gender, with certain males feeding mainly on fish and certain females mainly on crustaceans, which may be driven the prevailing environmental conditions that lead individuals to search for alternative prey, and cause sexual diet segregation. Our results provide further information to help improve understanding about sexual segregation and individual specialization of marine organisms, while contributing valuable information on the winter diet for Antarctic monitoring programs and for modelling Antarctic marine food webs.

Analysis of stable isotope ratios in blood of tracked wandering albatrosses fails to distinguish a δ13C gradient within their winter foraging areas in the southwest Atlantic Ocean

RATIONALE The main limitation of isotopic tracking for inferring distribution is the lack of detailed reference maps of the isotopic landscape (i.e. isoscapes) in the marine environment. Here, we attempt to map the marine δ(13) C isoscape for the southwestern sector of the Atlantic Ocean, and assess any temporal variation using the wandering albatross as a model species. METHODS Tracking data and blood and diet samples were collected monthly from wandering albatrosses rearing chicks at Bird Island, South Georgia, during the austral winter between May and October 2009. The δ(13) C and δ(15) N values were measured by mass spectrometry in plasma and blood cells, and related to highly accurate data on individual movements and feeding activity obtained using three types of device: GPS, activity (immersion) loggers and stomach temperature probes. RESULTS The tracked birds foraged in waters to the north or northwest of South Georgia, including the Patagonian shelf-break, as far as 2000 km from the colony. The foraging region encompassed the two main fronts in the Southern Ocean (Polar and Subantarctic fronts). The δ(13) C values varied by only 2.1 ‰ in plasma and 2.5 ‰ in blood cells, and no relationships were found between the δ(13) C values in plasma and the mean latitude or longitude of landings or feeding events of each individual. CONCLUSIONS The failure to distinguish a major biogeographic gradient in δ(13) C values suggest that these values in the south Atlantic Ocean are fairly homogeneous. There was no substantial variation among months in either the δ(13) C or the δ(15) N values of plasma or blood cells of tracked birds. As birds did not show a significant change in diet composition or foraging areas during the study period, these results provide no evidence for major temporal variation in stable isotope ratios in consumer tissues, or in the regional marine isoscape in the austral winter of 2009.

Environmentally driven sexual segregation in a marine top predator

Sexual segregation in foraging occurs in many animal species, resulting in the partitioning of resources and reduction of competition between males and females, yet the patterns and drivers of such segregation are still poorly understood. We studied the foraging movements (GPS-tracking), habitat use (habitat modelling) and trophic ecology (stable isotope analysis) of female and male Cory’s shearwaters Calonectris borealis during the mid chick-rearing period of six consecutive breeding seasons (2010–2015). We found a clear sexual segregation in foraging in years of greater environmental stochasticity, likely years of lower food availability. When food became scarce, females undertook much longer foraging trips, exploited more homogeneous water masses, had a larger isotopic niche, fed on lower trophic level prey and exhibited a lower body condition, when compared to males. Sexual competition for trophic resources may be stronger when environmental conditions are poor. A greater foraging success of one sex may result in differential body condition of pair mates when enduring parental effort, and ultimately, in an increased probability of breeding failure.

Distribution, habitat and trophic ecology of Antarctic squid Kondakovia longimana and Moroteuthis knipovitchi: inferences from predators and stable isotopes

Cephalopods have a key role in the marine environment though knowledge of their distribution and trophic ecology is limited by a lack of observations. This is particularly true for Antarctic species. Toothfish species are key predators of cephalopods and may be viewed as ideal biological samplers of these species. A total of 256 cephalopod lower beaks were identified from the stomachs of Patagonian toothfish (Dissostichus eleginoides) and Antarctic toothfish (Dissostichus mawsoni), captured in fisheries of South Georgia and the South Sandwich Islands in the South Atlantic between March and April 2009. Long-armed octopus squid (Kondakovia longimana) and smooth-hooked squid (Moroteuthis knipovitchi) were the main cephalopod prey and both were predated upon wherever toothfish were captured, though this cephalopod species appear to inhabit deeper waters at the South Sandwich Islands than at South Georgia. Measurements of δ13C from beak material indicated a clear segregation of habitat use comparing adult and sub-adult sized K. longimana. Variation in δ15N with size indicated an ontogenetic shift in the diet of cephalopods and also suggested some trophic plasticity among years. This study provides new insights into the private life of some elusive Antarctic cephalopods in an underexplored region of the South Atlantic.

Distribution of short-finned squid Illex argentinus (Cephalopoda: Ommastrephidae) inferred from the diets of Southern Ocean albatrosses using stable isotope analyses

The diets of marine predators are a potential source of information about range shifts in their prey. For example, the short-finned squid Illex argentinus, a commercially fished species on the Patagonian Shelf in the South Atlantic, has been reported in the diet of grey-headed, Thalassarche chrysostoma; black-browed, T. melanophris; and wandering, Diomedea exulans, albatrosses breeding at Bird Island, South Georgia (54°S 28°W) in the Southern Ocean. Tracking data suggest that these birds may feed on I. argentinus while foraging in Southern Ocean waters during their breeding season. This led to the hypothesis that I. argentinus may occur south of the Antarctic Polar Front. To test this hypothesis, we used stable isotope analyses to assess the origin of I. argentinus. We compared I. argentinus beaks from the diets of the three albatross species with beaks of cephalopod species endemic to the Patagonian Shelf and others from the Southern Ocean. Our results show that I. argentinus from the diet of albatrosses at Bird Island have ?13C values in the range ?18.77 to ?15.28‰. This is consistent with ?13C values for Octopus tehuelchus, a typical species from the Patagonian Shelf. In contrast, Alluroteuthis antarcticus, a Southern Ocean squid, has typically Antarctic ?13C in the range ?25.46 to ?18.61‰. This suggests that I. argentinus originated from warmer waters of the Patagonian Shelf region. It is more likely that the albatross species obtained I. argentinus by foraging in the Patagonian Shelf region than that I. argentinus naturally occurs south of the Antarctic Polar Front.

How fishing intensity affects the spatial and trophic ecology of two gull species breeding in sympatry

How fishing intensity affects the spatial and trophic ecology of two gull species breeding in sympatry Diana M. Matos*, Jaime A. Ramos, Joana G. Calado, Filipe R. Ceia, Jessica Hey, and Vitor H. Paiva Department of Life Sciences, MARE—Marine and Environmental Sciences Centre, University of Coimbra, Rua da Matemática 49, 3004–517 Coimbra, Portugal Cardiff School of Biosciences, Cardiff University, The Sir Martin Evans Building, Museum Ave, Cardiff CF10 3AX, UK *Corresponding author: tel: þ 351 91 684 30 81; e-mail: dianammatos92@outlook.com

Eastern rockhopper penguins Eudyptes filholi as biological samplers of juvenile and sub-adult cephalopods around Campbell Island, New Zealand

Early life-history stages of cephalopods are known to play an important role as prey in food webs of the Southern Ocean, but little information is available about their biology and availability to predators. Top predators, such as penguins, are known to feed regularly on coastal juvenile/sub-adult cephalopods. Using eastern rockhopper penguins Eudyptes filholi as coastal biological samplers, we examined in detail the cephalopod component of their diet in Campbell Island (New Zealand) during two consecutive breeding seasons in order to evaluate (1) the relative importance of cephalopods (by frequency of occurrence, by number and by mass) to the diet of both adult and chick penguins, (2) the habitat and trophic levels of the cephalopods in the region and (3) the status of the juvenile/sub-adult cephalopod community in the waters around Campbell Island. Our results show that eastern rockhopper penguins feed on eight species of juvenile and sub-adult cephalopods, with Onykia ingens, Martialia hyadesi and Octopus campbelli being the most important species by frequency of occurrence, number and mass. Differences between the diets of adult and chick penguins and between breeding seasons were found. Habitat (δ13C) and trophic level (δ15N) information also showed that all cephalopod species (and all studied stages) occupy similar habitat on the Campbell shelf, with M. hyadesi showing lower δ15N values than O. ingens and O. campbelli. This study indicates that eastern rockhopper penguins can be valuable biological samplers of local juvenile/sub-adult cephalopods (including poorly known cephalopod species) around Campbell Island when breeding, that these cephalopods were likely to be caught naturally (not from fisheries), providing relevant information for the conservation of these penguins.

Isotopic niches of sympatric Gentoo and Chinstrap Penguins: evidence of competition for Antarctic krill?

As climate change, among other factors, is increasingly affecting Antarctic marine systems, competition for prey may increase between predators, particularly in the Antarctic Peninsula which has warmed more than elsewhere. Under such a context, we tested the feeding and trophic ecology of Gentoo (Pygoscelis papua) and Chinstrap (Pygoscelis antarctica) penguins breeding in sympatry at Livingston Island (Antarctic Peninsula) in a single season. We compared the diets of adults (from faecal samples, and stable isotopes in feathers and blood) and chicks (from stomach contents, and stable isotopes in down feathers, toenails and muscles of chicks that had died of unknown causes). Antarctic krill Euphausia superba dominated the diet of both species, although Gentoo Penguins fed on larger Antarctic krill than did Chinstrap Penguins. Stable isotope analyses of adult tissues revealed that both species fed at different niches in successive years, as depicted by the different levels δ13C in feathers (showing values from the previous breeding season) and whole blood (showing values from the current season). Tissues collected from chicks confirmed their diet over different time scales (i.e. days to weeks): Gentoo Penguins fed at a higher trophic level (possibly due to a more varied diet) and in different habitats than Chinstrap Penguins, providing evidence of isotopic niche separation of penguins. Our results may be relevant to the monitoring programmes of the Convention on the Conservation of Antarctic Marine Living Resources (CCAMLR) and suggest that adult scats, and stomach contents and tissues of recently died chicks, can be used in such programmes.

Stable Isotope Dynamics (δ13C and δ15N) in Neritic and Oceanic Waters of the North Atlantic Inferred From GPS-Tracked Cory’s Shearwaters

Intrinsic markers, such as stable isotopes, are a powerful approach to trace wildlife movements because they do not require initial marking of the organism. The main limitation of the isotopic method is the lack of knowledge in spatio-temporal patterns and dynamics of stable isotopes in marine environments, especially at local scales. Here, we combine GPS-tracks and isotopic signatures from Cory’s shearwaters as a model species to define isoscapes in the North Atlantic, and assess δ13C and δ15N dynamics, from local to regional spatial scales. Tracking data and blood samples were collected seasonally (during pre-laying and chick-rearing periods) across six years (2010-2015) from a total of 191 birds breeding at both neritic and oceanic environments. Tracked birds encompassed a large latitudinal and longitudinal area of the mid-North Atlantic, from the Eastern to Central North Atlantic. Overall, the δ13C and δ15N values of birds’ plasma over the region ranged from -20.2 to -16.2‰, and from 10.8 to 15.5‰, respectively. As expected, strong biogeographic isotopic patterns were found in δ13C values at a regional scale, mostly driven by an inshore/offshore gradient and chlorophyll a concentration. Although a moderate expression of spatial isotopic gradients on δ15N values (i.e. latitudinal and inshore/offshore) in the whole region, these were primarily influenced by temporal drivers (i.e. annual variability). At a local scale (i.e. in a radius of 100 km around the colony, within the neritic environment), both δ13C and δ15N values were very influenced by temporal drivers, suggesting that wide-ranging top consumers are hard to trace locally. This study shows that the δ13C values of marine top consumers are good indicators of the foraging habitat at a regional scale in the mid-North Atlantic, especially in terms of inshore/offshore gradients and areas of higher productivity.