A deep dive into fat: Investigating blubber lipidomic fingerprint of killer whales and humpback whales in northern Norway

In cetaceans, blubber is the primary and largest lipid body reservoir. Our current understanding about lipid stores and uses in cetaceans is still limited, and most studies only focused on a single narrow snapshot of the lipidome. We documented an extended lipidomic fingerprint in two cetacean species present in northern Norway during wintertime. We were able to detect 817 molecular lipid species in blubber of killer whales (Orcinus orca) and humpback whales (Megaptera novaeangliae). The profiles were largely dominated by triradylglycerols in both species and, to a lesser extent, by other constituents including glycerophosphocholines, phosphosphingolipids, glycerophosphoethanolamines, and diradylglycerols. Through a unique combination of traditional statistical approaches, together with a novel bioinformatic tool (LION/web), we showed contrasting fingerprint composition between species. The higher content of triradylglycerols in humpback whales is necessary to fuel their upcoming half a year fasting and energy-demanding migration between feeding and breeding grounds. In adipocytes, we assume that the intense feeding rate of humpback whales prior to migration translates into an important accumulation of triacylglycerol content in lipid droplets. Upstream, the endoplasmic reticulum is operating at full capacity to supply acute lipid storage, consistent with the reported enrichment of glycerophosphocholines in humpback whales, major components of the endoplasmic reticulum. There was also an enrichment of membrane components, which translates into higher sphingolipid content in the lipidome of killer whales, potentially as a structural adaptation for their higher hydrodynamic performance. Finally, the presence of both lipid-enriched and lipid-depleted individuals within the killer whale population in Norway suggests dietary specialization, consistent with significant differences in δ15N and δ13C isotopic ratios in skin between the two groups, with higher values and a wider niche for the lipid-enriched individuals. Results suggest the lipid-depleted killer whales were herring specialists, while the lipid-enriched individuals might feed on both herrings and seals

Higher plasma oxidative damage and lower plasma antioxidant defences in an Arctic seabird exposed to perfluoroalkyl carboxylic acids

International audiencePerfluoroalkyl and polyfluoroalkyl substances (PFASs) may cause detrimental effects on physiological function and reproduction of Arctic animals. However, there is a paucity of information on the link between PFASs and oxidative stress, which can have potential detrimental effects on key fitness traits, such as cellular homeostasis or reproduction. We have examined the correlations between multiple blood-based markers of oxidative status and several perfluoroalkyl acids (i.e., with 8 or more carbons) in male Arctic black-legged kittiwakes (Rissa tridactyla) during the pre-laying period. Higher protein oxidative damage was found in those birds having higher concentrations of perfluorododecanoic acid (PFDoA), perfluorotridecanoic acid (PFTriA) and perfluorotetradecanoic acid (PFTeA). Lower plasmatic non-enzymatic micro-molecular antioxidants were found in those birds having higher concentrations of perfluoroundecanoic acid (PFUnA), PFDoA and PFTeA. Effect size estimates showed that the significant correlations between PFASs and oxidative status markers were intermediate to strong. The non-enzymatic antioxidant capacity (including antioxidants of protein origin) was significantly lower in those birds having higher plasma concentration of linear perfluorooctanesulfonic acid (PFOSlin). In contrast, the activity of the antioxidant enzyme glutathione peroxidase in erythrocytes was not associated with any PFAS compounds. Our results suggest that increased oxidative stress might be one consequence of long-chain PFASexposure. Experimental work will be needed to demonstrate whether PFASs cause toxic effects on free-living vertebrates through increased oxidative stress

Establishment of killer whale (Orcinus orca) primary fibroblast cell cultures and their transcriptomic responses to pollutant exposure

Populations of killer whale (Orcinus orca) contain some of the most polluted animals on Earth. Yet, the knowledge on effects of chemical pollutants is limited in this species. Cell cultures and in vitro exposure experiments are pertinent tools to study effects of pollutants in free-ranging marine mammals. To investigate transcriptional responses to pollutants in killer whale cells, we collected skin biopsies of killer whales from the Northern Norwegian fjords and successfully established primary fibroblast cell cultures from the dermis of 4 out of 5 of them. Cells from the individual with the highest cell yield were exposed to three different concentrations of a mixture of persistent organic pollutants (POPs) that reflects the composition of the 10 most abundant POPs found in Norwegian killer whales (p,p’-DDE, trans-nonachlor, PCB52, 99, 101, 118, 138, 153, 180, 187). Transcriptional responses of 13 selected target genes were studied using digital droplet PCR, and whole transcriptome responses were investigated utilizing RNA sequencing. Among the target genes analysed, CYP1A1 was significantly downregulated in the cells exposed to medium (11.6 µM) and high (116 µM) concentrations of the pollutant mixture, while seven genes involved in endocrine functions showed a non-significant tendency to be upregulated at the highest exposure concentration. Bioinformatic analyses of RNA-seq data indicated that 13 and 43 genes were differentially expressed in the cells exposed to low and high concentrations of the mixture, respectively, in comparison to solvent control. Subsequent pathway and functional analyses of the differentially expressed genes indicated that the enriched pathways were mainly related to lipid metabolism, myogenesis and glucocorticoid receptor regulation. The current study results support previous correlative studies and provide cause-effect relationships, which is highly relevant for chemical and environmental management.publishedVersio

High levels of mercury and low levels of persistent organic pollutants in a tropical seabird in French Guiana, the Magnificent frigatebird, Fregata magnificens

In the present study, trace elements and persistent organic pollutants (POPs) were quantified from Magnificent frigatebirds (Fregata magnificens) breeding at a southern Atlantic island. Stable isotope ratio of carbon (δ13C) and nitrogen (δ15N) were also measured to infer the role of foraging habitat on the contamination. For another group from the same colony, GPS tracks were recorded to identify potential foraging areas where the birds may get contaminated. Fourteen trace elements were targeted as well as a total of 40 individual POPs, including organochlorine pesticides (OCPs), polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs). The concentration of Hg in the blood was up to 6 times higher in adults (5.81 ± 1.27 μg g−1 dw.) than in nestlings (0.99 ± 0.23 μg g−1 dw.). A similar pattern was found for POPs. ∑PCBs was the prevalent group both in adults (median 673, range 336–2801 pg g−1 ww.) and nestlings (median 41, range 19–232 pg g−1 ww.), followed by the sum of dichlorodiphenyltrichloroethanes and metabolites (∑DDTs), showing a median value of 220 (range 75–2342 pg g−1 ww.) in adults and 25 (range 13–206 pg g−1 ww.) in nestlings. The isotope data suggested that the accumulation of trace elements and POPs between adults and nestlings could be due to parental foraging in two different areas during incubation and chick rearing, respectively, or due to a shift in the feeding strategies along the breeding season. In conclusion, our work showed high Hg concentration in frigatebirds compared to non-contaminated seabird populations, while other trace elements showed lower values within the expected range in other seabird species. Finally, POP exposure was found generally lower than that previously measured in other seabird specie

Occurrence of emerging brominated flame retardants and organophosphate esters in marine wildlife from the Norwegian Arctic

To understand the exposure and potential sources of emerging brominated flame retardants (EBFR) and organophosphate esters (OPEs) in marine wildlife from the Norwegian Arctic, we investigated concentrations of EBFRs in 157 tissue samples from nine species of marine vertebrates and OPEs in 34 samples from three whale species. The samples, collected from a wide range of species with contrasting areal use and diets, included blubber of blue whales, fin whales, humpback whales, white whales, killer whales, walruses and ringed seals and adipose tissue and plasma from polar bears, as well as adipose tissue from glaucous gulls. Tris(2-ethylhexyl) phosphate (TEHP) and tris(2-chloroisopropyl) phosphate (TCIPP) ranged from <0.61 to 164 and < 0.8–41 ng/g lipid weight, respectively, in blue whales and fin whales. All other EBRFs and OPEs were below the detection limit or detected only at low concentration. In addition to the baseline information on the occurrence of EBFRs and OPEs in marine wildlife from the Arctic, we provide an in-depth discussion regarding potential sources of the detected compounds. This information is important for future monitoring and management of EBFRs and OPEs

Conséquences physiologiques d’une exposition aux substances perfluoroalkylées, aux composés organochlorés et au mercure chez un oiseau marin Arctique

Due to increasing human activities, a growing number of threats are challenging the fate of biodiversity. Among them, environmental contamination is particularly concerning for living organisms. Used and released in industrialized countries, these highly persistent contaminants can reach remote areas such as the Arctic ecosystem and will biomagnify though food webs and bioaccumulate in organisms. Long-lived seabirds are located in the upper levels of the food chains and thus particularly exposed and sensitive to a chronic contaminants exposure. Through endocrine disruption, these contaminants can impact physiological mechanisms and behavioural traits, inducing in fine, long-term fitness consequences on individuals and populations. My thesis focuses on three groups of contaminants: (i) poly- and perfluoroalkyl substances (PFASs), still broadly used in a vast array of industrial processes and increasing in the Arctic; (ii) “legacy” organochlorine contaminants (OCs, pesticides and industrial compounds), banned from use but still well present in the Arctic and (iii) mercury (Hg), a non-essential metal coming of both natural and anthropic origins. Based on a correlative approach conducted in natura, I investigated the physiological and behavioural consequences of exposure to these contaminants during the whole breeding cycle (from pre-laying to chick-rearing period) in an Arctic seabird, the black-legged kittiwake (Rissa tridactyla) from Svalbard, Norwegian Arctic. Specifically, I examined the relationships between several PFASs, OCs, Hg and fertility (sperm morphology and motility), sexual signaling (visual: integument coloration and olfactory: chemical signature), parental care behaviors (incubation temperature and egg-turning), ageing (telomere length) and energy expenditure (basal metabolic rate). In addition, some potential underlying mechanisms were also studied to better understand the way through which contaminants can be detrimental for kittiwakes. Furthermore, since physiological mechanisms and behavioral traits investigated here are tightly involved in self maintenance and reproduction, possible effects on fitness are then discussed. This PhD work underlines the major role of certain legacy chlorinated organic compounds (e.g. chlordanes) and significantly contributes at documenting the poorly known toxicological consequences of PFASs exposure in wildlife. Importantly, this PhD shows that PFASs and OCs could impact ageing, energy expenditure and some parental care behaviors in a contrasted manner. Specifically, oxychlordane, a metabolite of a banned organochlorine pesticide was associated with decreased telomere length, lowered metabolic rate and reduced ability to incubate the eggs. Conversely, elongated telomere, increased BMR and enhanced egg rotation were observed in birds bearing the highest concentrations of PFASs. Finally, at least for the considered endpoints, Hg appears as a coming minor threat for kittiwakes. This study highlights the importance of considering several groups of contaminants when investigating the consequences of environmental contaminants exposure in wildlife.A cause d’une anthropisation toujours plus forte des écosystèmes, de plus en plus de menaces pèsent sur la biodiversité. Parmi celles-ci, l’exposition aux contaminants est particulièrement problématique pour les organismes vivants. Emis et utilisés dans les pays industrialisés, ces contaminants hautement persistants dans l’environnement vont gagner les régions polaires puis se bio-accumuler dans les organismes vivants au cours du temps et se bio-amplifier le long du réseau trophique. Ainsi, les oiseaux marins, longévifs et situés dans les maillons supérieurs de la chaine alimentaire, sont particulièrement exposés et vulnérables à une exposition chronique à ces contaminants. A travers une perturbation endocrinienne, ces contaminants vont pouvoir impacter certains mécanismes physiologiques et traits comportementaux, entrainant in fine des conséquences à long-terme sur la fitness des individus et populations. Ma thèse s’articule autour de trois grandes familles de contaminants : i) les composés perfluoroalkylés (PFASs), encore largement utilisés dans plusieurs secteurs industriels et agricoles et en augmentation dans l’environnement ; (ii) les composés organochlorés dits « d’héritage » (OCs), interdits depuis des années mais entrainants toujours des effets délétères sur la biodiversité et (iii) le mercure (Hg), métal lourd non-essentiel ayant une origine à la fois anthropique et naturelle. Basé sur une approche corrélative in natura, je me suis intéressé aux conséquences physiologiques et comportementales d’une exposition chronique à ces trois grandes familles de contaminants présents chez la mouette tridactyle (Rissa tridactyla) de l’Arctique Norvégien (Svalbard) au cours de son cycle reproducteur (depuis l’accouplement jusqu’à l’élevage des poussins). Spécifiquement, j’ai étudié les relations entre ces contaminants et la fertilité (morphologie et motilité des spermatozoïdes), l’expression des signaux sexuels (visuel : coloration des téguments, olfactif : signature chimique), les comportements de soins parentaux (température d’incubation et rotation de l’œuf), le vieillissement cellulaire (longueur des télomères) et la dépense énergétique (métabolisme de base). Je me suis également penché sur de potentiels mécanismes sous-jacents permettant d’expliquer ces relations. Puisque ces mécanismes physiologiques et comportementaux sont fortement impliqués dans la valeur sélective des individus, les possibles conséquences à long terme de cette exposition sur la reproduction et survie des individus sont discutées. Ce travail permet de souligner la forte toxicité de certains composés organochlorés « historiques » (en particulier les chlordanes) et d’apporter de toutes nouvelles connaissances sur la toxicité très mal connue des PFASs chez la faune sauvage. Fait important, ce travail de thèse révèle que les PFASs et les OCs pourraient agir de manière contrastée sur plusieurs mécanismes physiologiques et traits comportementaux. Spécifiquement, une forte exposition à l’oxychlordane, un métabolite du chlordane, pesticide interdit depuis des décennies, est associée à des télomères plus courts, une réduction du métabolisme de base et à une moindre capacité à incuber les œufs. A l’inverse, on observe une élongation des télomères, une augmentation du métabolisme de base et une rotation des œufs accrue chez les individus les plus exposés aux PFASs. Le Hg, au moins en ce qui concerne les paramètres étudiés, ne semble pas jouer un rôle majeur. Cette étude souligne l'importance de tenir compte de plusieurs groupes de contaminants lorsqu'on étudie les conséquences de l'exposition aux contaminants environnementaux chez la faune sauvage

Mass strandings of seven toothed and baleen whale species in Northern Norway in March 2020 call for further investigation

Monitoring whale strandings are a key aspect of ecosystem management as stranded animals can provide indications on ecosystem health, pollution and adverse efects due to anthropogenic activities. Most mass mortality events are reported for toothed whales and rarely involve baleen whales. In the course of one month in spring 2020, 17 whales belonging to seven diferent species, stranded on the shores of Northern Norway, above the Arctic circle. This multi-species event included humpback (Megaptera novaeangliae), fn (Balaenoptera physalus) and sperm whales (Physeter macrocephalus), that were accompanied by northern bottlenose whales (Hyperoodon ampullatus), a white-beaked dolphin (Lagenorhynchus albirostris), a long-fnned pilot whale (Globicephala melas) and a harbour porpoise (Phocoena phocoena). We discuss some potential causes of death based on the previous literature and available information for the area, highlighting the need for further investigation on cetacean strandings at high latitudes. Ultimately, the reasons for the stranding could only be identifed by a thorough examination of all the animals, which was unfortunately not conducted. As the threats to polar ecosystems and access to local shores are likely to increase, reports of cetacean mortality are also expected to surge, particularly in high latitude regions where climate variations and anthropogenic activities are increasing. This study makes recommendations for future steps and considerations for monitoring networks and standardized sampling methods for future marine mammal stranding events. Finally, we suggest that national and international eforts based on the collaborative relationships are implemented, considering the multiple facets of animal ecology and health as an achievable step in the near future

Comparative egg attendance patterns of incubating polar petrels

International audienceAbstract Background The internal environment of eggs in most birds is regulated by transferring heat energy through contact incubation, maintaining nest microclimate, and frequent egg turning by the incubating parent on its nest. However, we lack information about egg attendance patterns in birds that breed in polar environments where variations in life history are expected to influence incubation behavior. Moreover, crevice/burrow nesting petrels in high-latitude regions are known for periodically leaving their egg unattended (hereafter ‘egg neglect’), but there is little reporting on the internal condition of unattended eggs. At Dumont d’Urville Station, Antarctica, we studied the incubation behavior of 24 snow ( Pagodroma nivea ) and 15 Cape ( Daption capense ) petrel pairs using egg loggers that recorded egg turning rates, orientation changes, and temperatures at 1 Hz for durations of 3–6 days. Results Egg turning frequency (1.31 ± 0.33 vs. 1.38 ± 0.39 turns h −1 ), angle change per turn (43.1 ± 43.2 vs. 48.6 ± 43.7° turn −1 ), and egg temperature (34.1 ± 2.3 vs. 34.1 ± 2.0 °C) were nearly identical for snow and Cape petrels, respectively. However, egg neglect was only observed in snow petrel nests (based on egg temperature changes) where loggers recorded mean durations of 1.34 ± 1.15 days (maximum duration of 3.63 days). During periods of neglect, eggs cooled to 5.5 ± 1.8 °C over an average of 91 min, but were rewarmed by parents in only 76 min at a rate of 0.33 °C min −1 . Conclusions Egg temperatures of both species during regular incubation were within 1–2 °C of other high-latitude petrel species, but neglected snow petrel eggs remained several degrees above freezing, which was likely attributed to crevice nesting where neglected eggs are buffered by environmental conditions. Using egg rewarming rates, thermal capacity of eggs, and published metabolic rates, we estimate egg rewarming costs in snow petrels to be 1.5 to 1.9 × BMR. Excluding egg neglect periods, turning rates for both petrel species were lower than other seabirds studied using biologging devices, which may be associated with the prolonged incubation periods that are characteristic of procellariiform seabirds