Lipid metabolites as indicators of body condition in highly contaminant-exposed belugas from the endangered St. Lawrence Estuary population (Canada)
Graphical abstract
Introduction
The St. Lawrence Estuary (SLE) beluga (Delphinapterus leucas) lives at the southernmost limit of the species range, and is geographically and reproductively isolated from all other populations in the Arctic. The conservation status of the SLE beluga population, which was estimated to 889 individuals in 2012 (Mosnier et al., 2015), was revised from threatened to endangered in 2014 by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC) (COSEWIC, 2014), a status echoed under the Species at Risk Act (DFO, 2017a). Despite the implementation of multiple protective measures over the years, this population has shown no sign of recovery (DFO, 2017b). Starting around 2000, this population that was relatively stable, started to show a decline in overall abundance and proportion of calves (Mosnier et al., 2015). Since 2008, this population also shows an abnormally elevated rate of newborn mortality (Lesage et al., 2014). The lack of recovery and current decline of the SLE beluga population can be explained by several factors including changes in food resource availability, disturbance from anthropogenic activities, and environmental pollution (DFO, 2014). As such, the critical habitat of SLE belugas overlaps with a busy commercial waterway and is located downstream of highly industrialized and agricultural regions within the Great Lakes and St. Lawrence River basin in Canada and the United States. These are known to discharge via municipal effluents and agricultural runoffs a wide range of organohalogen contaminants, which were found to accumulate in the subcutaneous adipose tissue (blubber) of SLE belugas at occasionally elevated concentrations (Simond et al., 2017, 2019; 2020; Lebeuf et al., 2014). These include polychlorinated biphenyls (PCBs), organochlorine (OC) pesticides, and halogenated flame retardants (HFRs). The extensive use of polybrominated diphenyl ether (PBDE) mixtures (Penta-, Octa-, and Deca-BDE) as HFRs has led to an increase of their concentrations in the blubber of SLE belugas between 1987 and the late 1990s, which have since 1997 remained relatively stable (Lebeuf et al., 2014; Simond et al., 2017). The international regulations on PBDE mixtures in 2009 (Penta- and Octa-BDE) and 2017 (Deca-BDE) have led to their progressive replacement with alternative chemicals known as emerging HFRs (e.g., hexabromobenzene, dechlorane plus, pentabromoethylbenzene, and dechlorane-related compounds) that have been determined at low concentrations in SLE beluga blubber (Simond et al., 2017).
Exposure to environmental contaminants can have deleterious effects on the energy metabolism (Simond et al., 2019, 2020), and ultimately on the health and survival of marine mammals (Ross, 2000; Weijs and Zaccaroni, 2016), and was suggested to be a contributing factor to certain causes of mortality reported in the SLE beluga population (Lair et al., 2014). Several organohalogens reported in tissues of SLE belugas, namely PCBs, OC pesticides, PBDEs and emerging HFRs, have been associated with exposure-related effects on the immune system in pinnipeds and cetaceans (Desforges et al., 2016). These are also known to affect endocrine systems in marine mammals (e.g., Sonne, 2010; Routti et al., 2019), including belugas (Villanger et al., 2011; Braverman and Cooper, 2012; Simond et al., 2019). Specifically, Simond et al. (2019, 2020) suggested that elevated organohalogen exposure (e.g., short-chain chlorinated paraffins) in SLE belugas may affect lipid metabolism, which in turn may perturb lipid composition and energy reserves. Energy reserves of toothed whales are mainly concentrated in blubber that can represent up to 40% of their body mass (Cornick et al., 2016; Lockyer, 1991). Lipids in blubber of belugas consist mainly of triacylglycerols (>90% of total lipids; Krahn et al., 2004; Koopman et al., 2018) and constitute a compact energy source, which can make up to 90% of the total body lipid burden (Mau, 2014). Triacylglycerols are composed of three fatty acids, which are used in the production of energy through beta-oxidation or serve as precursors in the synthesis of, among others, essential fatty acids. These are known for their beneficial effects on metabolism and health of humans and several animal species (e.g., Saini and Keum, 2018; Akbary et al., 2011). Perturbation of energy reserves in terms of quantity or quality (physiological condition) in SLE belugas due to exposure to contaminants or any biological and ecological factors leading to poorer body condition may be reflected by changes in their lipid reserves. For instance, alteration of lipid composition has been reported following exposure to PCBs and OC pesticides in certain marine mammals as reviewed by Filimonova et al. (2016). Furthermore, correlations were observed between adipose tissue lipid content and fatness index (i.e., qualitative observation of subcutaneous fat depot) in polar bears from the western Hudson Bay and Beaufort Sea in the Canadian Arctic (Stirling et al., 2008).
The objective of this study was to investigate the associations between body condition and blubber concentrations of organohalogens of major environmental concern and lipid composition (fatty acids, acylcarnitines, lysophosphatidylcholines, phosphatidylcholines, and sphingomyelins) in male and female SLE beluga carcasses recovered between 1998 and 2016, and for which the cause of mortality was confirmed via necropsy. We hypothesized that SLE belugas exhibit profiles of lipids and organohalogens that vary as a function of their body condition and cause of mortality. Organohalogens selected in this study (PCBs, OC pesticides, PBDEs, and emerging HFRs) were among the most abundant contaminants reported in the blubber of SLE belugas, and/or were shown to elicit exposure-related effects on energetic metabolism and endocrine regulation in marine mammals including SLE belugas (emerging HFRs: Simond et al., 2019, 2020). Results from this study will provide important knowledge on the status of energy reserves in SLE belugas and the linkages between lipid composition, contaminant exposure, and body condition.
Section snippets
Sampling and necropsies
Samples from the outer blubber including skin (total area: 15 cm2) were obtained from 51 adult belugas (37 females and 14 males) found dead between 1998 and 2016 in the Estuary or Gulf of St. Lawrence, Canada. A stage of decomposition was attributed to each beluga carcass in the field according to the scale described by Geraci and Lounsbury (2005) as follows: 1: Live animals; 2: Carcass in good condition (fresh/edible); 3: Fair (decomposed, but organs basically intact); 4: Poor (advanced
Biological variables, body condition and causes of mortality
Male SLE belugas were 15% larger (total body length) and 50% heavier (body mass) than females (Table 1). However, both sexes showed similar scaled mass index (indicator for body condition) and age distribution (Table 1). All SLE belugas in our sample were adults (i.e., ≥8 years old; Suydam, 2010). Scaled mass index differed significantly between the three body condition groups in both males and females (−2.88 < z-score < 5.66; 0.001 < p < 0.02; Fig. S1). Body condition did not vary over the
Discussion
Body condition is a widely used individual fitness metric that represents a key component in marine mammal physiology as it is tightly linked to several biological functions and status of energy reserves. Results from the present study indicated that concentrations of several lipids including phosphatidylcholine analogues were related to changes in body condition in SLE belugas, being in general more abundant in animals in poor body condition relative to those in good body condition. Similar
Conclusions
The present study highlighted for the first time a decrease in fatty acid content in the blubber (outer layer) of SLE belugas over the past two decades (1998–2016). This temporal trend in blubber composition coincides with substantial changes in the vital rates and reproductive cycle of this population. In addition, a change in the composition of PUFA/MUFA ratios and essential fatty acids was observed in male SLE belugas according to their body condition, suggesting that males that are in good
Credit author statement
Conceptualization: Jonathan Verreault, Alexandre Bernier-Graveline. Methodology: Alexandre Bernier-Graveline, Jory Cabrol, Robert Michaud, Maikel Rosabal, Jonathan Verreault. Investigation: Alexandre Bernier-Graveline, Jonathan Verreault. Writing - Original Draft: Alexandre Bernier-Graveline, Jonathan Verreault. Writing - Review & Editing: Alexandre Bernier-Graveline, Véronique Lesage, Jory Cabrol, Stéphane Lair, Maikel Rosabal, Jonathan Verreault. Supervision: Jonathan Verreault. Project
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
Funding for this research was provided in part by the National Contaminants Advisory Group of Fisheries and Oceans Canada. We thank K. Brown (Faculté de médecine vétérinaire, Université de Montréal) for assistance with sample handling. We also thank T. Plantevin and S. Amouch (AGAT Laboratories) for PCB and OC pesticide analyses and H. Butler (SGS AXYS) for lipidomic analysis, as well as their advice on data handling. Finally, we extend our appreciation to L. Wang (Université du Québec à
References (64)
- et al.
Cellular fatty acid metabolism and cancer
Cell Metabol.
(2013) - et al.
Immunotoxic effects of environmental pollutants in marine mammals
Environ. Int.
(2016) - et al.
Fatty acid profiling as bioindicator of chemical stress in marine organisms: a review
Ecol. Indicat.
(2016) - et al.
Tumor cell metabolism: cancer's Achilles' heel
Canc. Cell
(2008) - et al.
A twenty-one year temporal trend of persistent organic pollutants in St. Lawrence Estuary beluga, Canada
Sci. Total Environ.
(2014) - et al.
Nuclear sphingolipids: metabolism and signaling
JLR (J. Lipid Res.)
(2008) - et al.
Cancer as a matter of fat: the crosstalk between adipose tissue and tumors
Trends Cancer
(2018) - et al.
Mobilisation of lipophilic pollutants from blubber in northern elephant seal pups (Mirounga angustirostris) during the post-weaning fast
Environ. Res.
(2014) - et al.
Mobilisation of blubber fatty acids of northern elephant seal pups (Mirounga angustirostris) during the post-weaning fast
Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology
(2015) - et al.
Insights into processes of population decline using an integrated population model: the case of the St. Lawrence beluga (Delphinapterus leucas)
Ecol. Model.
(2015)
Adipose tissue and adipocytes support tumorigenesis and metastasis
Biochim. Biophys. Acta
Selective mobilization of fatty acids from adipose tissue triacylglycerols
Prog. Lipid Res.
Glyceroneogenesis and the triglyceride/fatty acid cycle
J. Biol. Chem.
State of knowledge on current exposure, fate and potential health effects of contaminants in polar bears from the circumpolar Arctic
Sci. Total Environ.
Omega-3 and omega-6 polyunsaturated fatty acids: dietary sources, metabolism, and significance - a review
Life Sci.
Temporal trends of PBDEs and emerging flame retardants in belugas from the St. Lawrence Estuary (Canada) and comparisons with minke whales and Canadian Arctic belugas
Environ. Res.
Metabolomic profiles of the endangered St. Lawrence Estuary beluga population and associations with organohalogen contaminants
Sci. Total Environ.
Associations between organohalogen exposure and thyroid-and steroid-related gene responses in St. Lawrence Estuary belugas and minke whales
Mar. Pollut. Bull.
Health effects from long-range transported contaminants in Arctic top predators: an integrated review based on studies of polar bears and relevant model species
Environ. Int.
Fatty acid flux in adipocytes: the in's and out's of fat cell lipid trafficking
Mol. Cell. Endocrinol.
Disruptive effects of persistent organohalogen contaminants on thyroid function in white whales (Delphinapterus leucas) from Svalbard
Sci. Total Environ.
Enrichment of Artemia nauplii with essential fatty acids and vitamin C: effect on rainbow trout (Oncorhynchus mykiss) larvae performance
Iran. J. Fish. Sci.
Distinctive metabolite profiles in in-migrating Sockeye salmon suggest sex-linked endocrine perturbation
Environ. Sci. Technol.
Werner Ingbar's the Thyroid: a Fundamental and Clinical Text. The Cardiovascular System in Thyrotoxicosis
Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation
Mar. Mamm. Sci.
Adipose tissue remodeling: its role in energy metabolism and metabolic disorders
Front. Endocrinol.
Seasonal and developmental differences in blubber stores of belugas in Bristol Bay, Alaska using high-resolution ultrasound
J. Mammal.
COSEWIC Assessment and Status Report on the Beluga Whale Delphinapterus leucas
Relationships between fatty acid composition of body lipids and lipid mobilization in rat. A study of carcass lipids
Ann. Biol. Anim. Biochim. Biophys.
Status of beluga (Delphinapterus leucas) in the St. Lawrence river Estuary
Critical Habitat of the Beluga Whale (Delphinapterus leucas) St. Lawrence Estuary Population Order (SOR/2017-263)
Review of the Effectiveness of Recovery Measures for St. Lawrence Estuary Beluga
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