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      Probing the Thermodynamics of Biomagnification in Zoo-Housed Polar Bears by Equilibrium Sampling of Dietary and Fecal Samples

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          Abstract

          In a proof-of-concept study, we recently used equilibrium sampling with silicone films to noninvasively derive the thermodynamic limit to a canine’s gastrointestinal biomagnification capability (BMF lim) by determining the ratio of the products of the volume ( V) and fugacity capacity ( Z) of food and feces. In that earlier study, low contaminant levels prevented the determination of contaminant fugacities ( f) in food and feces. For zoo-housed polar bears, fed on a lipid-rich diet of fish and seal oil, we were now able to measure the increase in f of nine native polychlorinated biphenyls (PCBs) upon digestion, providing incontestable proof of the process of gastrointestinal biomagnification. A high average BMF lim value of ∼171 for the bears was caused mostly by a remarkable reduction in fugacity capacity driven by a high lipid assimilation capacity. Lipid-rich diets increase the uptake of biomagnifying contaminants in two ways: because they tend to have higher contaminant concentrations and because they lead to a high Z value drop during digestion. We also confirmed that equilibrium sampling yielded similar Z values for PCBs originally present in food and feces and for isotopically labeled PCBs spiked onto those samples, which makes the method suitable for investigating the biomagnification capability of organisms, even if native contaminant concentrations in their diet and feces are low.

          Abstract

          A completely noninvasive experimental approach provides the biomagnification factor of lipophilic contaminants in higher organisms and proof of gastrointestinal biomagnification.

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          Most cited references47

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          Food web-specific biomagnification of persistent organic pollutants.

          Substances that accumulate to hazardous levels in living organisms pose environmental and human-health risks, which governments seek to reduce or eliminate. Regulatory authorities identify bioaccumulative substances as hydrophobic, fat-soluble chemicals having high octanol-water partition coefficients (K(OW))(>/=100,000). Here we show that poorly metabolizable, moderately hydrophobic substances with a K(OW) between 100 and 100,000, which do not biomagnify (that is, increase in chemical concentration in organisms with increasing trophic level) in aquatic food webs, can biomagnify to a high degree in food webs containing air-breathing animals (including humans) because of their high octanol-air partition coefficient (K(OA)) and corresponding low rate of respiratory elimination to air. These low K(OW)-high K(OA) chemicals, representing a third of organic chemicals in commercial use, constitute an unidentified class of potentially bioaccumulative substances that require regulatory assessment to prevent possible ecosystem and human-health consequences.
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            Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish.

            Persistent organic pollutants (POPs) encompass an array of anthropogenic organic and elemental substances and their degradation and metabolic byproducts that have been found in the tissues of exposed animals, especially POPs categorized as organohalogen contaminants (OHCs). OHCs have been of concern in the circumpolar arctic for decades. For example, as a consequence of bioaccumulation and in some cases biomagnification of legacy (e.g., chlorinated PCBs, DDTs and CHLs) and emerging (e.g., brominated flame retardants (BFRs) and in particular polybrominated diphenyl ethers (PBDEs) and perfluorinated compounds (PFCs) including perfluorooctane sulfonate (PFOS) and perfluorooctanic acid (PFOA) found in Arctic biota and humans. Of high concern are the potential biological effects of these contaminants in exposed Arctic wildlife and fish. As concluded in the last review in 2004 for the Arctic Monitoring and Assessment Program (AMAP) on the effects of POPs in Arctic wildlife, prior to 1997, biological effects data were minimal and insufficient at any level of biological organization. The present review summarizes recent studies on biological effects in relation to OHC exposure, and attempts to assess known tissue/body compartment concentration data in the context of possible threshold levels of effects to evaluate the risks. This review concentrates mainly on post-2002, new OHC effects data in Arctic wildlife and fish, and is largely based on recently available effects data for populations of several top trophic level species, including seabirds (e.g., glaucous gull (Larus hyperboreus)), polar bears (Ursus maritimus), polar (Arctic) fox (Vulpes lagopus), and Arctic charr (Salvelinus alpinus), as well as semi-captive studies on sled dogs (Canis familiaris). Regardless, there remains a dearth of data on true contaminant exposure, cause-effect relationships with respect to these contaminant exposures in Arctic wildlife and fish. Indications of exposure effects are largely based on correlations between biomarker endpoints (e.g., biochemical processes related to the immune and endocrine system, pathological changes in tissues and reproduction and development) and tissue residue levels of OHCs (e.g., PCBs, DDTs, CHLs, PBDEs and in a few cases perfluorinated carboxylic acids (PFCAs) and perfluorinated sulfonates (PFSAs)). Some exceptions include semi-field studies on comparative contaminant effects of control and exposed cohorts of captive Greenland sled dogs, and performance studies mimicking environmentally relevant PCB concentrations in Arctic charr. Recent tissue concentrations in several arctic marine mammal species and populations exceed a general threshold level of concern of 1 part-per-million (ppm), but a clear evidence of a POP/OHC-related stress in these populations remains to be confirmed. There remains minimal evidence that OHCs are having widespread effects on the health of Arctic organisms, with the possible exception of East Greenland and Svalbard polar bears and Svalbard glaucous gulls. However, the true (if any real) effects of POPs in Arctic wildlife have to be put into the context of other environmental, ecological and physiological stressors (both anthropogenic and natural) that render an overall complex picture. For instance, seasonal changes in food intake and corresponding cycles of fattening and emaciation seen in Arctic animals can modify contaminant tissue distribution and toxicokinetics (contaminant deposition, metabolism and depuration). Also, other factors, including impact of climate change (seasonal ice and temperature changes, and connection to food web changes, nutrition, etc. in exposed biota), disease, species invasion and the connection to disease resistance will impact toxicant exposure. Overall, further research and better understanding of POP/OHC impact on animal performance in Arctic biota are recommended. Regardless, it could be argued that Arctic wildlife and fish at the highest potential risk of POP/OHC exposure and mediated effects are East Greenland, Svalbard and (West and South) Hudson Bay polar bears, Alaskan and Northern Norway killer whales, several species of gulls and other seabirds from the Svalbard area, Northern Norway, East Greenland, the Kara Sea and/or the Canadian central high Arctic, East Greenland ringed seal and a few populations of Arctic charr and Greenland shark. Copyright 2009 Elsevier B.V. All rights reserved.
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              The caloric value of whole ringed seals (Phoca hispida) in relation to polar bear (Ursus maritimus) ecology and hunting behavior.

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                Author and article information

                Journal
                Environ Sci Technol
                Environ Sci Technol
                es
                esthag
                Environmental Science & Technology
                American Chemical Society
                0013-936X
                1520-5851
                20 May 2022
                05 July 2022
                : 56
                : 13
                : 9497-9504
                Affiliations
                []Department of Chemistry and Department of Physical and Environmental Sciences, University of Toronto Scarborough , 1265 Military Trail, Toronto, Ontario, Canada M1C 1A4
                []Nutrition Science, Toronto Zoo , 361A Old Finch Avenue, Toronto, Ontario, Canada M1B 5K7
                Author notes
                [* ]F.W.: email, frank.wania@ 123456utoronto.ca ; tel, +1-416-287-7225.
                Author information
                https://orcid.org/0000-0002-4196-4362
                https://orcid.org/0000-0003-3836-0901
                Article
                10.1021/acs.est.2c00310
                9260956
                35593505
                4079024d-af91-4902-9256-049a7f97c52a
                © 2022 The Authors. Published by American Chemical Society

                Permits non-commercial access and re-use, provided that author attribution and integrity are maintained; but does not permit creation of adaptations or other derivative works ( https://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 14 January 2022
                : 30 April 2022
                : 13 April 2022
                Funding
                Funded by: Natural Sciences and Engineering Research Council of Canada, doi 10.13039/501100000038;
                Award ID: NA
                Categories
                Article
                Custom metadata
                es2c00310
                es2c00310

                General environmental science
                biomagnification,equilibrium sampling,noninvasive,fugacity,fugacity capacity

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