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Pollutant dehalogenation capability may depend on the trophic evolutionary history of the organism: PBDEs in freshwater food webs.

ABSTRACT: Organohalogen compounds are some of the most notorious persistent pollutants disturbing the Earth biosphere. Although human-made, these chemicals are not completely alien to living systems. A large number of natural organohalogens, part of the secondary metabolism, are involved in chemical trophic interactions. Surprisingly, the relationship between organisms' trophic position and synthetic organohalogen biotransformation capability has not been investigated. We studied the case for polybromodiphenyl ethers (PBDE), a group of flame-retardants of widespread use in the recent years, in aquatic food webs from remote mountain lakes. These relatively simple ecosystems only receive pollution by atmospheric transport. A large predominance of the PBDE congener currently in use in Europe, BDE-209, largely dominated the PBDE composition of the basal resources of the food web. In contrast, primary consumers (herbivores and detritivores) showed a low proportion of BDE-209, and dominance of several less brominated congeners (e.g. BDE-100, BDE47). Secondary consumers (predators) showed large biomagnification of BDE-209 compare to other congeners. Finally, top predator fish characterized by low total PBDE concentrations. Examination of the bromine stable isotopic composition indicates that primary consumers showed higher PBDE biotransformation capability than secondary consumers. We suggest that the evolutionary response of primary consumers to feeding deterrents would have pre-adapted them for PBDE biotransformation. The observed few exceptions, some insect taxa, can be interpreted in the light of the trophic history of the evolutionary lineage of the organisms. Bromine isotopic composition in fish indicates that low PBDE values are due to not only biotransformation but also to some other process likely related to transport. Our finding illustrates that organohalogen compounds may strongly disturb ecosystems even at low concentrations, since the species lacking or having scarce biotransformation capability may be selectively more exposed to these halogenated hydrophobic semi-volatile organic pollutants due to their high bioaccumulation potential.

SUBMITTER: Bartrons M

PROVIDER: S-EPMC3407054 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Pollutant dehalogenation capability may depend on the trophic evolutionary history of the organism: PBDEs in freshwater food webs.

Bartrons Mireia M Grimalt Joan O JO de Mendoza Guillermo G Catalan Jordi J

PloS one 20120727 7

Organohalogen compounds are some of the most notorious persistent pollutants disturbing the Earth biosphere. Although human-made, these chemicals are not completely alien to living systems. A large number of natural organohalogens, part of the secondary metabolism, are involved in chemical trophic interactions. Surprisingly, the relationship between organisms' trophic position and synthetic organohalogen biotransformation capability has not been investigated. We studied the case for polybromodip ...[more]

PMID: 22848624

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Project description:Detritivory is the dominant trophic paradigm in most terrestrial, aquatic, and marine ecosystems, yet accurate measurement of consumer trophic position within detrital (="brown") food webs has remained unresolved. Measurement of detritivore trophic position is complicated by the fact that detritus is suffused with microbes, creating a detrital complex of living and nonliving biomass. Given that microbes and metazoans are trophic analogues of each other, animals feeding on detrital complexes are ingesting other detritivores (microbes), which should elevate metazoan trophic position and should be rampant within brown food webs. We tested these hypotheses using isotopic (15N) analyses of amino acids extracted from wild and laboratory-cultured consumers. Vertebrate (fish) and invertebrate detritivores (beetles and moths) were reared on detritus, with and without microbial colonization. In the field, detritivorous animal specimens were collected and analyzed to compare trophic identities among laboratory-reared and free-roaming detritivores. When colonized by bacteria or fungi, the trophic positions of detrital complexes increased significantly over time. The magnitude of trophic inflation was mediated by the extent of microbial consumption of detrital substrates. When detrital complexes were fed to vertebrate and invertebrate animals, the consumers registered similar degrees of trophic inflation, albeit one trophic level higher than their diets. The wild-collected detritivore fauna in our study exhibited significantly elevated trophic positions. Our findings suggest that the trophic positions of detrital complexes rise predictably as microbes convert nonliving organic matter into living microbial biomass. Animals consuming such detrital complexes exhibit similar trophic inflation, directly attributable to the assimilation of microbe-derived amino acids. Our data demonstrate that detritivorous microbes elevate metazoan trophic position, suggesting that detritivory among animals is, functionally, omnivory. By quantifying the impacts of microbivory on the trophic positions of detritivorous animals and then tracking how these effects propagate "up" food chains, we reveal the degree to which microbes influence consumer groups within trophic hierarchies. The trophic inflation observed among our field-collected fauna further suggests that microbial proteins represent an immense contribution to metazoan biomass. Collectively, these findings provide an empirical basis to interpret detritivore trophic identity, and further illuminate the magnitude of microbial contributions to food webs.

Dataset Information

Pollutant dehalogenation capability may depend on the trophic evolutionary history of the organism: PBDEs in freshwater food webs.

Publications

Pollutant dehalogenation capability may depend on the trophic evolutionary history of the organism: PBDEs in freshwater food webs.

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