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Grass Litter Decomposition and Soil Animal Colonization: Impact of Benzo(A)Pyrene and Pcb 52 in Former Sewage Fields

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Grass Litter Decomposition and Soil Animal Colonization: Impact of Benzo(A)Pyrene and Pcb 52 in Former Sewage Fields GRASS LITTER DECOMPOSITION AND SOIL ANIMAL COLONIZATION: IMPACT OF BENZO(A)PYRENE AND PCB 52 IN FORMER SEWAGE FIELDS von Diplom Biologin Silvia Pieper aus Mailand (Italien) von der Fakultät VII -Architektur, Umwelt, Gesellschaft- der Technischen Universität Berlin zur Erlangung des akademischen Grades Doktorin der Naturwissenschaften - Dr. rer. nat. - genehmigte Dissertation Promotionsausschuss: Vorsitzender: Prof. Dr. Dr. B.-M. Wilke Berichter: Prof. Dr. G. Wessolek Berichter: PD Dr. W. Kratz Berichter: Prof. Dr. M. Renger Tag der wissenschaftlichen Aussprache: 14.12.2001 Berlin 2004 D 83 1 SUMMARY Polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs) are organic chemicals ubiquitous in the environment. Because of their toxicity to man, their recalcitrance to degradation and their persistency in the environment, PAHs and PCBs are listed in the inventory of priority pollutants compiled by several Environmental Protection Agencies. The far greatest amount of PAHs and PCBs are stored in the soil. Despite of this fact, the amount of data available on the toxicity of these organic compounds to soil animals and soil processes is very scarce. Aim of this thesis was to assess the response of soil fauna to a contamination of soil and litter with the chosen reference substances benzo(a)pyrene (BaP; PAH) and 2,2'-5,5' tetrachloro- biphenyl (PCB 52; PCB). The overall experimental approach was designed so to investigate the impact of BaP and PCB52 on terrestrial ecosystems at different level of biological organization: Surveyed were the reactions of single species but also the time course of selected soil processes. One further issue addressed to was the characterization of the behavior of the reference compounds exposed in the field by means of litter as carrier matrix. Two litter decomposition experiments were the core experiments of this study. The first was carried out on a former sewage field (RefB field) near Berlin, Germany, employing the litter of the typical grass species of the study area (Agropyron repens L.). The second decomposition experiment was performed under semi-field condition in so-called Mitscherlich vessels. In this second trial, radio-labeled compounds were utilized to contaminate the litter, in contrast to the "cold" BaP and PCB 52 used in the field experiment. The concentrations of extractable parent compounds were monitored in both experiments. After a brief exposure in the field, extractable concentration of BaP as well as of PCB 52 decreased sharply: After one year, only 15 % and 10% of the initial applied amounts, respectively, could be recovered by solvent extraction from the litter of the field experiment. The complete combustion of the litter from the Mitscherlich vessel experiment, however, revealed that 80% of the initially applied 14C activity was still present in the BaP treatment, but only 50% in the PCB 52 variant. Moreover, the 14C activity in the vessels treated with PCB 52 was almost evenly distributed between litter and the topmost soil layers, whereas 95 % of the recovered BaP activity was detected in the litter layer. Thin layer chromatographies of the organic phase of the litter solvent extraction were performed to assess the percentage amount of the non metabolized parent compound vs. the transformed metabolites. The overall picture points to a 'real' loss of PCB 52 and its metabolites during the exposure in the field, with the remaining 14C activity in the litter still belonging to the parent compound. In contrast, BaP was metabolized to a higher extent, but the transformed metabolites were strongly bound to the organic matrix and did not move into the soil. In the Mitscherlich vessels, the grass litter decomposed more slowly than in the field. After 9 months, 65% of the litter remained in these containers in contrast to 45 % on RefB area. 2 Nevertheless, the two decomposition experiments were comparable regarding the time course of the extractable amounts of BaP and PCB 52: The concentrations were related to the decomposition extent of the litter and not to the absolute time it had been exposed in the field. The contamination of the litter with PCB 52 had no detectable effect on the litter decay rates up to the tested concentration of 11 mg PCB 52 x kg-1 litter. Benzo(a)pyrene, on the contrary, enhanced markedly the decomposition process, with maximum differences in the highly contaminated variants (100 mg BaP x kg-1 litter) of 18 % compared to the uncontaminated controls. The time course of the litter decay as affected by BaP displayed an effect curve typical for an environmental contamination with compounds that become less available or transformed with time: The decay rates were similar in the beginning, diverged with time, but approached the control values towards the end of the experiment. The colonization of the litter by microarthropods revealed a differentiated response of single Collembola and oribatid mite species to the grass litter contamination with BaP and PCB 52. No species was found that reacted with decreased colonization densities to a contamination with BaP. In the PCB 52 treated litter, some species with low dominance displayed reduced individual densities. Euryoecious Collembola and Oribatida did not avoid the highly contaminated litter of both variants. Laboratory tests on the reproductive performance of Collembola were carried out according to ISO standard procedures: Folsomia candida displayed higher reproduction rates in soils contaminated with PCB 52 and BaP. Benzo(a) pyrene influences directly the reproduction rate of soil animals, probably via mimicry of steroid hormone structure. Summarizing the gained insight achieved within this thesis on the reaction of the decomposer community to a contamination with BaP and PCB 52, we may point to the reported higher colonization densities of soil organisms in the field BaP treatments as responsible for the higher litter decay rates. In order to compare the results achieved by means of experimental spiking of litter and soil materials with the possible effects resulting from long-term contamination histories in the field, I investigated the fauna composition and activity in differently contaminated former sewage areas. Reforestation of the fields allowed for a diverse microarthropod fauna to colonize the soils, but the population structure of nematodes reflected the superficiality of the changes occurred, for all species present were typical for strongly disturbed sites. Finally, in a first risk assessment, I applied simple extrapolation methods to the achieved data on the response of soil animals and soil processes to a contamination with BaP and PCB 52. In the investigated sites the maximum soil concentrations at which the soil decomposer community may still be protected from adverse effects are reached. Concerning their loads with organic contaminants, the sewage field soils have no security margin in respect to the compliance of protection targets as defined in the German Soil Protection Act. 3 ZUSAMMENFASSUNG Polyzyklische Aromatische Kohlenwasserstoffe (PAKs) und Polychlorierte Biphenyle (PCBs) sind organische Stoffverbindungen mit einer ubiquitären Umweltverbreitung. Aufgrund ihrer Toxizität für den Menschen, ihrer geringen Abbaubarkeit und ihrer hohen Persistenz in der Umwelt werden PAKs und PCBs in den Listen prioritärer Schadstoffe vieler Länder geführt. Obwohl der größte Anteil der PAKs und PCBs in terrestrischen Ökosystemen gespeichert vorliegt, sind die Kenntnisse über die Toxizität dieser organischen Verbindungen für Boden- organismen und Bodenprozesse sehr gering. Ziel dieser Arbeit war es, die Auswirkungen einer Belastung von Streu und Boden mit den Referenzsubstanzen Benzo(a)pyren (BaP; PAK) und 2,2'-5,5'-Tetrachlorbiphenyl (PCB 52; PCB) auf die Bodenfauna zu charakterisieren und zu bewerten. Der experimentelle Ansatz wurde so gewählt, dass der Einfluss von BaP und PCB 52 auf Bodenorganismen auf verschiedenen Stufen biologischer Organisation untersucht werden konnte. Hierfür wurden sowohl die Reaktionen einzelner Arten erfasst, als auch der zeitliche Ablauf wichtiger Bodenprozesse aufgezeichnet. Ein weiterer Schwerpunkt der Arbeit bestand in der Charakterisierung des Verhaltens der gewählten PAK- und PCB-Referenzsubstanzen im Laufe der Freilandversuche. Zwei Streuabbauversuche bildeten die Hauptuntersuchungen dieser Arbeit. Der erste Streu- abbauversuch wurde auf einer ehemaligen Rieselfeldfläche (RefB) in der Nähe von Berlin mit standorttypischer Streu (Agropyron repens L.) durchgeführt. Der zweite Versuch fand dagegen unter semi-Freiland-Bedingungen in sogenannten Mitscherlich-Gefäßen statt: hier konnte radioaktiv markiertes BaP und PCB 52 eingesetzt werden, im Gegensatz zu den "kalten" Substanzen in den Freilandversuchen. Bereits nach einer kurzen Exposition im Freiland sanken in der Streu die Konzentrationen an extrahierbarem BaP und PCB 52 stark ab. Nach einem Jahr konnten nur noch 15 % bzw. 10 % der applizierten Mengen durch Lösungsmittelextraktion nachgewiesen werden. Eine vollständige Verbrennung der Streu aus den Versuchen mit radioaktiven Referenzsubstanzen zeigte jedoch, dass 80 % der anfänglich applizierten 14C-Aktivität weiterhin in den BaP- Varianten vorhanden war. In den PCB-Varianten konnten dagegen noch 50 % der 14C-Aktivität nachgewiesen werden. Interessanterweise war die 14C-Aktivität in den Varianten, die mit radioaktivem PCB 52 kontaminiert wurden, gleichmäßig zwischen Streu- und oberster Bodenschicht verteilt, wohingegen 95% der wiedergefundenen 14C-Aktivität
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