The ability of terrestrial Oligochaeta to survive in ultramafic soils and the assessment of toxicity at different levels of organisation

[摘要] Metals are natural elements of the earth crust usually present at low concentrations in all soils.Although many metals such as cobalt, copper, iron and zinc are essential to living organisms, atelevated concentrations most metals are toxic to organisms living in and on soils. Elevatedconcentrations of metals are caused either by anthropogenic deposition following remobilisationfrom the earth crust or are of natural origin.Ultramafic soils do not only pose unfavourable living conditions such as drought and poor organiccontent, these soils are also characterized by extremely high concentrations of a range of metalsknown to be toxic under normal circumstances. Ultramafic soils are of high ecological importanceas a high proportion of endemic organisms, especially plants, live on these soils.As it is known that earthworms do occur in ultramafic soils, the aims of the present study were toinvestigate the abilities of earthworms to survive in these soils and the influences of elevatedchromium, cobalt, copper, manganese and nickel levels.For the evaluation of the metal background conditions, soils originating from ultramafic rocks of theBarberton Greenstone Belt, Mpumalanga, South Africa were collected and different fractionsrepresenting different levels of bioavailability were analyzed for arsenic, chromium, cobalt, copper,manganese and nickel. To assess the mobile, readily available metal fraction, i.e. Ca2+-exchangeable metal cations, a 0.01 mol/L CaCl2 extraction was performed. To investigate themobilisable metal fraction, representing the amount of easily remobilisable complexed andcarbonated metal ions, a DTPA (di-ethylene-triamine-pentaacetic acid) extraction was conducted.In relation to non-ultramafic or anthropogenic contaminated soils, a far lower proportion of metalswere extractable by the above mentioned extraction methods.To investigate the availability and effects of these metals on earthworms, two ecophysiologicallydifferent species were employed. Aporrectodea caliginosa and Eisenia fetida were long-termexposed to the ultramafic soils collected at the Barberton region and a control soil from a locationat Stellenbosch with a known history of no anthropogenic metal contamination. The responses tothe ecological stress originating in the ultramafic soils were measured on different levels ofearthworm organisation. As endpoints affecting population development, cocoon production,fecundity and viability were evaluated. On individual level, growth, metal body burden and tissuedistribution were investigated. As endpoints on subcellular level, the membrane integrity wasassessed by the neutral red retention assay, the mitochondrial activity was measured by the MTTcolorimetric assay and as a biomarker for the DNA integrity, the comet assay was performed.Focussing on manganese and nickel, the uptake by E. fetida of these metals was investigated withthe exclusion of soil related properties using an artificial aqueous medium to draw comparisons tothe uptake of these metals in natural soils.The possible development of resistance towards nickel was tested by exposing pre-exposed (formore than 10 generations) E. fetida specimens to ultramafic soils with concentrations of more than4000 mg/kg nickel. The results showed that, except on the endpoint survival, which was less sensitive than all otherbioassays, significant responses to the ultramafic challenge were observed in all earthwormbioassays and on all levels of organisation. The sensitivity of the responses of the earthwormstowards the ultramafic conditions was not predictable by the level of organisation.The two species showed different strategies of metal elimination. In A. caliginosa, metals such asnickel, manganese and chromium were transported to the posterior section and the posteriorsection was subsequently pushed off by autotomization. In E. fetida, metals such as chromium andnickel were sequestered in storage compartments in the coelomic cells or fluid. Other metals, suchas cobalt, were not taken up at elevated concentrations.Although an increased accumulation of nickel was observed in E. fetida specimens pre-exposed tonickel, development of resistance or cross resistance was not observed in this species. In contrast,pre-exposed specimen exposed to elevated concentrations of nickel showed a higher sensitivity interms of survival, indicating the absence of acclimatisation or even genetic adaptation.A comparison of the two species employed indicated that A. caliginosa was less suited for theassessment of the ultramafic soils due to the high individual variation in metal body burden, themass loss observed and the slow reproduction rate even in the control soils. This happeneddespite the fact that A. caliginosa was a soil dwelling species supposed to be better adapted to thesoil substrate than the litter dwelling E. fetida.The toxicity of the ultramafic soils was not necessarily related to total or environmentally availableamounts of the selected metals. Thus, it can be speculated that either these soils containedunidentified toxicants with resulting interactions between toxicants playing an important role orearthworms were able to remobilize metals occurring in these soils.As the singular application of an ecotoxicological endpoint did not give reliable results, especiallyseen over the duration of the exposures, it can be concluded that, when studying soils with such acomplex composition, the utilisation of endpoints addressing different levels of organisation isnecessary for the assessment of toxic stress emerging from these ultramafic soils.

[发布机构] Stellenbosch University