Article pubs.acs.org/est
Microplastics in the Terrestrial Ecosystem: Implications for Lumbricus terrestris (Oligochaeta, Lumbricidae) Esperanza Huerta Lwanga,*,†,‡ Hennie Gertsen,‡ Harm Gooren,‡ Piet Peters,‡ Tamás Salánki,§ Martine van der Ploeg,‡ Ellen Besseling,∥,⊥ Albert A. Koelmans,∥,⊥ and Violette Geissen‡ †
Agroecología, El Colegio de la Frontera Sur, Unidad Campeche, Av Poligono s/n, Ciudad Industrial, Lerma, Campeche Mexico Soil Physics and Land Management Group, Wageningen University, Droevendaalsesteeg 4, 6708PB Wageningen, The Netherlands § Soil Quality Department, Wageningen University, Droevendaalsesteeg 4, 6708PB Wageningen, The Netherlands ∥ Aquatic Ecology and Water Quality Management Group, Department of Environmental Sciences, Wageningen University, P.O. Box 47, 6700 AA Wageningen, The Netherlands ⊥ IMARES - Institute for Marine Resources & Ecosystem Studies, Wageningen UR, P.O. Box 68, 1970 AB IJmuiden, The Netherlands ‡
S Supporting Information *
ABSTRACT: Plastic debris is widespread in the environment, but information on the effects of microplastics on terrestrial fauna is completely lacking. Here, we studied the survival and fitness of the earthworm Lumbricus terrestris (Oligochaeta, Lumbricidae) exposed to microplastics (Polyethylene, 28%. We cannot directly compare our data with those from studies for aquatic worms (for instance, the one by Besseling et al.)10 because exposure was different in their study, i.e., from uniformly mixed sediment rather than from a plastic containing layer of litter on top. However, in general terms we see some similar patterns; higher doses of microplastic cause increased uptake, weight loss, and lower growth rates. No effects on reproduction were observed, which may be due to the type of earthworm studied. Large K-strategists earthworms41 such as L. terrestris invest energy in few but heavy cocoons.42−44 Investment in reproduction is favored, and investment in growth rate seems to be compromised under microplastic pressure.45 Darwin recognized the magnitude of the effects that earthworms can have on the environment by the deposition of casts and construction of burrows. Earthworm casts concentrate nutrients;46 for example, L. terrestris casts in loam soil contain 2-fold more organic carbon than the surrounding soil.46 The concentration of microplastics in our study with 7% microplastics was also twice as high in casts than in the original litter, which can be explained by the digestion of organic matter, leading to the concentration of the persistent microplastic in the cast. The cast concentration factor CF was highest for the 7% treatment, which implies that this process was most efficient at this microplastic concentration in the litter. This can be explained from the fact that at this dose, the percentage of organic matter in the ingested litter (i.e., 93%) was highest, leading to a high increase in concentration of the microplastic in the cast due to partial digestion of this organic matter. L. terrestris casts with concentrated microplastics are then deposited on the walls of the burrows or on the soil surface. This concentration of microplastics on cast by a factor of 2 leads to a higher risk of incorporation of microplastic into the soil, with possibly enhanced leaching to the groundwater. The dose of 7% microplastics in litter was not harmful for L. terrestris during 60 days, probably because at this dose, still-sufficient nutritious organic matter is available (i.e., 93%). The treatments with microplastic concentrations in litter higher than 7%, however, showed progressively lower increases in concentration in the casts. This can be explained from the fact that at the very high plastic concentrations in the ingested litter, only relatively small amounts of organic matter are available for digestion, leading to a more limited relative
increase in concentration of microplastic in the cast. Consequently, CF approaches unity (within error limits) at high microplastic concentrations. As a consequence, under these conditions, L. terrestris expels the microplastics directly into the environment, resulting in casts with the same concentration as in the litter. Although this proposed mechanism is quite plausible, here we emphasize that this study was not designed to elucidate these physiological mechanisms, which implies that more work on this mechanism is to be recommended. We found a different microplastic size distribution in egested casts compared to the ingested litter microplastics. It appeared that the smallest particles are preferentially retained in the worms, which most likely suggests microplastics particle selection,47,48 although formally, the decomposition of the smallest particles in the gut of L. terrestris cannot be excluded. The bioaccumulation of microplastics in earthworms like L. terrestris may cause longer-term ecological effects to this species but may also lead to the transfer of microplastics to other organisms because earthworms form the base of many food chains. We conclude that the ecological impact of microplastics on soil involves effects on various levels. First, K-strategy earthworms fitness seems not to be affected by microplastics dosed via litter on the soil surface at a concentration in litter of 7% w/w, but with 28, 45, and 60% w/w microplastics in litter, L. terrestris is affected (i.e., decrease in growth rate and consequent weight loss). No effect on reproduction was observed even with higher concentrations. Second, microplastics may have effects on the ecosystem level on primary and secondary productivity, organic-matter decomposition, and nutrient cycling. After all, once microplastics are in casts and available, they can be transferred to other organisms, or they can be degraded by microorganisms that participate in nutrient cycling. Third, the bioconcentration of microplastics (i.e., from 7% microplastic in litter) on cast by a factor of 2 may lead to a higher risk of incorporation of microplastic into the soil with possibly enhanced leaching to the groundwater.
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.5b05478. Images showing soil surface cover by plastic, Lumbricus terretris mesocosms, Lumbricus terrestris cocoons collected from mesocosms, Lumbricus terrestris in petri dishes after 2 days of starvation, microplastics (white particles) collected from casts, and Lumbricus terrestris in E
DOI: 10.1021/acs.est.5b05478 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Article
Environmental Science & Technology
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petri dishes. A graph showing preliminary Lumbricus terrestris mortality study. A table showing treatment descriptions. (PDF)
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We acknowledge Michiel Kotterman for providing the microplastics and good advice for using them. E.H. thanks the WIMEK Institute of Wageningen University for providing a fellowship as a visiting scientist in 2015. We thank Xiaomei Yang and Hongming Zhang for the field plastic photos, and we are grateful to three anonymous reviewers for their valuable and useful comments.
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NOTE ADDED AFTER ASAP PUBLICATION This paper published ASAP on February 8, 2016 with incomplete corrections. The corrected paper reposted on February 10, 2016.
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DOI: 10.1021/acs.est.5b05478 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
