Accumulation of Trace Metal Elements (Cu, Zn, Cd, and Pb) in Surface Sediment via Decomposed Seagrass Leaves: A Mesocosm Experiment Using Zostera marina L.

RESEARCH ARTICLE Accumulation of Trace Metal Elements (Cu, Zn, Cd, and Pb) in Surface Sediment via Decomposed Seagrass Leaves: A Mesocosm Experiment Using Zostera marina L. Shinya Hosokawa1*, Susumu Konuma2¤a, Yoshiyuki Nakamura2¤b 1 Marine Environmental Information Group, Port and Airport Research Institute, 3-1-1 Nagase, Yokosuka, Kanagawa 239–0826, Japan, 2 Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1 Nagase, Yokosuka, Kanagawa 239–0826, Japan a11111 OPEN ACCESS Citation: Hosokawa S, Konuma S, Nakamura Y (2016) Accumulation of Trace Metal Elements (Cu, Zn, Cd, and Pb) in Surface Sediment via Decomposed Seagrass Leaves: A Mesocosm Experiment Using Zostera marina L.. PLoS ONE 11 (6): e0157983. doi:10.1371/journal.pone.0157983 Editor: Jin-Tian Li, Sun Yat-Sen University, CHINA Received: September 14, 2015 Accepted: June 8, 2016 Published: June 23, 2016 Copyright: © 2016 Hosokawa et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work was supported by the Steel Industry Foundation for the Advancement of Environmental Protection Technology (http://sept.or. jp/index.html). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. ¤a Current address: Department of Civil Engineering, Nihon University, 1–8 Kanda Surugadai, Chiyoda-ku, Tokyo 101–8308, Japan ¤b Current address: Department of Civil Engineering, Yokohama National University, 79–5 Tokiwadai, Hodogaya-ku, Yokohama, Kanagawa 240–8501, Japan * Abstract Accumulation of Cu, Zn, Cd, and Pb in the sediment of seagrass ecosystems was examined using mesocosm experiments containing Zostera marina (eelgrass) and reference pools. Lead was approximately 20-fold higher in the surface sediment in the eelgrass pool than in eelgrass leaves and epiphytes on the eelgrass leaves, whereas zinc and cadmium were significantly lower in the surface sediment than in the leaves, with intermediate concentrations in epiphytes. Copper concentrations were similar in both the surface sediment and leaves but significantly lower in epiphytes. Carbon and nitrogen contents increased significantly with increasing δ13C in surface sediments of both the eelgrass and reference pools. Copper, Zn, Cd, and Pb also increased significantly with increasing δ13C in the surface sediment in the eelgrass pool but not in the reference pool. By decomposition of eelgrass leaves with epiphytes, which was examined in the eelgrass pool, copper and lead concentrations increased more than 2-fold and approximately a 10-fold, whereas zinc and cadmium concentrations decreased. The high copper and lead concentrations in the surface sediment result from accumulation in decomposed, shed leaves, whereas zinc and cadmium remobilized from decomposed shed leaves but may remain at higher concentrations in the leaves than in the original sediments. The results of our mesocosm study demonstrate that whether the accumulation or remobilization of trace metals during the decomposition of seagrass leaves is trace metal dependent, and that the decomposed seagrass leaves can cause copper and lead accumulation in sediments in seagrass ecosystems. Competing Interests: The authors have declared that no competing interests exist. PLOS ONE | DOI:10.1371/journal.pone.0157983 June 23, 2016 1 / 18 Trace Metal Accumulation in Seagrass Sediments Introduction Seagrass beds, which occur with dense stands of vegetation in coastal and estuarine areas, can be contaminated by trace metals as a consequence of human activity [1] and can be a longterm biogeochemical sink of trace metals [2]. Seagrasses tend to be tolerant of the trace metal impacts in populations in contaminated areas [3]. However, because trace metals may affect benthic community health (e.g. Simpson et al. [4]) and faunal community structures in the ecosystems [5] because of their toxicity, trace metals in seagrass beds would be harmful pollutants in such ecosystems. Plant litter and related biofilms have been suspected of having an important role in the cycling and biotransfer of trace metals in freshwater ecosystems [6]. In seagrass ecosystems seagrass leaves and epiphytes, which attach to the surface of seagrass leaves, are a major productive part of plants [7, 8], and the leaves can be stored efficiently in dense seagrass beds [9–11]. Because they can contain high concentrations of trace metals, at concentrations correlating to environmental concentrations [12, 13], they are suggested to have significant roles in the cycling of trace metals [14–16]. In addition, accumulation and remobilization of trace metals that occur in the leaves after shedding would be a key process of their biogeochemical deposition in natural seagrass beds. However, disturbances by waves and currents make it difficult to clarify their mechanisms in the natural field. Few previous studies have focused on estimations of the variation in trace metal concentrations in seagrass beds. Lyngby and Brix [17] examined leaf decomposition of the seagrass Zostera marina (eelgrass) in a flow-through system to test the effects of shed leaves on the beds. Their results explain that the sedimentation of dead eelgrass leaves had higher concentration of lead and chromium and lower concentrations of cadmium than green, living leaves in natural eelgrass beds in the Limfjord, Denmark. However, their results could not explain the behaviour of zinc. The insufficient explanation for zinc may be the result of their experiments being performed using experimental seawater, which may have differed from that in the field, and by the complex conditions in the field that may not have been simulated in the experimental system. Mesocosm experiments simulate natural field conditions. The mesocosm experiment using pools protected from physical disturbances have the advantage that we can extract biological, chemical, and biochemical interactions in individuals, populations, communities, and ecosystems. For seagrasses, mesocosm experiments have clarified the effects of water temperature on the life span of leaves in a seagrass population [18], species interactions in the community associating with seagrass [19], and the effects of nutrients in the water column and sediments on seagrass growth in seagrass ecosystems [20–22]. By using mesocosm experiments, the cycling mechanisms of trace metals in seagrass beds via the leaves may be revealed. In this study, we focused on the sinking of Cu, Zn, Cd, and Pb in seagrass bed, because their fate and toxicity is commonly focused in seagrass beds [1]. We hypothesized that these trace metal could accumulate in the sediment in se (...truncated)