Environ Sci Pollut Res DOI 10.1007/s11356-015-4984-7

ECOTOX, THE INRA'S NETWORK OF ECOTOXICOLOGISTS

Plant responses to a phytomanaged urban technosol contaminated by trace elements and polycyclic aromatic hydrocarbons Lilian Marchand 1,2,3 & Celestino-Quintela Sabaris 4 & Dominic Desjardins 5 & Nadège Oustrière 1,2 & Eric Pesme 3 & Damien Butin 3 & Gaetan Wicart 3 & Michel Mench 1,2

Received: 1 May 2015 / Accepted: 29 June 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract Medicago sativa was cultivated at a former harbor facility near Bordeaux (France) to phytomanage a soil contaminated by trace elements (TE) and polycyclic aromatic hydrocarbons (PAH). In parallel, a biotest with Phaseolus vulgaris was carried out on potted soils from 18 sub-sites to assess their phytotoxicity. Total soil TE and PAH concentrations, TE concentrations in the soil pore water, the foliar ionome of M. sativa (at the end of the first growth season) and of Populus nigra growing in situ, the root and shoot biomass and the foliar ionome of P. vulgaris were determined. Despite high total soil TE, soluble TE concentrations were generally low, mainly due to alkaline soil pH (7.8–8.6). Shoot dry weight (DW) yield and foliar ionome of P. vulgaris did not reflect the soil contamination, but its root DW yield decreased at highest soil TE and/or PAH concentrations. Foliar ionomes of M. sativa and P. nigra growing in situ were generally similar

to the ones at uncontaminated sites. M. sativa contributed to b ioa va ila ble T E s tri pp ing by sh oo t re m ov al ( in g ha−1 harvest−1): As 0.9, Cd 0.3, Cr 0.4, Cu 16.1, Ni 2.6, Pb 4, and Zn 134. After 1 year, 72 plant species were identified in the plant community across three subsets: (I) plant community developed on bare soil sowed with M. sativa; (II) plant community developed in unharvested plots dominated by grasses; and (III) plant community developed on unsowed bare soil. The shoot DW yield (in mg ha−1 harvest−1) varied from 1.1 (subset I) to 6.9 (subset II). For subset III, the specific richness was the lowest in plots with the highest phytotoxicity for P. vulgaris.

Keywords Ecological restoration . Gentle remediation option . Medicago sativa . Plant community . Phytoremediation

Responsible editor: Elena Maestri Highlight Medicago sativa well developed on an alkaline soil highly contaminated by trace elements and polycyclic aromatic hydrocarbons at a former harbor dock and displayed low trace element concentrations in its shoots. Phaseolus vulgaris was a relevant bioindicator of soil phytotoxicity. Electronic supplementary material The online version of this article (doi:10.1007/s11356-015-4984-7) contains supplementary material, which is available to authorized users. * Lilian Marchand [email protected]

1

INRA, UMR 1202 BIOGECO, 69 route d’Arcachon, FR-33612 Cestas cedex, France

2

University of Bordeaux, UMR 1202 BIOGECO, Bat B2, Allée Geoffroy St-Hilaire, CS50023, FR-33615 Pessac cedex, France

3

Mairie de BORDEAUX, Service Aménagements Paysagers, Direction des Parcs, des Jardins et des Rives, 77 Boulevard Alfred Daney, 33000 Bordeaux, France

4

Departamento Biología Vegetal y Ecología, Facultad de Ciencia y Tecnologia, Universidad del País Vasco/EHU, 48080 Bilbao, Spain

5

Institut de Recherche en Biologie Végétale (IRBV), Université de Montréal–Jardin Botanique de Montréal, 4101 Rue Sherbrooke, Est Montréal, QC H1X 2B2, Canada

Environ Sci Pollut Res

Abbreviations BTEX Benzene toluene ethylbenzene xylene CEC Cationic exchange capacity DGT Diffusive gradients in thin-film DOM Dissolved organic matter DW Dry weight EC Electrical conductivity EXAFS Extended x-ray absorption fine structure FCA Factorial correspondence analysis GRO Gentle remediation option ISO International organization for standardization Mg Megagram MPC Maximum permitted concentration in green forages in France OM Organic matter PAH Polycyclic aromatic hydrocarbons PCA Principal component analysis PCB Polychlorinated biphenyls SPW Soil pore water TE Trace element THC Total hydrocarbons UCT Upper critical threshold concentration in feedstuff USEPA United State Environmental Protection Agency WHC Water holding capacity XANES X-ray Absorption near edge structure

Introduction In EU, approximately 10 million ha have been contaminated by trace elements (TE) from either anthropogenic or natural sources (Evangelou et al. 2012), totaling 1.5 million, and potentially up to 3 million, contaminated sites (Mench et al. 2010; Panagos et al. 2013). In France, 264,758 sites are recorded in the national inventory of past and present industrial sites and service activities with a potential pollutant source (BASIAS 2015). Among them, 13,835 sites (5.2 %) are located in the Aquitaine region (SW, France), and in particular, 4184 (1.5 %) are in the Gironde county (1.7 % of the total French area), Bordeaux being the major conurbation (BASIAS 2015). Brownfields emerge when a given land use, e.g., a factory or business estate turns from being highly beneficial to society to having a marginal or even detrimental effect or simply comes to an end (HOMBRE 2014). The expansion, redevelopment, and reuse of brownfields may be complicated by the (potential) presence of hazardous substances (USEPA 2011). In France, 5958 brownfields are identified by the national authorities (BASOL 2015). The most common contaminants in soils and groundwater at these sites are hydrocarbons (21.6 %), Pb (10.4 %), PAH (9.7 %), Cu (8.2 %), halogenated solvents (8.2 %), Cr (8.1 %), and As (7.8 %), followed by Zn, Ni, PCB, cyanides, and Cd, respectively (BASOL 2015).

Among these brownfields, 581 sites are located in the Aquitaine region, representing 9.8 % as compared to the total number listed in France. In Aquitaine, 365 sites are monitored, essentially to assess the groundwater quality (63 % of the total brownfields), and 115 sites displayed a justified lack of control (20 % of the total brownfields, BASOL 2015). In the Gironde county, 293 brownfields are listed. Among them, 84 sites are contaminated by hydrocarbons and/or by Pb (36), PAHs (28), Cu (24), As (22), Ni (21), Cr (16), Cd (13), and Zn (6) (site number within brackets, BASOL 2015). Brownfield soils can be secondary sources of trace elements (TE, here essential and non-essential metal(loid)s with common concentrations in plant shoots below 100 mg kg−1 dry weight (DW) Adriano 2001) with human exposure through dermal contact, soil and dust ingestion, and inhalation, leading to health risks (Zheng et al. 2010; PeñaFernández et al. 2014; Soltani et al. 2015). In addition, TE in dissolved and solid forms may migrate to aquatic ecosystems due to runoff and leaching, where they accumulate in sediments and living organisms (Marchand et al. 2011; Moreno-Jiménez et al. 2011; Kalman et al. 2015). Moreover, during short intense summer rainstorms, TE concentrations in effluents released from both main wastewater treatment plants (WWTP) of the Bordeaux conurbation are up to 2 (Cr), 3 (Pb, Cu, and Ni), and 5 (Cd and Zn) times higher than those measured upstream in the Garonne River, respectively (Deycard et al. 2014). Consequently, the Gironde fluvial–estuarine system is subjected to TE contamination (Petit et al. 2013). Trace elements are salted out at high concentrations and generate strong deleterious impacts on the aquatic and terrestrial ecosystems (Deycard et al. 2014). National and European legislations require closer monitoring and regulations on TE released into the environment for coping with these contaminations (Deycard et al. 2014). In France, the National Plans for Health and Environment (e.g., PNSE 3 2014) aims at reducing the pollutant linkages and the exposome. The term pollutant linkage refers to the combination of a source-pathway-receptor, as reported in the Greenland guideline (http://www.greenlandproject.eu), while the term exposome encompasses the totality of human environmental (i.e., non-genetic) exposures from conception onwards, complementing the genome (Wild 2005). On a local scale, PNSE are declined in Regional Plans for Health and Environment (PRSE), and to date in Aquitaine, two PRSE have been implemented (PRSE 2 Aquitaine 2008). Locally, the Bordeaux conurbation (CUB) implements Bgreen^ urban projects to reduce the pollutant linkages, e.g., realization of eco-districts (Ginko project), rehabilitation of a 162ha brownfield site in the Bordeaux downtown (Bassin-àflots project), and ecological restoration of the former harbor docks (Parc-aux-Angéliques project, http://www. developpement-durable.gouv.fr/IMG/pdf/CUB2.pdf)

Environ Sci Pollut Res

The lack of efficient and sustainable remediation technologies combined with other hindrances, e.g., the unwillingness or insolvency/bankruptcy of owners, site abandonment, and weak recognition by the authorities and consultants, has led to either an improper or a complete lack of management of TEcontaminated soils such as brownfields for decades (Adriaensen et al. 2009; Kumpiene et al. 2014). Conventional approaches to contaminated land risk management have focused on containment, cover, and removal to landfill (Cundy et al. 2013). However, shifts are emerging towards sustainable practices within the remediation industry, with particular development of the phytotechnologies (Vangronsveld et al. 2009; Mench et al. 2010; Cundy et al. 2013; Kidd et al. 2015). Among them emerged notably in situ contaminant stab i l i z a t i o n ( Bi n a c t i v a t i o n ^) a n d p l a n t - b a s e d (Bphytoremediation^) options (Cundy et al. 2013; Kumpiene et al. 2014; Kidd et al. 2015). The use of GRO aims at disrupting the pollutant-linkages (DEFRA 2012) either by controlling the source (e.g., extracting the contamination from the subsurface); managing the pathway(s) (e.g., preventing migration of contamination); and protecting the receptor(s) (e.g., planning or institutional controls to avoid sensitive land uses). These options can be used separately or in combination (Cundy et al. 2013). The need to implement a GRO strategy was evaluated at the Chaban-Delmas site (4.5 ha), on the right bank of Garonne River, nearby Bordeaux downtown. This urban brownfield site is the legacy of former industrial and harbor activities. Based on the survey of physicochemical properties, it displays sandy technosols with total TE (Zn, Cd, Cu, As, Mo, and Ni) and PAH concentrations largely higher than that of the common values in French sandy soils, under alkaline conditions (pH > 8) (Marchand and Mench 2014). For this site, TE leaching beneath the technosol and topsoil phytotoxicity was explored to complete the assessment of the pollutant linkages. Therefore, (1) plant testing using dwarf bean (Phaseolus vulgaris L.) was performed on potted technosols from the Chaban-Delmas site for assessing their phytotoxicity, and (2) accordingly, one plant-based GRO was applied on site. Cultivation of alfalfa (Medicago sativa L.) started at the beginning of 2013. The choice of this Fabaceae was based on its beneficial ecological function in cropping systems (Radović et al. 2009) including production of root nodules hosting nitrogen fixation and other plant probiotic bacteria (PPB) (MartínezHidalgo et al. 2014). M. sativa may (1) stimulate the plant/ microorganisms consortium growth (Kirk et al. 2005), (2) play the role of Bnurse plant^ to facilitate the plant community development under TE/PAH excess (Krumins et al. 2015), (3) promote PAH rhizodegradation (Kirk et al. 2005; Sun et al. 2011; Teng et al. 2015), and (4) contribute to TE phytostabilisation (Wang et al. 2012; Zribi et al. 2015). Total and soluble TE concentrations and total PAH contents in technosols developed at the Chaban-Delmas site, plant

growth parameters and foliar ionome of P. vulgaris grown ex situ in potted technosols, the in situ organization of plant communities, plant growth parameters and shoot ionome of M. sativa growing in situ, and foliar ionome of five poplar patches colonizing the site are reported.

Material and methods Soil preparation and analysis The Chaban-Delmas site (4.5 ha) is located in southwest France (44° 51′ 20.416″ N, 0° 33′ 7.89″ W; GPS coordinates are in wgs84), in Bordeaux downtown, at the outlet of the Chaban-Delmas bridge, on the right bank of Garonne River (Fig. 1). This former harbor dock is a brownfield site. From October 2009 to December 2012, it was used as a repository of material stocks and machinery required for the bridge construction. The Bordeaux city has decided to convert it into an urban park. The technosol developed over embankments, displays a sandy texture with high total TE concentrations (in mg kg−1 DW; Zn [392–7899], Cd [1.7–9], Cu [140–2838], As [41–182], Pb [301–1306], and Ni [20–114]) and PAH concentrations (26–163 mg kg−1 DW) in soils exceeding the background values for French sandy soils (Table 1, Baize 2000; Baize et al. 2007; Villaneau et al. 2008; arrêté du 28/ 10/2010), under alkaline conditions (pH>8). Such soil contamination is the legacy of former industrial and harbor activities located on the Garonne riverbanks. The site was firstly divided into 18 plots (50×50 m, labeled from A to R) in June 2013 and then subdivided into 72 subplots (25×25 m, labeled from 1 to 72) in November 2013 (Fig. 1). Among the 18 plots, four plots (A, B, J, and K) were colonized before the site development by a plant community dominated by herbaceous species, which was not mechanically removed during the bridge construction. In contrast, the vegetation on the remaining 14 plots was removed when work began and plot surface turned into a bare soil. Among these 14 plots, 10 were sowed in spring 2013 with M. sativa (C, D, E, F, G L, M, N, O, and P) while four plots (H, I, Q, and R) remained unsowed. Two soil samples (1.5 kg fresh weight, FW, each) were collected at each subplot in November 2013, one within the 0–30 cm soil layer, with an unpainted steel spade, and a second within the 30–60 cm soil layer, after excavation with an excavator (both average soil samples made of n =4 subsamples plot−1 for both soil layers, AFNOR ISO 10381–2 2003). Total soil TE and PAH concentrations were determined respectively by ICP-AES (AFNOR ISO 11885 2009) and GC/ MS at EUROFINS (Saverne, France) using standard methods (Table 1). In the result section, plot labels are indicated within brackets and TE concentrations are expressed in milligram per kilogram DW soil. To measure soil pH and electrical

Environ Sci Pollut Res Fig. 1 Location of the ChabanDelmas site, plots, and sub-plots. Letters (A–R) and numbers (1–72), respectively, indicate the sampling plots (50×50 m) and sub-plots (25×25 m). GPS coordinates are given in wgs84

conductivity (EC), 50 mL of milli-Q water was mixed to 10 g of air-dried soil and the mixture was allowed to react for 2 h before measurements (AFNOR ISO 10390 2005). In August 2013, 1.5 kg FW soil samples from the 0–30 cm soil layer were collected in triplicates in 10 out of the 18 plots (A, D, E, F, I, K, L, N, O, and P) to establish a gradient based on total soil TE. Soils were air dried and sieved at 5 mm. For all soil samples, a 1-kg DW aliquot was potted in a plastic pot (1.3 L). One Rhizon MOM moisture sampler (Eijkelkamp, The Netherlands) was inserted with a 45° angle into each potted soil. Soils were watered twice a week with deionized water and maintained at 70 % of water holding capacity (WHC) during 2 weeks. For all pots, soil-pore water (SPW) was collected (three times 10 mL on the first 3 days of week 36) to make a 30-mL sample and kept at 4 °C prior to TE analysis by ICP-AES at EUROFINS (Bordeaux, France) using standard methods (AFNOR ISO 11885 2009). Plants Plant testing with dwarf beans In August 2013, three soil samples (1.5 kg fresh weight, FW, for each) were collected at each plot within the 0–30 cm soil layer, with an unpainted steel spade. In week 33, soils were air dried, sieved at 2 mm (nylon mesh), and a 1-kg DW aliquot potted in plastic pots

(1.3 L) placed in controlled conditions under a greenhouse (INRA, Villenave d’Ornon, France). Soils were maintained at 70 % of WHC with deionized water. In week 34, four seeds of dwarf beans (P. vulgaris L., cv Saxa) were sowed at 0.5-cm deep in each of the 54 (18×3) pots and in three pots filled with an uncontaminated, air dried, and sieved

Plant responses to a phytomanaged urban technosol contaminated by trace elements and polycyclic aromatic hydrocarbons.

Medicago sativa was cultivated at a former harbor facility near Bordeaux (France) to phytomanage a soil contaminated by trace elements (TE) and polycy...
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