A tree from waste: Decontaminated dredged sediments for growing forest tree seedlings

Journal of Environmental Management 211 (2018) 269e277

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Journal of Environmental Management journal homepage: www.elsevier.com/locate/jenvman

Research article

A tree from waste: Decontaminated dredged sediments for growing forest tree seedlings Francesca Ugolini a, *, Barbara Mariotti b, 1, Alberto Maltoni b, Andrea Tani b, Fabio Salbitano b, Carlos García Izquierdo c, Cristina Macci d, Graziana Masciandaro d, Roberto Tognetti e, f a

Institute of Biometeorology e National Research Council of Italy, Via G. Caproni 8, 50145 Firenze, Italy  di Firenze, Via S. Bonaventura 13, 50145 Firenze, Italy Dipartimento di Gestione dei Sistemi Agrari, Alimentari e Forestali (GESAAF), Universita Consejo Superior de Investigaciones Cientifica - Centro de Edafologia y Biologia Applicada del Segura, Campus Espinardo, Murcia, Spain d Institute of Ecosystem Studye National Research Council of Italy, c/o Area di Ricerca di Pisa, via Moruzzi 1, 56124 Pisa, Italy e  del Molise, 86100 Campobasso, Italy Dipartimento di Agricoltura, Ambiente e Alimenti, Universita f The EFI Project Centre on Mountain Forests (MOUNTFOR), Edmund Mach Foundation, via E. Mach 1, 38010 San Michele all’Adige, TN, Italy b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 9 November 2017 Received in revised form 19 January 2018 Accepted 21 January 2018 Available online 4 February 2018

The sediments dredged from a waterway and decontaminated through a phytoremediation process have been used as substrates alternatively to the traditional forest nursery substrate for pot productions of holm oak (Quercus ilex L.) planting stocks. The substrates, made by mixing decontaminated sediments to agricultural soil at different degrees, were tested in order to evaluate their suitability as growth substrates. The experiment was carried out at the nursery of the Department of Agricultural, Food and Forestry Systems of the University of Florence (Italy). The experimental design consisted of four randomized blocks with six pots as replicates for each of the following treatments: 100% sediments, 66% sediments, 33% sediments, 100% agronomic soil and 100% traditional peat based substrate. In each pot, one holm oak acorn was seeded. Germination and both physiological and morphological traits of the seedlings were analysed during and at the end of the first growing season. Holm oak grown in phytoremediated sediments at higher concentrations showed germination levels comparable to those in the traditional substrate, and survival capacity (especially in 66% sediments) slightly higher than in 100% soil. Physiological performance of seedlings resembled that on the traditional substrate which required the addition of fertilizer, at least for the first growing season. Seedlings grown in mixed substrates with higher sediment concentrations occasionally showed better photosynthetic capacity with improved connectivity between the units of the photosystem II. At the end of the first growing season, height as well as the number of growth flushes of the seedlings grown in sole sediment or soil-sediment substrates were similar to what generally is observed for forest nursery stock of Quercus spp.. Regarding the rootsystem articulation and growth in depth, results in the mixed substrates were comparable to those for seedlings grown in the traditional forest nursery media, and higher than seedlings grown in 100% agronomic soil. According to our results, the reclamation of dredged sediments can provide appropriate nursery substrate for germination beds for forestry species. © 2018 Elsevier Ltd. All rights reserved.

Keywords: Holm oak Mediterranean ecosystem Morphological traits Nursery substrate Physiological responses Remediated sediments

1. Introduction Sediments deposited in harbours and waterways interfere with

* Corresponding author. Istituto di Biometeorologia e Consiglio Nazionale delle Ricerche, Italy. E-mail address: [email protected] (F. Ugolini). 1 Co-first author. https://doi.org/10.1016/j.jenvman.2018.01.059 0301-4797/© 2018 Elsevier Ltd. All rights reserved.

navigational activities, so that dredging is necessary to maintain a sailing depth; however, they adsorb and retain the settled contaminants (including metals) and nutrients (such as N and P), with consequent environmental impacts and socio-economic issues (Manap and Voulvoulis, 2015). In Europe, the classification of dredging spoils, defined as the waste dredged out of canals, rivers, lakes and harbours to allow or facilitate the navigation of surface waters, follows the list of wastes adopted with Commission

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Decision 2000/532/EC, which also bases on the list of hazard wastes of the Directive 91/689/CEE, if the concentration of pollutants is above the set thresholds. Therefore, sediments with concentration of pollutants over the European (Commission Decision 2000/532/ EC) or the national law (DL 152/2006) thresholds must be dredged and then stocked in specific confined disposals and then brought to landfilling. Anyhow, in 2008, the European Commission has also introduced the principle of “recovering and recycling” (Directive 2008/98/CE), which allows a waste to cease to be waste and to become a secondary raw material, after all needed measures to ensure human health and environment safety (e.g., risk to water, air, soil, plants or animals, noise or odours, and to countryside or places of special interest). Indeed, dredged sediments that are not contaminated can be relocated farther offshore in deep-sea conditions or even reused in civil engineering works such as filling material to restore eroded beaches. On the other hand, the transportation to landfill even of slightly polluted materials generates high management costs and it increases soil and space consumption for disposals and landfilling. SedNet consortium (Salomons and Brils, 2004) reported that in Europe about 200∙106 m3 of sediments are produced every year, 65% of which contaminated by heavy metals and hydrocarbons. Therefore, the decontamination and transformation of such special waste into a valuable product would contribute reducing the environmental impact generated by dredging activities and creating ‘new products’ through the variety of treatments available nowadays (Netzband et al., 2002; Manap and Voulvoulis, 2015). For instance, previous experience on sediments dredged from a dredged canal in Tuscany (Navicelli, Pisa) demonstrated successful decontamination methodologies for the creation of agronomic substrates (Iannelli et al., 2010; Doni et al., 2013; Mattei et al., 2016, 2017). Nevertheless, the application of these decontaminated sediments in the agricultural sector remains poorly studied. Potentially, decontaminated sediments can be used in preparing planting stock for soil reclamation, functioning as initial substrate for hosting plants. Therefore, the suitability of decontaminated sediments as substrates needs to be tested in terms of plant adaptation to the physical and chemical characteristics of these substrates in varying proportions. In agriculture, one of the most consuming and demanding sector for natural resources is plant nursery that requires large volumes of soils for in-field plantations or of light substrates for inpot cultivations, which are currently mostly represented by peat (29 million cubic meters produced worldwide for this sector (Apodaca, 2015)). In this frame, it is recommendable the use of alternative substrates that guarantee quality products and as less as possible use of primary resources. Since the use of peat as plant growing substrate is no longer sustainable (Lazzerini et al., 2016), alternative plant growth media need to be tested, including contaminated biosolids (e.g., Sebastiani et al., 2004; Tognetti et al., 2004), in order to reduce the overexploitation of peatlands. Variable results for woody plants grown on dredged sediments were previously reported (Vervaeke et al., 2003; Hartley et al., 2011). Indeed, although soil quality was generally enhanced, the risk of trace element transfer to the wider environment is still a matter of debate. Nevertheless, the potential use of sediments in this sector is under-investigated, especially in consideration of the variety of cultivation typologies, substrate mixtures and plant stages (e.g., in containers or in field, for bare-root or rootball productions, seeding, transplanting, etc.). Phytotechnologies were proven useful for remediating dredged marine sediments (Bert et al., 2009), and offered efficient solutions for the degradation of organic pollutants and chemical stabilization of heavy metals in dredged sediments (Doni et al., 2015). In a pilot phytoremediation experiment on silty saline sediments

contaminated by heavy metals and organic compounds, Masciandaro et al. (2014) obtained positive indication on plant efficiency in remediating and ameliorating agronomic and functional sediment properties. Mattei et al. (2017) evaluated the potential of a phytoremediated sediment, dredged from maritime port, as peatfree growth substrate for ornamental plants and Cleansed Consortium (2016) tested the potential of phytoremediated sediments for growing ornamental shrubs, finding that the re-use by plant nursery industry can be a sustainable management solution for sediments dredged from a canal though operational limits due to the heterogeneous size of the clay aggregates. In this study, we used the same decontaminated sediments previously tested in Ugolini et al. (2017), though improved in structure homogeneity by breaking mechanically big aggregates and sieving the material. The new substrates were obtained by mixing the decontaminated sediments to agricultural soil in different percentage per volume and they were compared to a traditional nursery substrate (peat:perlite, 50:50) in order to evaluate their suitability as growth substrates for forest tree species, from the germination stage. The studied species was holm oak (Quercus ilex L.), which is the dominant tree of many mature forest communities over large areas of the Mediterranean Basin and represents the degradation sequences of Mediterranean-type climax vegetation (Tomaselli, 1977; Le Houerou, 1993). Holm oak is of high functional value to the overall ecological complexity of Mediterranean ecosystems (Tognetti et al., 1998), to the extent that even restoration of degraded lands in such ecosystems take the species into account (Papadimitriou, 2013). In parallel, it is widely used in urban settings due to its symbolic and landscape value as well as to its ecological and genetic adaptability. Morphological and physiological traits of holm oak seedlings were monitored throughout the first growth season in nursery conditions. The hypothesis under investigation was that the adaptive traits to soil nutrients are expressed by holm oak seedlings in relation to their concentration in the substrates. The objective was to ascertain that the application of dredged sediments to the growth substrate does not impair plant development in holm oak seedlings and, thus, may be potentially used to complement traditional substrates in nursery cultivation, eventually. 2. Material and methods 2.1. Study site, seed characteristics and nursery cultivation The experiment was carried out at the nursery of the Department of Agricultural, Food and Forestry Systems of the University of Florence (Italy, Lat. 43
480 30.5300 N; Long. 11
120 01.4600 E) during 2015 growing season. The climate is mild Mediterranean, with an annual mean temperature 14.9
C (max 20.5
C, min 9.3
C) and 861 mm annual rainfall; the dry season occurs from the beginning of June to the end of July. Details on environmental conditions of the study site can be found in Cambi et al. (2017). Weather parameters relative to the period of the experiment were taken from the closest meteorological station in Cascine (Firenze, Lat. N. 43
510100, Long. E. 11
1401300 , 40 m a.s.l.) equipped with a TEKNA data acquisition system (TEKNA, Firenze, IT) and sensors for the main weather parameters. The seeds were collected in October 2014 in an autochthonous holm oak stand (according to 1999/105/CE) approved for seed production in Migliarino San Rossore Regional Park (Tuscany, Italy, Lat. 43
430 1000 N, Long. 10
180 2500 E). Seeds were stored in refrigerator at 3
C in moist sand, during winter 2014e2015. In midMarch 2015, the acorns were placed in wet sand at 18
C and, after a week of pre-germination, 120 randomly selected acorns with radicles <5-mm long were sowed. This procedure was carried out to

F. Ugolini et al. / Journal of Environmental Management 211 (2018) 269e277

ensure that only the viable acorns were sown. 2.2. Substrates and experimental design In March 2015, 120 white plastic containers, 20 cm wide and 40 cm deep, were set up and filled with the substrates. The tested substrates consisted of four different mixtures of decontaminated sediments and agronomic soil compared to a traditional forest nursery substrate, considered as control. The sediments were dredged from Navicelli canal (Pisa, Italy) and decontaminated through a phyto-decontamination process using the Agriport and CleanSed methodologies (Doni et al., 2013; Masciandaro et al., 2015), which lowered total petroleum hydrocarbons and heavy metal concentrations to values below the legal limits for urban greening in industrial areas (Dlgs. 152/2006, D.M. 161/2012 and Dlgs. 217/2006). Agronomic soil was collected in Pistoia alluvial valley (Tuscany). Therefore, the treatments were five: a) decontaminated sediments at 100% (100%SED), b) decontaminated sediments 66% and 33% agronomic soil by volume (66%SED), c) decontaminated sediments 33% and 66% agronomic soil by volume (33%SED), d) 100% agronomic soil (100%SOIL) and e) Klasmann-Deilmann Select® Special mixture as fertilized nursery substrate which is a peat:vermiculite (50:50), considered traditional substrate (100%TS). Before filling the containers, each substrate or mixture was sieved using a net of 20 mm grid to sift the bigger skeleton. The experimental design consisted of four randomized blocks with 6 replicates (containers) for each treatment (24 replicates per treatment, 120 containers in total). Three additional replicates per treatment were also kept for an initial substrate characterization. In the nursery, the containers were placed at 5 cm distance from each other within the blocks, in order to avoid any disturbance and shading differences among seedlings; 1 m was the distance among the blocks. Top dressing fertilization (Nutricote Plus 16N-11P-10Kþ2MgO) was added to the traditional substrate (20 g/plant) at the beginning of the experiment as done traditional practice in nursery productions. No fertilization was added to the substrates during cultivation. Seedlings were irrigated to maintain the substrates moist in the range 20e30% in all substrates, and soil moisture was monitored regularly using a soil moisture sensor (PCE-SMM1, PCE Instruments). 2.3. Substrate analysis For the physical and chemical analysis, a composite sample of soil mixtures was taken at the beginning of the experiment and dried at ambient air. The particle size distribution (except for TS) was analysed using the pipette procedure (Indorante et al., 1990). Bulk density was measured by taking three samples of 10 cm3 per treatment from the upper 10 cm of unsown pots, recording the dry mass of the substrate by volume after drying at 70
C for 72 h. For the initial chemical analysis, the samples were sent to the Ionomics Service of the CEBAS-CSIC (Murcia, Spain). The pH and electrical conductivity (EC) were measured in deionized water (1:2.5 and 1:5 w/v, respectively) by selective electrode. Total macro and micro elements determination was done in samples digested using a high-performance microwave reaction with HNO3:H2O2 (4:1 V/V e Ultraclave, Milestone, Shelton, CT, USA) and then analysed with inductively coupled plasma-optical emission spectrometry (ICP-OES), in a Thermo ICAP 6000SERIES model. Water soluble elements were measured by ICP-OES from aqueous extracts (soil-water, ratio of 1:10) after shaking for 4 h followed by filtration. Carbon and nitrogen content were determined using a Flash 1112 series EA carbon/nitrogen analyser.

271

For the analysis of inorganic anions fluorides (F), Chlorides 3 (Cl), Nitrates (NO 3 ) and Phosphates (PO4 ), samples were weighted and diluted in deionized water, centrifuged for 30 min and decanted. The solution was filtered prior to analysis and anions were determined by ionic chromatography using a DIONEX chromatograph. The average from three instrumental readings are reported for the analysed elements as characterization of the substrates. 2.4. Emergence and growth monitoring At young stage, holm oak is a shade tolerant species, therefore, a shading mesh was used to protect the plants from full sun during nursery cultivation. Seedlings were monitored weekly since sowing. Height (H) and growth flushes (GF) were measured weekly from April 13 to October 16 and the last data collection by destructive sampling was made November 2. 2.5. Physiological measurements 2.5.1. Leaf water potential The plant water status was assessed through the measurement of leaf water potential, using a pressure chamber (PMS, Co. Corvallis, OR, USA). The measurement was taken when the plants were big enough not to affect growth. Pre-dawn (Jp, at 4e5 a.m.) and minimum (Jm, at 1e2 p.m.) water potentials were measured on July 27 and September 2, generally taking the 5th or 6th leaf from the stem apex. One leaf was detached from one plant per block (for a total of four fully expanded leaves per treatment), and readings were made immediately after detaching. 2.5.2. Leaf gas exchange Leaf gas exchange (photosynthesis - Pn, transpiration e Tr, and stomatal conductance - gs) was measured on 8 fully expanded leaves (two plants per block) in each substrate, using a CIRAS-1 Infrared Gas Analyser (PPSystem, Hitchin, UK). The measurements were taken at 10e11 a.m., before irrigation (May 26, June 22, July 16 and 28, August 11, September 10), with PAR (photosynthetically active radiation) > 1000 mmol m2 s1. Instantaneous water use efficiency (WUE) was then calculated as the ratio between Pn and Tr. 2.5.3. Chlorophyll a fluorescence Chlorophyll (Chl) a fluorescence was measured with a PEA (Plant Efficiency Analyser, Hansatech, Instruments Ltd., King's Lynn, UK) on a sample of 16 fully expanded leaves per substrate (four clips per block) at 10e11 a.m., before irrigation (May 25, July 16 and September 10). Leaves were dark-adapted for 25 min with leaf clips, and direct fluorescence was then detected during 5 s of exposure to actinic light. Data were downloaded using the Winpea 32 software (v.1.00, Hansatech, Instruments Ltd., King's Lynn, UK) and processed in a Biolyzer 3.0 (JIP-Test Analysis Program v.3.0, Laboratory of Bioenergetics, University of Geneva). The rising fluorescence transients were induced by red light (peak at 650 nm) of 3000 mmol photons m2 s1 provided by an array of six light emitting diodes; they were recorded for 1 s, starting from 50 ms after the onset of illumination, with 12-bit resolution. The fluorescence induction curve from F0 to Fm in dark-adapted samples is known as the “fluorescence transient” and its analysis is formalized in the JIP-test (Strasser et al., 2000, 2004). The different steps of this polyphasic transient are labelled as: O (50 ms, in the JIP-test, represents F0 i.e. initial fluorescence), J (2 ms), I (30 ms) and P (peak, or Fm i.e. maximum fluorescence). To assess the photosystem efficiency, the following

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parameters were then calculated:

3. Results

1. Fv/Fm (FPO) or maximum quantum yield of PSII primary photochemistry, which expresses the probability that an absorbed photon will be trapped by the PSII reaction centre (initial phase of the electron transport chain); 2. Jo, which expresses the probability that a photon trapped by the PSII reaction centre enters the electron transport chain; 3. I-P phase (DVI-P) (Oukarroum et al., 2009), which indicates the amplitude of the I-P phase, i.e. the efficiency of electron transport around PSI to reduce the final acceptors of the electron transport chain (i.e. ferredoxin and NADP) and then brought to the carboxylation; 4. Performance Index (PIABS), which is the performance index for energy conservation of photons absorbed by PSII, through the electron transport chain, from PSII to PSI; 5. Band L and K, which represent peaks at approximately 150 and 300 ms (Oukarroum et al., 2012).

3.1. Weather conditions

Comparisons between substrates were made, and then the parameters were relativized (i.e., expressed as treated/control ratio).

2.6. Morphological traits In November 2, the seedlings were harvested. The plants were accurately treated in order to preserve fine roots; they were extracted, washed and immediately measured. Morphological attributes of the root and the shoot system were analysed and included: leaf area, root collar diameter (RcD), main root (MR) length, and dry biomass of leaves, stem, branches and of the total shoot system. The root system dry mass was measured separating the main root (MR) from the first order lateral roots (FOLR) and both were weighted dividing the root system in depth sections: 0e20 cm and 21e40 cm. FORL were separated according to insertion depth. The dry mass (DW) was obtained placing the samples in paper bags and drying at 70
C until reaching a constant dry weight. H/Rcd, shoot/root system and FOLR/root system ratios were also calculated. The leaf area was measured using Model Li-3000 leaf area meter (Lincoln, Nebraska, USA).

Spring 2015 recorded about 20% more rainfall than the longterm climatic average, with March particularly rainy (84 vs. 59 mm). In contrast, from May to July the weather was particularly dry with 36% less rainfall. Additionally, July recorded exceptionally high minimum temperatures (27.3
C), 9
C higher than the climate average. Hence, also mean temperature (28.2
C) was higher (~3
C) than the average. August was wetter than usual, with 118.6 mm of rain (vs. 50 mm of the climate average).

3.2. Substrate analysis According to the USDA classification, the agronomic soil (100% SOIL) was loamy soil, whilst the sole sediment (100%SED) was sandy loam. The mixed substrates with phytoremediated sediments and agronomic soil (33%SED, 66%SED) were also characterized by a sandy loam texture, with intermediate clay content and higher sand content, resulting from the former treatment of the dredged sediments. All substrates were slightly alkaline with pH ranging from 7.5 in 100%SOIL to 7.8 in 100%SED, likely due to the presence of soluble Ca ions in the phytoremediated sediments, whilst the traditional substrate was neutral (pH 6.75). EC increased with phytoremediated sediment content in the substrate (Table 1). The mixed substrates seemed to have higher total nitrogen content, organic carbon compared to 100%SOIL, but also higher content of macronutrients, like K, P, and S, compared to 100%SOIL or 100%TS (Table 2). Microelements, like B, Cu, Fe, Mn, Mo, Ni, Se, and Z, were present at higher concentrations in the pure phytoremediated sediments, and they were also more soluble - with the exception of Fe -, in the pure sediments compared to other substrates (Table 2). Toxic elements, like Cd, Cr, and Pb, were not detected in the soluble solution, though the total amount of Cr and Cd in the soil was close to the law set threshold (DL 152/2006) in 66%SED and 100%SED (Table 2).

2.7. Statistical analysis

3.3. Emergence and growth monitoring

The statistical analysis was carried out using Statistica (Release 12, StatSoft, Inc. 1984e2014). Sample normality for the chemical properties of the substrates, leaf gas exchange, Chl a fluorescence parameters, plant biomass and growth parameters was tested using the Shapiro-Wilk test. ANOVA followed by Tukey's test for post-hoc comparison of means was then performed for identifying the statistical differences between the substrates. Statistical differences between two samples (e.g., water potentials in two dates) were performed using the T-test for independent samples analysis. Morphological traits were analysed by Multifactorial ANOVA and Tukey's test for post-hoc comparison considering as source of variation blocks and treatments. Ratios were transformed using arcsin square transformation. Chi square (c2) test was performed to evaluate emergence (comparing occurrence frequency) and survival, both among treatments and among blocks. Data on emergence were collected until the May 4, survival was evaluated at the end of the experiment.

According to c2 results, treatments and blocks did not have a significant effect on the emergence of seedlings; the same test on survival resulted significant (c2 among treatments ¼ 16.0, p < 0.01; among blocks ¼ 1.36 n.s.) and distinguished the following groups: A) 66%SED 100%TS; B) 100%TS and 100%SED both 95.8%; C) 33%SED and 100%SOIL 70.1% and 75.0%, respectively. Growth during the vegetative season (Fig. 1) did not evidence great variability between treatments of holm oak development, with the exception of a few dates in which 100%SED enhanced the growth of seedlings, especially compared to 100%SOIL. However, at the end of the season, no statistical differences among treatments or blocks occurred (p between treatments 0.823; p between blocks ¼ 0.974), even though seedlings in 66%SED and 100%SED showed the highest value. At the end of the experiment, all treatments did not show significant differences in the number of growth flushes (Table 4), even though a higher number of flushes (n > 4) was observed in the seedlings grown in 100%SED or in soilsediment combinations than in 100%TS and 100%SOIL (n < 4).

F. Ugolini et al. / Journal of Environmental Management 211 (2018) 269e277

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Table 1 Physical and chemical characteristics of the substrates. Values are instrument average from a composite mixed sample.

Clay: Silt: Sand Bulk density (g/cm3) Vol. Relative Water Content at field capacity (%) pH EC (mS/cm) Total C (g/100 g) Total N (g/100 g) TOC (g/100 g) CEC Fluorides (mg/L) Chlorides (mg/L) Nitrates (mg/L) Phosphates (mg/L)

100%SOIL

33%SED

66%SED

100%SED

100%TS

18.2: 33.4: 48.3 1.3 48.2 7.5 101.9 1.49 0.14 1.46 322.0 3,3555 11,045 23,8865 <0,5

11.6: 34.7: 53.7 1.25 48.6 7.5 157.2 2.29 0.20 1.62 517.5 5311 11,626 25,3185 <0,5

11.2: 32.7: 56.1 1.15 41.1 7.6 261.0 2.98 0.26 1.74 552.0 4936 9,3295 19,632 <0,5

8.3: 33.8: 57.9 1.05 40.4 7.7 248.0 3.76 0.29 1.91 770.5 3,7625 39,067 1976,644 <0,5

e 0.09 31.1 6.75 185.5 12.71 0.28 12.70 310.5 1,4715 17,104 11,2895 <0,5

Table 2 Total and soluble elements in the five substrates (mg of element per kg of dry soil). Values are instrument average from a composite mixed sample. 100%SOIL

Ca K Mg P S B Cu Fe Mn Mo Na Zn Al Cd Cr Pb

33%SED

66%SED

100%SED

100%TS

(mg/kg)

(mL/L)

(mg/kg)

(mL/L)

(mg/kg)

(mL/L)

(mg/kg)

(mL/L)

(mg/kg)

(mL/L)

10400 8400 9700 400 300 14.98 43.04 24000 621 0.56 500 67.25 32700 0.53 97.84 30.18

70.06 154.80 5.38 0.10 7.64 0.05 0.01 1.06 0.03 <0.01 8.47 0.01 0.19 <0.01 <0.01 <0.01

21700 9700 1000 500 1500 22.95 51.7 25600 582.2 2.13 500 162.38 36400 5.59 133.02 42.48

21.18 6.87 1.81 0.38 8.23 0.06 0.03 0.12 0.03 0.03 7.08 0.01 1.34 <0.01 <0.01 <0.01

35800 9500 1070 500 1900 24.38 54.83 25900 591.23 2.9 600 205.67 36900 8.71 150.44 51.38

38.28 7.58 2.78 0.23 25.03 0.07 0.02 0.33 0.02 0.04 8.7 0.01 0.49 <0.01 <0.01 <0.01

39700 1060 1100 700 4200 32.89 65.29 31100 1342.8 4.97 600 323.54 41900 14.46 235.22 67.53

603.60 23.28 26.47 0.28 369.00 0.14 0.08 0.01 0.3 0.12 11.07 0.01 0.1 <0.01 <0.01 <0.01

6000 700 800 100 400 2.82 6.76 500 30.1 2.56 1700 5.61 500 0.09 8.6 2.83

18.51 6.63 3.66 0.37 5.93 0.08 0.01 0.32 0.04 0.15 12.37 0.02 0.53 <0.01 <0.01 <0.01

Fig. 1. Growth curve of the holm oak seedling in the treatments (DOY: day of year). *Anova test results p < 0.05. 100%SED represents pure phytoremediated sediments; 66%SED is the substrate with 66% phytoremediated sediments and 33% agricultural soil; 33%SED is the substrate with 33% phytoremediated sediments and 66% agricultural soil, 100%SOIL represents the agricultural soil, 100%TS is the traditional substrate (50 peat: 50 vermiculite).

3.4. Physiological measurements 3.4.1. Leaf water potentials Jp ranged between 0.25 and 0.5 MPa in July, with no

differences between the substrates (Fig. 2). In September, Jp ranged between 0.14 and 0.4 MPa, with significantly lower values in 100%TS than in 100%SOIL (Fig. 2), in which holm oak showed also a significant recovery in Jp, between July and

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Fig. 2. Pre-dawn (Jp) and minimum (Jmin) water potentials in holm oak growing on the five substrates at mid (20 July) and at the end of the summer (2 September) 2015. Mean values and standard deviations are shown for the substrates. Significant differences between the substrates (Tukey test at P < 0.05) are shown by letters in each date of measurement (N ¼ 4 per sample), whilst the significant differences (T-test for independent samples) between dates within the same substrate are shown by * at P < 0.05.

September. Jmin did not change between the dates in all substrates (Fig. 2), ranging between 0.76 and 2.6 MPa, in July, and between 1 and 2.1 MPa, in September. No differences were observed between the substrates in July, whilst in September, in the traditional substrate (100%TS), values were significantly lower than in 33%SED, and intermediate values were recorded in the other treatments. DJ, representing the difference between Jp and Jmin, was similar in the five substrates.

3.4.2. Leaf gas exchange Holm oak seedlings showed high variability within treatments, with significant differences between them observed only in a few dates (Fig. 3). On June 10 and July 16, Pn was higher in 66%SED, especially in comparison with 100%TS. On the other hand, on June

10, transpiration was relatively high in 66%SED and in 100%TS, evidencing the best and the worst water use efficiency respectively. On July 29, Pn and Tr were higher in 100%SED, though no differences in WUE were observed between treatments. Afterwards, no differences between the treatments were found. In general, in all treatments, there was an increasing trend of Pn and Tr until the beginning of July, when growth conditions were optimal, whilst WUE reached the minimum values in mid July.

3.4.3. Chlorophyll a fluorescence Chlorophyll a fluorescence was measured on three representative dates (late spring; mid summer; late summer; Table 3). In late spring, the plants growing on 100%TS showed lower F0 values in comparison with those on other substrates, indicating a better energy transfer between the light harvesting system and the

Fig. 3. The graphs represent the mean values and standard deviations of leaf transpiration - Tr (A); stomatal conductance e gs (B); net photosynthesis e Pn (C) and water use efficiency e WUE (D) in holm oak seedlings during the experiment. Significant differences (Tukey test at P < 0.05 for unequal samples) between the five substrates (100%SED, 66% SED, 33%SED, 100%SOIL, 100%TS) are shown by letters in each date of measurement (N~8 in each substrate).

F. Ugolini et al. / Journal of Environmental Management 211 (2018) 269e277 Table 3 Parameters of direct fluorescence analysis. Fm (maximum fluorescence); F0 (initial fluorescence); Band L and K; ФPO (maximum quantum yield of primary photochemistry of a dark-adapted leaf; Jo (probability that a photon trapped by the PSII reaction centre enters the electron transport chain); DVIP (probability with which a PSII trapped electron is transferred until PSI acceptors); PIABS (performance index for energy conservation from photons absorbed by PSII to the reduction of intersystem electron acceptors). Mean values and standard deviations are shown with significant differences between substrates marked by letters, identified by Tukey test at P < 0.05 for equal samples. Parameter

Thesis

26/05/2015

16/07/2015

10/09/2015

Fm

100%SOIL 100%SED 66%SED 33%SED 100%TS 100%SOIL 100%SED 66%SED 33%SED 100%TS 100%SOIL 100%SED 66%SED 33%SED 100%TS 100%SOIL 100%SED 66%SED 33%SED 100%TS 100%SOIL 100%SED 66%SED 33%SED 100%TS 100%SOIL 100%SED 66%SED 33%SED 100%TS 100%SOIL 100%SED 66%SED 33%SED 100%TS 100%SOIL 100%SED 66%SED 33%SED 100%TS

2114 ± 372 2148 ± 141 2098 ± 188 2116 ± 133 1991 ± 46 547 ± 64 ab 541 ± 38 ab 604 ± 61 a 590 ± 85 ab 510 ± 25 b 0.06 ± 0.01 0.05 ± 0.01 0.06 ± 0.01 0.06 ± 0.01 0.05 ± 0.01 2.5 ± 0.2 ab 2.7 ± 0.2 a 2.4 ± 0.2 ab 2.4 ± 0.4 b 2.6 ± 0.1 ab 0.28 ± 0.05 0.29 ± 0.04 0.27 ± 0.04 0.30 ± 0.06 0.31 ± 0.02 0.74 ± 0.03 0.75 ± 0.02 0.71 ± 0.02 0.72 ± 0.05 0.74 ± 0.01 0.57 ± 0.09 0.57 ± 0.07 0.49 ± 0.09 0.52 ± 0.14 0.59 ± 0.06 21.0 ± 10.3 23.7 ± 8.1 12.5 ± 5.0 18.4 ± 12.7 23.0 ± 8.5

1911 ± 164 ab 1963 ± 160 ab 2048 ± 192 a 1882 ± 195 ab 1829 ± 242 b 510 ± 63 498 ± 70 504 ± 75 523 ± 87 468 ± 47 0.05 ± 0.006 a 0.04 ± 0.007 ab 0.04 ± 0.007 b 0.04 ± 0.009 ab 0.05 ± 0.007 ab 2.4 ± 0.3 2.7 ± 0.3 2.6 ± 0.3 2.5 ± 0.4 2.5 ± 0.3 0.36 ± 0.04 ab 0.33 ± 0.04 b 0.35 ± 0.04 ab 0.39 ± 0.06 a 0.36 ± 0.06 ab 0.73 ± 0.06 0.74 ± 0.05 0.75 ± 0.04 0.72 ± 0.07 0.74 ± 0.06 0.6 ± 0.05 b 0.63 ± 0.08 ab 0.69 ± 0.05 a 0.64 ± 0.08 ab 0.61 ± 0.11 ab 23.1 ± 11.5 33.5 ± 18 40 ± 14.8 28 ± 20 29.1 ± 15.4

2069 ± 239 a 1860 ± 380 ab 1911 ± 234 ab 1714 ± 309 b 1955 ± 223 ab 495 ± 30 517 ± 57 519 ± 44 488 ± 63 501 ± 42 0.044 ± 0.01 ab 0.041 ± 0.01 ab 0.040 ± 0.01 ab 0.040 ± 0.01 b 0.048 ± 0.01 a 2.8 ± 0.24 2.7 ± 0.22 2.8 ± 0.16 2.7 ± 0.27 2.6 ± 0.18 0.32 ± 0.04 0.29 ± 0.05 0.31 ± 0.05 0.31 ± 0.04 0.29 ± 0.04 0.76 ± 0.02 0.71 ± 0.09 0.72 ± 0.04 0.71 ± 0.04 0.74 ± 0.03 0.65 ± 0.05 0.61 ± 0.12 0.65 ± 0.05 0.64 ± 0.07 0.62 ± 0.07 35.8 ± 9.7 27.2 ± 18.2 29 ± 12 26.7 ± 13.7 27.7 ± 12.4

F0

Band L

Band K

DVIP

ФPO

Jo

PIabs

reaction centre. In mid summer (July 16), with high temperatures and following a relatively dry period, the best performance was observed in 66% SED. Fm recorded the highest values, the Band L was less pronounced (indicating better connectivity between the units of PSII) and Jo (probability that a trapped exciton moves an electron further than Q A ) was also higher than in other substrates. However, PIabs was not affected by the substrate. In September, significant differences were found only for Fm (that recorded the highest values in 100%SOIL and the lowest in 33% SED), and band L with lowest values in 33%SED and highest in 100% TS. 3.5. Morphological traits Results of ANOVA on morphological attributes are shown in Table 4. Above-ground traits did not differ between treatments. Differences occurred in below-ground characteristics. The seedlings grown in 100%SOIL developed a shorter tap-root, at least 29.3% (about 14 cm), than the mean length of the main root

275

in other treatments. Statistical differences between treatments were also observed for the biomass of first order lateral roots (FOLR). Seedlings grown in 100%SED showed higher FOLR biomass (total and in the first depth section 0e20 cm) than plants grown in 33%SED. Higher main root biomass development in the deeper part of the container occurred in the nursery 100%TS. The seedlings grown in all treatments revealed a general absence of root articulation in the deepest part of the container. Shoot/root system ratio was significantly higher in seedlings grown in 33%SED and lower in plants grown in 100%TS; an opposite result occurred in the ratio between FORL and root system biomass. 4. Discussion The focus of this study was on assessing the potential of phytoremediated sediments (mixed with agronomic soil or alone) for being used as substrate to grow forest tree seedlings in nursery conditions. The substrate with decontaminated sediments slightly improved the germination capacity of the holm oak acorns. After one growing season, the growth of seedlings in the sediment mixtures was comparable to that of seedlings grown in the traditional nursery substrate. Seedlings grown in the sediment mixtures showed even better performance than those grown in the agronomic soil. The height of the seedlings grown in sediment or soilsediment substrates was comparable to that generally observed for Quercus spp. nursery stock grown in containers during the first growing season (e.g., Mariotti et al., 2015a, 2015b). Moreover, the number of growth flushes was copious, confirming the promising growth conditions in such sediments or mixtures. Indeed, Quercus spp. are generally characterized by multiple flushing, and the flush number is related to growth in favourable environmental conditions (Bobinac et al., 2012; Collet and Frochot, 1996). Only when seedlings were two months old, those growing in 100%SED grew taller than in other substrates, suggesting a fertilization effect by the sediments, even though the differences disappeared later on. Positive effects of growth substrate amended with biosolids of industrial origins (containing low to medium levels of heavy metals) on growth traits and physiological functions have been reported for other forest tree species (e.g., Sebastiani et al., 2004; Tognetti et al., 2004), most probably for the nutrients contained in the industrial waste. In the present case, phytoremediated sediments enriched the agronomic soil of micro and macro nutrients, also in the soluble form and increased the cation exchange capacity. The substrate pH was relatively higher than the range of the typical nursery substrate. Although the moderate alkalinity may limit the availability of some nutrients, it probably prevented the availability of toxic heavy metals, like Cd and Cr, and Pb, which were not detected in the soluble form, even though their total concentration was close to the national law set threshold (DL 152/2006). Nevertheless, substrate pH may deviate from alkaline upon medium acidification with time, which warrants long-term experiment to prolong plant exposure to dredged sediments (Mattei et al., 2017). Yet, heavy metals can be compartmented and immobilized, reducing the risk of phytotoxic effects on major physiological processes (Tognetti et al., 2004; Cocozza et al., 2008, 2014; Di Baccio et al., 2011, 2014). The physiological measurements, investigating the acclimation response to environmental conditions, showed minor differences between treatments, due to the variability within samples. Concerning the minimum leaf water potential, seedlings in the traditional substrate recorded in general the lowest values, averaging 1.8/-2 MPa, and again great variability was observed in other treatments. The traditional substrate tended to dry quickly, likely lowering the leaf water potential as the water evapotranspired. Physiological measurements further support the hypothesis that the application of decontaminated dredged

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Table 4 Results of multifactorial ANOVA test and Tukey's post hoc for the morphological attributes of seedlings after the destructive analysis (mean values ± standard deviation, homogeneous groups at P < 0.005, P values). Abbreviations mean: main root (MR), root collar diameter (RcD), plant height (H), first order lateral roots (FOLR), dry weight (DW); 0e20 and 20e40 are the two depth section used to analyze root-system traits.

H (cm) RcD (mm) H/RcD GF (n) MR length (cm) MR DW 0e20 (g) MR DW 21e40 (g) MR DW tot (g) FOLR 0e20 (g) FOLR 21e40 (g) FORL DW tot (g) Root system DW (g) Stem DW (g) Branches DW (g) Shoot system DW (g) Leaves DW (g) Shoot system þ leaves DW (g) Leaf area (cm2) Shoot/root system DW FOLR/root system DW

100%SOIL

33%SED

66%SED

100%SED

100%TS

P

21.0 ± 15.0 5.2 ± 1.9 37.2 ± 19.3 3.7 ± 1.4 33.3 ± 12.2 a 1.5 ± 1.0 0.1 ± 0.1 a 1.6 ± 1.1 0.4 ± 0.5 ab 0.0 ± 0.1 0.5 ± 0.5 ab 2.0 ± 1.4 1.2 ± 1.4 0.3 ± 0.3 1.6 ± 1.4 2.0 3.7 ± 3.5 158.8 ± 159.1 0.6 ± 0.3 ab 0.2 ab

21.9 ± 9.6 4.8 ± 1.5 45.8 ± 14.9 4.1 ± 0.7 47.1 ± 16.6 b 1.6 ± 1.5 0.2 ± 0.3 ab 1.9 ± 1.7 0.2 ± 0.3 a 0.1 ± 0.1 0.3 ± 0.3 a 2.2 ± 1.8 1.0 ± 0.9 0.3 ± 0.4 1.4 ± 1.1 1.9 ± 1.7 3.3 ± 2.8 134.4 ± 141.3 0.5 ± 0.2 b 0.2 ± 0.1 a

23.6 ± 10.6 5.3 ± 1.2 43.1 ± 12.1 4.1 ± 1.1 48.8 ± 12.9 b 1.50.9± 0.2 ± 0.2 ab 1.7 ± 1.0 0.5 ± 0.5 ab 0.1 ± 0.1 0.5 ± 0.5 ab 2.2 ± 1.3 1.1 ± 1.0 0.3 ± 0.2 1.4 ± 1.3 2.2 ± 1.4 3.6 ± 2.4 147.6 ± 109.0 0.6 ± 0.4 ab 0.2 ± 0.2 ab

23.4 ± 11.2 5.9 ± 1.5 39.3 ± 15.1 4.1 ± 1.0 50.7 ± 9.5 b 1.6 ± 0.9 0.3 ± 0.2 ab 1.9 ± 1.0 0.8 ± 0.6 b 0.1 ± 0.1 0.8 ± 0.6 b 2.7 ± 1.4 1.1 ± 0.9 0.3 ± 0.2 1.4 ± 1.3 2.3 ± 1.6 3.7 ± 2.4 142.3 ± 115.4 0.5 ± 0.1 ab 0.3 ± 0.1 ab

20.1 ± 8.5 5.0 ± 1.4 39.5 ± 11.2 3.6 ± 0.7 54.8 ± 12.5 b 1.5 ± 0.7 0.4 ± 0.3 b 1.8 ± 1.0 0.7 ± 0.7 ab 0.1 ± 0.1 0.8 ± 0.7 ab 2.5 ± 1.3 1.0 ± 0.6 0.2 ± 0.1 1.2 ± 1.1 1.8 ± 0.9 2.9 ± 1.5 127.8 ± 68.8 0.4 ± 0.1 a 0.3 ± 0.2 b

.8226 .2659 .4603 .3555 .0000 .9897 .0490 .9454 .0294 .5216 .0220 .5235 .9326 .7949 .8847 .7633 .7839 .9296 .0278 .0181

sediments to the growth substrate does not impair structures and functions of holm oak seedling. Leaf gas exchange did not reveal differences between the treatments, with the exception of a few dates, although, only on June 10, 100%TS showed the lowest water use efficiency. In 100% SED and 66%SED, holm oak seedlings showed relatively higher photosynthetic capacity, confirmed also by chlorophyll a fluorescence measurements. For instance, in mid-summer, when the conditions were hot and dry, improved photosynthetic performance was observed in 66%SED, with higher Fm and lower Band L, indicating better connectivity between the units of PSII. Similar results, in terms of plant growth and leaf physiology, were found by Ugolini et al. (2016a) in ornamental plants grown in sediments mixtures at 33% and 50% with alluvial soil without mechanical treatment. In this study, thanks to mechanical breakage and sieving, the decontaminated sediments provided also a more homogenous physical substrate for the development of the main and secondary roots, while ensuring water drainage. Final height and aerial biomass did not show differences between treatments. The presence of sediments in the growth media avoided the need of fertilization and it promoted the extension of the main root, as well as the traditional substrate. In fact, seedlings grew 40 cm more in depth, reaching the bottom of the containers, which were also deeper and larger than the types generally used for forest nursery stock (see Mariotti et al., 2015a, 2015b). This was most likely due to a combination of the loose structure, the homogeneous size of the aggregates, and the particle size distribution of the sediment-based substrates in comparison to 100%SOIL, which easily tends to compaction. Regarding the main root biomass, contrarily to what observed in a previous study (Ugolini et al., 2017), no dead roots were found in the looser the substrates (100%SED), which was likely due to the improved homogeneity of the growth media reducing excessive water drainage. Yet, 100%SED and 100%TS showed a greater amount of lateral roots, especially in the first 20 cm. The traditional substrate showed lower shoot to root ratio, indicating a greater allocation of biomass to roots, though the substrate with higher concentration of sediments and the sediments alone showed similar values. An increased partitioning of biomass to roots can be expected under higher nutrient availability due to sediment addition, at least to a certain extent. The lower compaction due to the presence of sediments

may also limit the phytoextraction of contaminants, decreasing the risk of excess uptake of toxic heavy metals (Wu et al., 2014). In addition, Mattei et al. (2017) found that sediment-based growing media increase the diversity of bacteria, fungi and archaea as compared to the untreated sediments, and that composted sediments with urban green waste had no substantial eco-toxicological impacts, allowing excellent plant growth performance. Cocozza et al. (2014) demonstrated that the integration of poplar plants and bacterial strains (isolated from compost and organic amendment) increases total removal of Cd, without interfering with plant growth, while improving the photosynthetic capacity. Sebastiani et al. (2004) and Tognetti et al. (2004) observed greater root biomass and assimilation rate in poplar plants developing in growth substrate amended with biosolids of industrial origins (containing heavy metals). 5. Conclusion The reclamation of dredged sediments, as component of plant nursery substrate, is proved a promising approach. The greater the concentration of decontaminated sediments in the substrate (66% SED, 100%SED) - without the need for fertilization - the better the seed germination and root growth, with excellent results also for shoot growth. These performances resembled those of seedlings grown in the traditional peat-based nursery substrate. In comparison with previous studies (Mattei et al., 2017; Ugolini et al., 2016b, 2017), the present study demonstrated the suitability of this multifunctional material in peat replacement, or as technosol, in order to shorten the distance between the production site and the final destination. In addition, this study evidenced the capacity of holm oak for developing and establishing in the tested mix of sediments and soil, opening the perspective of using remediated substrate for addressing land degradation processes, in particular due to the depletion of this species (i.e., the reduction in the numbers of forest stands and their health) in Mediterranean and Southern-European areas (Papadimitriou, 2012; Papadimitriou and Mairota, 1996). Further investigation may elucidate the performance of other tree species, as well as that of transplanted seedlings formerly grown in sediment-amended substrates, or directly sown in soil-sediment mixtures in long-term restoration projects.

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