The use of compost in afforestation of Mediterranean areas: Effects on soil properties and young...

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The use of compost in afforestation of Mediterranean areas: Effects on soil properties and young tree seedlings Marie Larchevêque, Christine Ballini , Nathalie Korboulewsky, Nicolas Montès Institut Méditerranéen d'Ecologie et de Paléoécologie UMR CNRS 6116 Université de Provence, Case 421, Faculté des Sciences et Techniques de St Jérôme, Avenue Escadrille Normandie Niemen, 13397 Marseille Cedex 20, France Received 6 February 2006; received in revised form 3 April 2006; accepted 3 April 2006 Abstract In Mediterranean frequently burnt areas, fire and erosion result in the decrease of soil fertility, so afforestation is a major concern. We carried out an in situ experiment of compost amendment to improve survival and growth of planted tree seedlings. One-year-tree seedlings of native species (Quercus ilex, Pinus halepensis and Pinus pinea) were planted on a frequently burnt calcareous site. Three rates of fresh co-composted sewage sludge and greenwastes (control without compost, 20 and 40 kg m 2 of compost) were incorporated into the soil at each seedling stem. Changes of soil properties and tree development were studied during 3 years (20012003) and 2 years (20022003) respectively. The compost improved survival of Quercus ilex and Pinus pinea seedlings in severe drought conditions, but had no effect on Pinus halepensis. For all species seedling length and radial growth and NPK nutrition were increased for both rates of amendment. Amendment improved soil fertility, but available P concentration increased 13 fold in the neighbouring soil of seedlings amended at the maximal rate compared to control. However, amendment did not significantly increase concentrations of Cd, Cr, Ni and Pb in soils or tree seedlings. It increased Cu and Zn total and available concentrations in soils, while foliar Cu and Zn concentrations in the seedlings remained similar in all plots. Compost can efficiently help afforestation of dry soils with low organic matter content. However, sewage sludge concentrations in P, and to a lesser extent in Cu and Zn, limit rates of application that can be applied without environmental hazard. © 2006 Elsevier B.V. All rights reserved. Keywords: Sewage sludge compost; Afforestation; Trace metals; Pinus halepensis; Pinus pinea; Quercus ilex 1. Introduction Soils in Mediterranean climates are undergoing degra- dation due to water erosion and recurrent fires (De Luis et al., 2001). The continual removal of weathered rock mate- rial has resulted in rather thin and infertile soils, which are often deficient in macronutrients (Archibold, 1995).There- fore, in Mediterranean frequently burnt areas, fire and erosion result in the loss of organic matter and nutrients, which decrease soil fertility. Post-fire vegetation is domi- nated by sclerophyllous shrubs or pioneer conifers, which are stress-tolerant species adapted to infertile habitats. Leaf traits of these species are thought in the long term to be responsible for maintaining low-nutrient levels of sites they colonize (Rundel, 1988; Aerts, 1995). On the contrary, broad-leaved tree species develop under higher nutrient and water levels, and are characteristics of mature stages of succession in the Mediterranean area. The regeneration of Science of the Total Environment xx (2006) xxx xxx + MODEL STOTEN-09417; No of Pages 11 www.elsevier.com/locate/scitotenv Corresponding author. Tel.: +33 491 288 874; fax: +33 491 288 707. E-mail address: [email protected] (C. Ballini). 0048-9697/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2006.04.017 ARTICLE IN PRESS

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ent xx (2006) xxx–xxx

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Science of the Total Environm

The use of compost in afforestation of Mediterranean areas:Effects on soil properties and young tree seedlings

Marie Larchevêque, Christine Ballini ⁎, Nathalie Korboulewsky, Nicolas Montès

Institut Méditerranéen d'Ecologie et de Paléoécologie UMR CNRS 6116 Université de Provence, Case 421, Faculté des Sciences et Techniques deSt Jérôme, Avenue Escadrille Normandie Niemen, 13397 Marseille Cedex 20, France

Received 6 February 2006; received in revised form 3 April 2006; accepted 3 April 2006

Abstract

In Mediterranean frequently burnt areas, fire and erosion result in the decrease of soil fertility, so afforestation is a major concern.Wecarried out an in situ experiment of compost amendment to improve survival and growth of planted tree seedlings. One-year-treeseedlings of native species (Quercus ilex, Pinus halepensis and Pinus pinea) were planted on a frequently burnt calcareous site. Threerates of fresh co-composted sewage sludge and greenwastes (control without compost, 20 and 40 kgm−2 of compost) were incorporatedinto the soil at each seedling stem. Changes of soil properties and tree development were studied during 3 years (2001–2003) and 2 years(2002–2003) respectively.

The compost improved survival of Quercus ilex and Pinus pinea seedlings in severe drought conditions, but had no effect on Pinushalepensis. For all species seedling length and radial growth andNPKnutritionwere increased for both rates of amendment. Amendmentimproved soil fertility, but available P concentration increased 13 fold in the neighbouring soil of seedlings amended at the maximal ratecompared to control. However, amendment did not significantly increase concentrations of Cd, Cr, Ni and Pb in soils or tree seedlings. ItincreasedCu and Zn total and available concentrations in soils, while foliar Cu andZn concentrations in the seedlings remained similar inall plots.

Compost can efficiently help afforestation of dry soils with low organic matter content. However, sewage sludge concentrations in P,and to a lesser extent in Cu and Zn, limit rates of application that can be applied without environmental hazard.© 2006 Elsevier B.V. All rights reserved.

Keywords: Sewage sludge compost; Afforestation; Trace metals; Pinus halepensis; Pinus pinea; Quercus ilex

1. Introduction

Soils in Mediterranean climates are undergoing degra-dation due to water erosion and recurrent fires (De Luis etal., 2001). The continual removal of weathered rock mate-rial has resulted in rather thin and infertile soils, which areoften deficient in macronutrients (Archibold, 1995).There-

⁎ Corresponding author. Tel.: +33 491 288 874; fax: +33 491 288707.

E-mail address: [email protected] (C. Ballini).

0048-9697/$ - see front matter © 2006 Elsevier B.V. All rights reserved.doi:10.1016/j.scitotenv.2006.04.017

fore, in Mediterranean frequently burnt areas, fire anderosion result in the loss of organic matter and nutrients,which decrease soil fertility. Post-fire vegetation is domi-nated by sclerophyllous shrubs or pioneer conifers, whichare stress-tolerant species adapted to infertile habitats. Leaftraits of these species are thought in the long term to beresponsible for maintaining low-nutrient levels of sites theycolonize (Rundel, 1988; Aerts, 1995). On the contrary,broad-leaved tree species develop under higher nutrient andwater levels, and are characteristics of mature stages ofsuccession in the Mediterranean area. The regeneration of

STOTEN-09417; No of Pages 11

Table 1Initial soil and compost characteristics, May 2001

Parameter Soil(fractionb2 mm)

Compost Increase (%)in soil fractionb2 mm,calculatedfor D20 rate

Density 1.4 (0.1)Clay (%) 28.2 (0.7)

Granulometry Silt (%) 50.0 (0.8)Sand (%) 12.4 (1.2)

Cation exchangecapacity (meq 100 g−1

DM)

20.9 (0.8)

Humidity (% FM) 34pHH20 7.96 (0.01) 7.70C/N 11.2 13.50Organic matter(% DM)

5.6 (0.2) 39.00 33

Total N (% DM) 0.29 (0.02) 0.69 11Total P (% DM) 0.03 (0.003) 0.59 94Available P(mg kg−1 DM)

15.2 (0. 66) 2515

Exchangeable/total K(% DM)

0.03 (0.0008) 0.22

Exchangeable/totalMg (% DM)

0.012 (0.0003) 0.17

Exchangeable/totalCa (% DM)

0.86 (0.014) 5.30

Cd (mg kg−1 DM) 0.33 (0.03) 0.77 11Cr (mg kg−1 DM) 50.7 (0.7) 21.9 2Cu (mg kg−1 DM) 18.7 (0.5) 122 31Hg (mg kg−1 DM) 0.06 (0.07) 0.88 70Ni (mg kg−1 DM) 42.7 (0.3) 14.7 2Pb (mg kg−1 DM) 35.2 (1.4) 65 9Zn (mg kg−1 DM) 67.4 (1.5) 266 19

Mean (SE), N=32 (except for total trace metal concentrations: N=10)DM: dry matter; FM: fresh matter. Exchangeable cation concentrationsin soil and total cation concentrations in compost.The trace elements were extracted in aqua regia.

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these broad-leaved trees can therefore be considerablydelayed in these post-fire stands, especially in the mostdegraded sites with very superficial soils. Improving soilfertility by organic amendments, such as biosolids, couldfavour the occurrence of broad-leaved tree species.

Sewage sludge is a source of organic matter and plantnutrients (Brockway, 1983; Martinez et al., 2003). Sprea-ding sewage sludge on natural or arable soils seems to be anattractive way to enhance soil potentialities and an alter-native to its landfill disposal (McKay and Moffat, 2001).However, recycling such biosolids presents potential envi-ronmental risks due to accumulation of heavymetal in soils(Brockway, 1983), as well as discharge of nutrients, espe-cially N and P, to surface and ground water (Martinez et al.,2003).

Sewage sludge composting stabilize the organic matterand thereby decrease risks of heavy metal and salt lea-ching (Garcia et al., 1990; Planquart et al., 1999). More-over, the use of other organic wastes with large C/N ratios(such as green wastes) in mixture with sewage sludge canreduce the rate of nitrogen mineralization and then de-creases the risk of leaching (McKay and Moffat, 2001)while providing durable release of available N to plants.

The use of composted biosolids as an amendment isincreasing for soil restoration and forest regeneration indegraded Mediterranean areas. Indeed, it has been shownthat such amendments increase soil fertility (Caravaca et al.,2002;Martinez et al., 2003), plant biomass (Guerrero et al.,2001; Moreno-Peñaranda et al., 2004), plant nutrition(Moreno et al., 1996) and plant cover (Larchevêque et al.,2005). However, these studies were carried out on post-firevegetation (matorral), but there are few in situ studies onMediterranean trees. Biosolids could be amended on burntsites to improve plantation success of broad-leaved treessuch as evergreenQuercus species which have resproutingcapabilities and are less combustible than sclerophyllousshrubs or conifers. These properties are of major interest inafforestation programmes for the prevention of fire effects.

We carried out a research study to monitor effects of asewage sludge compost applied on a plantation of Medi-terranean tree seedlings over a three year period. Our aimswere to (i) determine effects of compost application on soilfertility; (ii) evaluate seedling survival, growth and nutrientstatus; (iii) evaluate trace metal contamination of soil andseedlings.

2. Material and methods

2.1. Site description

The experiment was carried out on a 3-ha site on theplateau of Arbois in the vicinity of Marseille (South Pro-

vence, France), at 240mabove sea level (5°18′6″E–43°29′10″N in WSG-84 Geodetic system). The silty–clayeychalky soil is a Rendzic Leptosol according to FAO (1998),with a high percentage of stones (70%) and a low averagedepth (about 24 cm). The last fire occurred in June 1995and the sitewas colonized byMediterranean sclerophyllousshrubs, with a 70% total cover before tree planting.Quercus coccifera L. and Brachypodium retusum Pers.were the two dominant species. This natural vegetationrepresents the early successional stages of the holm oak(Quercus ilex L.) series. During the two years ofexperimentation (2002 and 2003), the mean air tem-peratures were respectively 14.1 °C and 14.3 °C, and thetotal annual rainfall 867 mm and 626 mm. The site wasstrongly exposed to harsh North–West winds increasingnatural drought. Before amendment, the soil had relatively

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high Cr, Ni and Pb concentrations (Table 1) (De Nicola etal., 2003; Hernandez et al., 2003) because of significantatmospheric pollution (AIRMARAIX, 1999).

2.2. Compost and experimental design

The six-month maturity compost was produced by alocal company (Biotechna, Ensuès, Provence, France)and was certified to conform to the NF U 44-095 (2002)on composts made from materials of water treatmentorigin. This compost was elaborated with greenwastes (1/3 volume), pine barks (1/3 volume), and local municipalsewage sludge (1/3 volume). The mixture was compostedfor 30 days at 75 °C to kill pathogenic microorganismsand decompose phytotoxic substances, and then sieved(b20-mmmesh) to remove large bark pieces and stored inswathes. The swathes were mixed several times in thenext 6 months to promote organic matter humification.The final compost met the French legal standards forpathogenic microorganisms, organic trace elements andheavymetals (Table 1; compost characteristics were givenby the company producing the compost).

The experimental design had two factor levels: com-post rate and seedling species. Three treatments wereapplied: control without compost (D0), 20 kg of freshcompost per seedling (D20) and 40 kg of fresh compostper seedling (D40), amended at the foot of each seedling.The site preparationwas as follows: first, the experimentalsite was divided in three 1-ha plots (a control plot and twoamended plots); in each plot, plantation lines spaced bythree meters were cleared of above-ground vegetation.Second, 1-m2 holes were dug on these plantation lines asdeeply as possible (given the low soil depth) each holecorresponding to one seedling and spaced by 4 m to thenext one. Ten contiguous sub-plots were then delimited ineach plot. Third, a unique compost amendment took placein May 2001. The compost was mechanically mixed withthe soil in each hole. The soil of the control (D0) wasmixed too. Given a density of plantation of about 400seedling ha−1, and compost locally amended at eachseedling foot, we globally spread 8 tons (D20) and 16 tons(D40) of fresh compost per hectare. Fourth, seven monthsafter the compost amendment (December 2001), 1-yearseedlings of 3 Mediterranean tree species were plantedwith their nursing soil: Q. ilex L., Pinus halepensisMill.,and Pinus pinea L. Each species was planted in a mini-mum of three randomly selected sub-plots per compostrate. Aminimumof one hundred seedlings of each specieswere planted per plot (per compost rate). Q. ilex waschosen because in calcareous Provence it is a dominanttree species in the mature stages of vegetation dynamics.The two pine species are fast-growing and stress-resistant,

and are therefore commonly planted for afforestation ofburnt areas. This allowed a comparison between speciesin response to compost amendment.

A 40×40 cm cellulose protection layer was laid on theground around each seedling stem to limit soil waterevaporation and interspecific competition with adventi-tious vegetation. A wire netting was placed around eachseedling to protect them from herbivory. Seedlings werewatered twice in August 2002 and 2003 to avoid exces-sive mortality due to drought.

2.3. Soil and plant sampling and analysis

Soil samples were collected before compost amend-ment (May 2001), at plantation time (December 2001),one year and a half (December 2002) and two years and ahalf after amendment (November 2003). For each dateand treatment, a minimum of 8 soil samples were collec-ted at the stem of seedlings. The soil was collected in thearea covered by the cellulose protection layer. All theaccessible soil down to bedrock was collected. The soilsamples were oven dried at 40 °C to constant weight andsieved through a 2 mm mesh before analysis. Severalphysico-chemical parameters were studied to determinethe effects of the amendment on soil fertility and environ-mental risks. Organic C was determined using sulphuric–chromic oxidation and spectrocolorimetry (NF ISO14235, AFNOR, 1999; Cary 50 VARIAN). Soil organicmatter concentration was calculated as 1.72×organic car-bon (C). Exchangeable potassium (K), calcium (Ca) andmagnesium (Mg) were extracted by a 1 M NH4Ac solu-tion, then analysed by atomic absorption spectrophotom-etry (NF X 31-108, AFNOR, 1999; FS220 VARIAN).Total nitrogen (N) was determined after dry combustionby thermic conductimetry (ISO 13878, AFNOR, 1999;FP 428 LECO). Total phosphorus (P) was measured ac-cording to NF EN ISO 11885 (VARIAN VISTA Radial),and available P was extracted with sodium hydrogeno-carbonate solution, then determined by spectrophotome-try (Olsen et al., 1954) (NF EN ISO 11263, AFNOR,1999; Cary 50VARIAN). Cu andZn available formswereextracted using EDTA and measured by atomic absorp-tion spectrophotometry (NF X 31-120, AFNOR, 1999;VARIAN VISTA Radial). To measure total concentra-tions of cadmium (Cd), chromium (Cr), copper (Cu),nickel (Ni), lead (Pb) and zinc (Zn), soil samples weredigested in aqua regia and analysed using plasma emis-sion spectrophotometry (NF EN ISO 11466, AFNOR,1999; VARIAN VISTA Axial).

Seedling survival and growth were measured oneyear (December 2002) and two years (November 2003)after planting. The annual length growth was measured

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as the difference between maximal seedling lengths atone year interval (December 2001–December 2002 andDecember 2002–November 2003). Likewise, the annualradial growth was calculated as the difference betweenseedling basal stem diameters at one year interval.Growth was then expressed in % for each one-yearperiod. Both length and diameter were measured on fiveseedlings per treatment and per species being fixed forall the experiment duration (except in case of seedlingdeath). For foliar chemical analyses (N, P, cations andtrace metals), three other seedlings per treatment andspecies were randomly sampled in December 2002 andNovember 2003 for analysis. Leaves and needles werewashed with demineralized water, oven dried at 40 °Cand grind with a trace metal free grinder (made withtungstene carbure, FOSS TECATOR Sample Mill 1093Cyclotec). For N, K, Ca and Mg analysis, 250 mg of

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Fig. 1. Soil properties before amendment (May 2001), seven months after am2002) and 2.5 years (November 2003) after amendment, for control (D0), 20(D40). Mean±SE (N=32 for May 2001; 8≤N≤14 for the other dates). ⋆p

sample were digested one night in 5 ml H2SO4 (96%)and 5 ml H2O2 (35%), then heated at 400 °C during 3 h(Bioblock Scientific Digestion Unit 10401). Then,solutions were diluted 500 times by adding ultrapurewater (Millipore Symplicity 185), filtered at 0.45 μmand analysed by ion chromatography (Dionex DX120)(method adapted from Masson and Andrieu, 1996). Theeluent used was 26 mmol L−1 methane sulfonic acid.Total concentrations of other elements, P, Cd, Cr, Cu,Ni, Pb and Zn, were measured after digestion in aquaregia using atomic absorption spectrometry.

2.4. Statistical analysis

When conditions of normality and variance homoge-neity (verified by Shapiro–Wilks and Bartlett testsrespectively) were met, data were interpreted using

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b0.05, ⋆⋆pb0.01, ⋆⋆⋆pb0.001.

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parametric tests: soil data using one-way ANOVA, andplant data using two-ways ANOVA (factors were rateand species). If there were no interactions between thetwo factors tested, results are presented as the mean ofthe three plant species. When significant effects offactors were observed, post hoc tests were carried outusing least significant different values (Tukey's test, 0.05significance level) (Zar, 1984). In case of non-homoge-neity of variance, the non-parametric Kruskall–Wallistest was used followed by the Newman–Student–Keulstest. Seedling survival was compared with χ2 test (0.01significance level). The software Statgraphics Plus(version 2.1: Statistical Graphics Corporation©, Copy-right 1994–1996) was used.

3. Results

3.1. Soil fertility

Compost significantly increased fertility of the soil(Fig. 1). Indeed, the organic matter content increased inD40 amended soil, but the effect declined over time. Inaddition, total N concentrations increased in amendedsoils 7 months (for D40) and 1.5 years (for D20) afteramendment. As with OM, this effect disappeared2.5 years after amendment.

Soil total and available P concentrations were alsosignificantly increased by the compost. At D40 rate, soil

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total P concentrations increased up to 5 times comparedto control (7 months and 1.5 years after amendment),and remained until the end of the experiment (four timesgreater 2.5 years after amendment). Similarly, soil avai-lable P concentrations significantly increased in amen-ded soil, especially at D40 rate. In the latter, soilavailable P concentrations reached 313.1 mg kg−1 DM1.5 years after amendment, which is more than 13 timeshigher than in the control.

Available soil cation concentrations were affected dif-ferently. Available Mg concentrations were significantlyincreased after amendment at D40 rate and up to the endof the study period, but Mg concentrations in D20 werenot different from the control. The compost increasedavailable K concentrations after amendment at D40 rate:this effect was significant 1.5 years after amendment andthen disappeared.

3.2. Soil and foliar trace metal concentrations

Soil total Cu and Zn concentrations increased inamended soil both for D20 and D40 rates 7 months and1.5 years after amendment and then decreased to thecontrol concentrations (Fig. 2). The increase reached 55%in D40 and 25% in D20 for soil total Cu, and 25% in D40and 12% in D20 for soil total Zn.

Available Cu and Zn concentrations increased signif-icantly in D40 amended soil in comparison with control

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onths after amendment (at plantation time in December 2001), 1.5 yearl (D0), 20 kg of compost per seedling (D20) and 40 kg of compost perates). ⋆pb0.05, ⋆⋆pb0.01, ⋆⋆⋆pb0.001.

Table 2Trace metal concentrations (mg/kg DM) in seedling leaves or needles one year (December 2002) and two years (November 2003) after plantation forcontrol (D0), 20 kg of compost per seedling (D20) and 40 kg of compost per seedling (D40)

Compost rate Cd (mg kg−1 DM) Cr (mg kg−1 DM) Cu (mg kg−1 DM) Ni (mg kg−1 DM) Pb (mg kg−1 DM) Zn (mg kg−1 DM)

2002 D0 0.05 (0.009)a 1.5 (0.5)a 5.7 (0.9)a 0.34 (0.18)a 0.83 (0.13)a 75 (4.6)a

D20 0.06 (0.005)a 1.95 (0.7)a 5.9 (0.6)a 0.54 (0.34)a 0.73 (0.11)a 91 (5.1)a

D40 0.04 (0.013)a 2.12 (0.6)a 6.6 (0.6)a 0.45 (0.28)a 0.78 (0.1)a 93 (12.7)a

2003 D0 b0.01 0.59 (0.09)a 5.5 (0.2)a 0.38 (0.04)a 0.79 (0.14)a 94 (8.9)a

D20 b0.01 0.69 (0.09)a 5.9 (0.2)a 0.38 (0.03)a 0.76 (0.14)a 100 (10.4)a

D40 b0.01 0.58 (0.08)a 5.7 (0.4)a 0.36 (0.04)a 0.61 (0.08)a 91 (8.6)a

The three species are considered all together. Mean (SE), N=9. Results of the comparison are given by an exponent letter: values that do not differ atthe 0.05 level are noted with the same letter.

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(Fig. 1). This effect was maximal 1.5 years after amend-ment for both elements and remained for Cu while itdisappeared for Zn 2.5 years after the amendment. Fur-thermore, the increase was also observed at D20 rate forsoil available Zn concentrations.

Soil concentrations of the other total trace elements(Cd, Cr, Ni and Pb) were not significantly affected by theamendment.

Compost had no significant effect on foliar trace metalconcentrations (Table 2).

3.3. Seedling responses to compost amendment

In 2002, the first year after plantation, compost amend-ment did not increase survival rate of the three species,while there was a significant positive effect forQ. ilex andP. pinea in 2003, the second year after planting (Fig. 3).Indeed, in 2003, survival was significantly higher in D40forQ. ilex (+40%), and in both compost rates for P. pinea(+30%) compared to control. Survival of P. halepensiswas not improved by compost in 2003. For all species andcompost rates, survival rates in 2003 were significantlylower than in 2002.

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Fig. 3. Annual survival (%) one year (December 2002) and two years (Novseedling (D20) and 40 kg of compost per seedling (D40). ⋆⋆⋆pb0.001.

Annual growth rates (length and radial growth) changedbetween compost rates, years, and species (Figs. 4 and 5).For all species and both years, the compost amendmentincreased length growth up to 3 times and doubled radialgrowth compared to control. Similarly to survival rates,annual growth rates were significantly lower in 2003 incomparison with 2002.

Seedling species were differently affected by the com-post amendment only in 2002 (two way ANOVA, spe-cies×compost rate, p=0.031) (Fig. 5). Indeed, P. pinealength growth increased proportionally to compost rate(33.5, 54.4 and 72.7% respectively for D0, D20 andD40).On the contrary, P. halepensis, and to a lesser extent Q.ilex, had a maximal length growth at D20 rate. Indeed, forthose 2 species, length growth at D40 rate (52.5 and33.5% respectively for P. halepensis and Q. ilex) wasintermediate between D20 rate (100.5 and 46.5%) andcontrol (18 and 24.8%).

Foliar N and P concentrations were significantly hig-her for seedlings grown in amended soils than in controlfor both 2002 and 2003 (Table 3). Foliar P concentrationssignificantly increased with the rate of compost in 2002and in 2003. Foliar nitrogen concentrationswere similar at

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Fig. 4. Mean annual length and radial growth (%) one year (December 2002) and two years (November 2003) after plantation for control (D0), 20 kgof compost per seedling (D20) and 40 kg of compost per seedling (D40). The three species are considered all together. Bars denote SE (N=15).Results of the comparison are given by an exponent letter: values that do not differ at the 0.05 level are noted with the same letter.

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D20 and D40 rates for both years, and significantly lowerin 2003 than in 2002.

The compost amendment increased significantly foliarK concentrations in 2002 for both compost rates (Table 3),whereas this effect did not arise in 2003. Compost had noeffect on foliar Mg and Ca concentrations.

4. Discussion

4.1. Effects on soil properties

The improvement of soil fertility observed aftercompost amendment has been widely observed(Guerrero et al., 2001; Korboulewsky et al., 2002;Martinez et al., 2003) and is the reason of its use inagriculture. Indeed, sewage sludge is source ofmacronutrients and organic C, due to concentrationof salts from water purification, these salts being fixedin microflora. However, these improving effectsdisappeared 2.5 years after amendment for N, OM

0

25

50

75

100

125

D0 D

% le

ngth

gro

wth

Q.ilex P.hale

Fig. 5. Length growth (%) of the three species during the first year of growt20 kg of compost per seedling (D20) and 40 kg of compost per seedling (D

and K. Likewise, Martinez et al. (2003) and Guerreroet al. (2001) found that compost effects on soildecreased over time, as its OM mineralized. In ourexperiment, the disappearing effect of N enrichmentcan have two combined explanations. On one hand, Nis probably the limiting nutrient in our ecosystem, asin most terrestrial ecosystems (Archibold, 1995;Davey and Wollum, 1984; Thirukkumaran andParkinson, 2002), and may have been highly absorbedby the seedlings, as foliar concentrations and growthrates suggest. On the other hand, part of N could havebeen leached (NO3

− form, Sands, 1984) especially thatthe highly fractured bedrock (Aubert, 1983) favours itstransport to groundwater. However, at D40 rate (16 tof fresh matter ha−1), the amount of N supplied bycompost reaches 73.9 kg ha−1 that is far below thequantity recommended by the EU legislation (from170 to 210 kg ha−1 an−1) preventing groundwaterpollution by nitrates (Council Directive of 12December 1991 concerning the protection of waters

20 D40pensis P.pinea

h (December 2001–December 2002) after plantation for control (D0),40). Mean±SE (N=5).

Table 3Nutrient concentrations in seedling leaves or needles one year (December 2002) and two years (November 2003) after plantation for control (D0),20 kg of compost per seedling (D20) and 40 kg of compost per seedling (D40)

N P K Mg Ca

(% DM) (% DM) (% DM) (% DM) (% DM)

2002 D0 1.28 (0.08)a 0.11 (0.008)a 0.59 (0.05)a 0.11 (0.004)a 0.54 (0.05)a

D20 1.38 (0.06)ab 0.17 (0.019)b 0.65 (0.06)b 0.12 (0.003)a 0.56 (0.05)a

D40 1.53 (0.07)b 0.19 (0.020)c 0.66 (0.06)b 0.11 (0.003)a 0.51 (0.04)a

2003 D0 1.15 (0.05)a 0.11 (0.007)a 0.45 (0.04)a 0.1 (0.006)a 0.49 (0.02)a

D20 1.37 (0.05)b 0.15 (0.016)b 0.5 (0.05)a 0.11 (0.006)a 0.53 (0.03)a

D40 1.41 (0.06)b 0.14 (0.015)b 0.5 (0.06)a 0.11 (0.005)a 0.48 (0.04)a

The three species are considered all together. Mean (SE), N=9. Results of the comparison are given by an exponent letter: values that do not differ atthe 0.05 level are noted with the same letter.

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against pollution caused by nitrates from agriculturalsources (91/676/EEC)).

Contrarily to N, as total P and Mg are brought inmuch higher amounts (Table 1), their concentrationsremained higher until the end of the experiment com-pared to control.

The sewage sludge entering compost compositioncomes from a sewage plant that applies a depho-sphatation process to sewage. Thus, P is concentrated inthe sludge that leads to the remarkable enrichment inavailable P. Likewise, Martinez et al. (2003) reported aten fold increase of available P in biosolids amended soil1 year after amendment. Although P is not particularlymobile in chalky soils because it may form inorganiccalcium phosphate (Khanna and Ulrich, 1984), itsbuildup exceeds plant uptake (it remained significant2.5 years after amendment in D40 amended soil) andcould lead to serious water pollution problems (Whalenand Chang, 2001) and limits rates of compost which canbe used.

4.2. Effects on seedlings

Foliar N, P and K levels in seedlings grown on amen-ded soils were higher than in seedlings grown on control.However, compost amendment had no significant effectonMg and Ca concentrations in seedling leaves, althoughcompost amendment induced significant and durableavailable Mg increase in soil. This might be due to theformation of humates and fulvates between the organicmatter of the compost and magnesium, so that it is retai-ned in a form unavailable to plants (Moreno et al., 1996).

Interspecific differences appeared in survival respon-ses to compost amendment. Compost improved survivalof seedlings of Q. ilex and P. pinea under drought con-ditions in 2003. This could be related to the betternutritional status (N, P, K) on amended soils, especially ahigher foliar K concentration. Welander and Ottosson

(2000) reported that transpiration rates of oak seedlingsdepends on foliar nutrient concentrations. High levels offoliar K are associated with reduced transpiration rates inseveral tree species, due to regulatory effect of this ion onstomatal movements (Van Den Driessche, 1984), andtherefore improve water saving in case of drought. More-over, Khanna and Ulrich (1984) reported that K defi-ciencies may particularly occur in plantations oncalcareous soils. However, we did not observed differ-ences in foliar nutrient concentrations between species.Therefore, foliar K status cannot by itself explain thedifferences of survival between species. Contrarily to P.pinea and Q. ilex, P. halepensis did not respond to com-post amendment neither in 2003 nor in 2002 for itssurvival. The differences between species could beexplained by their ecology. P. halepensis can grow invery dry habitats in the Mediterranean basin, on all typesof soils, and can withstand 6–8 months of summerdrought (Quézel and Médail, 2003). On the contrary P.pinea colonizes essentially littoral humid habitats, on lightand deep soils. This species is more sensitive to waterdepletion, as is also Q. ilex, compared to P. halepensis.Under the severe drought in 2003, these species were thusmore responsive to compost which probably improvedsoil water retention.

For Q. ilex and P. pinea grown on D40 rate, rootbehaviour should be taken into account in the seedlingresponse to water availability. We can assume that com-post has also increased root growth because of nutrientsupply, since it has increased stem growth. Some previousstudies have reported that organic or mineral fertilizationincreased root biomass and development of Quercusseedlings. Root biomass of Quercus petraea seedlingswas enhanced by organic fertilization (slow-release ferti-lizer) (Berger and Glatzel, 2001). Villar-Salvador et al.(2004) have reported a higher root growth capacity on N-fertilized Q. ilex seedlings. As root system developeddeeper, seedlings were able to access more water.

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Therefore, seedlings could resist more efficiently to waterdepletion in severe drought conditions.

Compost amendment also increased growth (lengthand radial growth) of all three species studied and bothyears. These results are in accordance with previous re-search on P. halepensis grown on composted urban waste(Román et al., 2003), on Picea sitchensis and Pinus resi-nosa grown on sewage sludge and compost (Dutch andWolstenholme, 1994; Brockway, 1983). The increasedgrowth may be linked to their better nutrient status (NPK)(Martin-Prével et al., 1984). Indeed, high foliar N con-centrations, and P to a lesser extent, in seedlings grown onamended soils, may be responsible for growth increase(McKay and Moffat, 2001).

The growth response to compost amendment of thethree species was not similar. The D40 compost rateinduced maximal length growth in 2002 for P. pineaseedlings, even though it was D20 compost rate for P.halepensis and Q. ilex seedlings. As compost inducedvery elevated concentrations of available P in D40amended soils, and as plant growth reductions havebeen reported when soil P is in excess (Bingham,1966), excessive available P may have inhibitedgrowth of P. halepensis, and Q. ilex, grown on thehighest rate of compost.

For all species and compost rates, the seedlingsurvival, growth and foliar nutrient concentrations werelower in 2003 than in 2002. Indeed, seedlings had tocope with an early and severe drought during the year2003. Drought decreases the nutrient absorption byplants, leading to lower foliar nutrient levels, survivaland growth rates.

4.3. Soil and foliar trace metal concentrations

Compost is usually considered as an extra source ofheavy metals (Cr, Cd, Ni and Pb), but in this experimen-tation, it was less contaminated than native soil (exceptfor a weak contamination in Cd (Table 1). The high pH ofthe calcareous soil, which favours immobilization ofmost heavy metals in soil (Martinez et al., 2003), mayhave protected seedlings from their absorption. Thus, notrace metal contamination induced by compost appearedin foliar parts of the seedlings after amendment.Moreover, Cd, Cr, Pb and Ni concentrations were farbelow toxic limits of sensitive plant species (Kabata-Pendias and Pendias, 1992). However, these elementsremain for very long periods of time in soils (Dai et al.,2004) and further changes in physicochemical soilconditions could induce some remobilization of thesetoxic elements and increase their disposability forseedlings (Planquart et al., 1999).

Among trace metals, the significant increase in totaland available Cu and Zn in soil at D40 rate had nosignificant consequence on foliar concentrations in thesemetals. In calcareous soil, Ca2+ is the major ion andreduces plant absorption of other polyvalent cations(competitive ion effect). Thus, Camay have prevented Cuand Zn from being absorbed despite their increased con-centrations in the soil. In addition, to assess seedling Cuabsorption, foliar concentrations may not be good indi-cators because of preferential root accumulation and res-tricted transport to foliage (Van Den Driessche, 1984;Wisniewski and Dickinson, 2003). Furthermore, phos-phorus, found in high concentrations in amended soils,might have complexed with Cu and Zn, depleting theirabsorption by seedlings (Kabata-Pendias and Pendias,1992; Khanna and Ulrich, 1984).

The soil available Zn and total Cu and Zn enrichmenteffect of compost had disappeared 2.5 years afteramendment. Since no significant foliar absorption ofCu and Zn was found on seedlings grown on amendedsoils, these elements might have been deep leachedthrough the highly fractured bedrock, explaining totalconcentrations decrease. Moreover, the progressivedegradation of organic matter reduced the number ofsite fixation for cations, inducing an increase in theirleachability, especially for Cu (Moreno et al., 1996).Thus, it is very likely that available Cu concentrationwill rapidly decrease to control concentration, even if itremained significantly higher in soil amended withD40 rate compared to control at the end of theexperimentation.

5. Conclusion

Compost improved the nutritional status (N, P, K) andgrowth of all three studied species, and reduced themortality of Q. ilex and P. pinea under droughtconditions in 2003. In consequence, compost could beamended in Mediterranean region to restore fertility ondegraded soils, and create better conditions for treeinstallation. This suggests that compost can significantlyimprove plantation success in afforestation of burnt siteswith Q. ilex. In early stages of succession, Q. ilex couldcompete more efficiently with post-fire P. halepensisseedlings.

P, Cu and Zn concentrations increased in amendedsoils with a potential negative effect on tree length growthand ground water quality when applied at high rates or incase of repeated amendments. According to our results, Pis the limiting factor for the use of this sewage sludge andgreen waste compost, and to a lesser extent Cu and Zn. Inconsequence, to prevent pollution, compost should be

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amended only below 40 kg m−2. Compost composition,and initial soil properties must be studied before expe-rimental setting.

Acknowledgements

This research was supported by the Conseil Généraldes Bouches-du-Rhône (France), the ADEME (AgenceDe l'Environnement et de la Maîtrise de l'Energie), theConseil Régional Provence-Alpes-Côte-d'Azur and theRhône-Méditerranée-Corse French Water Agency.

Sylvie Dupouyet and Stéphane Greff are gratefullyacknowledged for the field and laboratory assistance.

References

Aerts R. The advantages of being evergreen. Trends Ecol Evol 1995;10(10):402–7.

AFNOR,.Qualité des sols. In: AFNORedition, Recueil de normes,Vol. 1et 2, Paris, 1999.

AIRMARAIX, 1999. Campagne de mesures temporaire de la camionn-ette laboratoire : Aix les Milles, France, 20.05.1999–8.07.1999.

Archibold O.W. Mediterranean ecosystems. In: Chapman and Hall,editors. Ecology of world vegetation, London, 1995, pp. 131–164.

Aubert G. Apport de la connaissance de la végétation spontanée dans larecherche des potentialités forestières d'un territoire en régionméditerranéenne. Revue Forestière Française 1983;XXXV(6):425–42.

Berger TW, Glatzel G. Response of Quercus petraea to nitrogen ferti-lization. For Ecol Manag 2001;149:1-14.

Bingham FT. Phosphorus. In: Chapman HD, editor. Diagnostic criteriafor plants and soils. University of California; 1966. p. 324–62.

Brockway DG. Forest floor, soil, and vegetation responses to sludgefertilization in red and white pine plantations. Soil Sci Soc Am J1983;47:776–84.

Caravaca F, Garcia C, Hernandez MT, Roldan A. Aggregate stabilitychanges after organic amendment and mycorrhizal inoculation in theafforestation of a semiarid site with Pinus halepensis. Appl Soil Ecol2002;19:199–208.

Dai J, Becquer T, Rouiller JH, Reversat G, Bernhart-Reversat F, LavelleP. Influence of heavymetals onC andNmineralisation andmicrobialbiomass in Zn-, Pb-, Cu-, and Cd-contaminated soils. Appl Soil Ecol2004;25:99-109.

Davey CB, Wollum AG. Nitrogen fixation systems in forest plantations.In: BowenGD,Nambiar EKS, editors. Nutrition of plantation forests.London: Academic Press; 1984. p. 181–210.

De Luis M, Garcia-Cano MF, Cortina J, Raventos J, Carlos Gonzalez-Hidalgo J, Rafael-Sanchez J. Climatic trends, disturbances and short-term vegetation dynamics in a Mediterranean shrubland. For EcolManag 2001;147:25–37.

De Nicola F, Maisto G, Alfani A. Assessment of nutritional status andtrace element contamination of holm oak woodlands through ana-lyses of leaves and surrounding soils. Sci Total Environ2003;311:191–203.

Dutch J, Wolstenholme R. The effects of sewage sludge application toa heathland site prior to planting with Sitka spruce. For EcolManag 1994;66:151–63.

FAO. World reference base for soil resources. Rome: International Societyof Soil Science; 1998.

Garcia C, Hernandez T, Costa F. The influence of composting and matu-ration processes on the heavy-metal extractability from some organicwastes. Biol Wastes 1990;31(4):195–219.

Guerrero C, Gomez I, Moral R, Mataix-Solera J, Mataix-Beneyto J,Hernandez T. Reclamation of a burned forest soil with municipalwaste compost: macronutrient dynamic and improved vegetationcover recovery. Bioresour Technol 2001;76:221–7.

Hernandez L, Probst A, Probs JL, Ulrich E. Heavy metal distribution insome French forest soils: evidence for atmospheric contamination.Sci Total Environ 2003;312:191–203.

Kabata-Pendias A, Pendias H. Trace elements in soils and plants. 2ndedition. USA: CRC Press LLC; 1992. 365 pp.

Khanna PH, Ulrich B. Soil characteristics influencing nutrient supply inforest soils. In: Bowen GD, Nambiar EKS, editors. Nutrition of plan-tation forests. London: Academic Press; 1984. p. 79-118.

Korboulewsky N, Dupouyet S, Bonin G. Environmental risks of applyingsewage sludge compost to vineyards: carbon, heavy metals, nitrogen,and phosphorus accumulation. J Environ Qual 2002;31:1522–7.

Larchevêque M, Montes N, Baldy V, Dupouyet S. Vegetation dynamicsafter compost amendment in a Mediterranean post-fire ecosystem.Agric Ecosyst Environ 2005;110:241–8.

Martinez F, Cuevas G, Calvo R, Walter I. Biowaste effects on soil andnative plants in semiarid ecosystem. J Environ Qual 2003;32:472–9.

Martin-Prével P, Gagnard J, Gautier P. L'analyse végétale dans lecontrôle de l'alimentation des plantes tempérées et tropicales. Paris:Lavoisier; 1984. 810 pp.

Masson P, Andrieu M. Simultaneous analysis of nitrogen, potassium,calcium and magnesium in digested plant samples by ionchromatography. Analusis 1996;24(9–10):380–2.

McKay HM, Moffat AJ. GB experience in the last decade: fromresearch to practice. Biosolids utilisation in forestry. InternationalWorkshop, 29–30 March 2001, Bordeaux, France. INRA editions;2001.

Moreno JL, Garcia C, Hernandez T, Pascual JA. Transference of heavymetals from a calcareous soil amended with sewage-sludgecompost to barley plants. Bioresour Technol 1996;55:251–8.

Moreno-Peñaranda R, Lloret F, Alcañiz JM. Effects of sewage sludgeon plant community composition in restored limestone quarries.Restor Ecol 2004;12(2):290–6.

NF U 44-095. Amendements organiques: Composts contenant desmatières d'intérêt agronomique issues du traitement des eaux.AFNOR, 2002;JO du 26/03/2004.

Olsen SR, Cola CV, Watanabe FS, Dean LA. Estimation of availablephosphorus in soils by extraction with sodium bicarbonate. CircUS Dep Agr 1954;939:1-19.

Planquart P, Bonin G, Prone A, Massiani C. Distribution, movementand plant availability of trace metals in soils amended with sewagesludge composts: application to low metal loadings. Sci TotalEnviron 1999;241:161–79.

Quézel P, Médail F. Ecologie et biogéographie des forêts du bassinméditerranéen. Environmental series. Paris: Elsevier; 2003. 571 pp.

RománR, FortúnC, García LópezDe SáME,AlmendrosG. Successfulsoil remediation and reforestation of a calcic regosol amendedwith composted urban waste. Arid Land Res Manag 2003;17:297-311.

Rundel PW. Leaf structure and nutrition in Mediterranean-climatesclerophylls. In: Specht RL, editor. Mediterranean-type ecosystems:a data source book. Dordrecht: Kluwer Academic Publishers; 1988.p. 157–67.

Sands R. Environmental aspects of plantation management. In: BowenGD, Nambiar EKS, editors. Nutrition of plantation forests. London:Academic Press; 1984. p. 413–38.

11M. Larchevêque et al. / Science of the Total Environment xx (2006) xxx–xxx

ARTICLE IN PRESS

Thirukkumaran CM, Parkinson D. Microbial activity, nutrientdynamics and litter decomposition in a Canadian Rocky Mountainpine forest as affected by N and P fertilizers. For Ecol Manag2002;159:187–201.

Van Den Driessche R. Nutrient storage, retranslocation and relationshipof stress to nutrition. In: BowenGD,Nambiar EKS, editors. Nutritionof plantation forests. London: Academic Press; 1984. p. 181–210.

Villar-Salvador P, Planelles R, Enríquez E, Peñuelas Rubira J. Nurserycultivation regimes, plant functional attributes and field performancerelationships in the Mediterranean oak Quercus ilex L. For EcolManag 2004;196:257–66.

Whalen JK, Chang C. Phosphorus accumulation in cultivated soils fromlong-term annual applications of cattle feedlot manure. J EnvironQual 2001;30:229–37.

Welander NT, Ottosson B. The influence of low light, drought andfertilization on transpiration and growth in young seedlings ofQuercus robur L. For Ecol Manag 2000;127:139–51.

Wisniewski L, Dickinson NM. Toxicity of copper to Quercus robur(English Oak) seedlings from a copper-rich soil. Environ Exp Bot2003;50:99-107.

Zar JH. Biostatistical analysis. 2nd edition. U.K.: NJ Prentice-Hall Inc;1984. 718 pp.