Agronomic and environmental effects of land application of residues in short-rotation tree plantations: A literature review

Biomass and Bioenergy 81 (2015) 378e400

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Review

Agronomic and environmental effects of land application of residues in short-rotation tree plantations: A literature review Nicolas Marron a, b, * a b

INRA, UMR 1137 Ecologie et Ecophysiologie Foresti
eres, F-54280 Champenoux, France Universit e de Lorraine, UMR 1137 Ecologie et Ecophysiologie Foresti
eres, F-54500 Vandœuvre-l
es-Nancy, France

a r t i c l e i n f o

a b s t r a c t

Article history: Received 19 January 2015 Received in revised form 16 July 2015 Accepted 19 July 2015 Available online xxx

Land application of residues in short-rotation plantation has a priori the double advantage to meet the nutrient needs of these tree plantations at lower cost while recycling residues. Agronomic and environmental effects of a very wide variety of residues on plants and soils have been studied worldwide. I attempt here to compile and to summarize the results of the studies about the effects of land applications of residues (mostly organic) in plantations or under controlled pot conditions of the three species mostly used for short-rotation coppice: willow, poplar, and eucalyptus. The spreading of most residues causes an enrichment of the soil in nutrients and a subsequent increase in the growth of plants. Manure, compost, sewage sludge, and wastewater seem most effective in stimulating growth. Ashes have less impact on growth. Few negative effects on the plant have been highlighted in response to spreading, except in the case of very rich effluents in salt in response to which growth reduction and leaf loss nevertheless did not lead to plant death. The high transpiration potentials of the fast growing species dedicated to intensive tree plantations allow them to absorb and tolerate, without major damages, nutrients in excess, most heavy metals, and antibiotics. In some cases, heavy metal accumulation in soils following the spreading of residues, but few of them showed leaching or water pollution. Nevertheless, the used doses and the intervals between applications were of primary importance to avoid leakage of undesirable elements in the environment. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Short-rotation coppice Land application Fertilization Residues Fast-growing tree species

1. Introduction The current energy and environmental issues have brought back to the center stage plantations dedicated to the production of plant biomass [1]. Among them, intensive tree plantations, with short rotations, are often installed on low fertility sites, not used for food agriculture, to avoid competition with these cultures. The species used (willow, poplar, eucalyptus) have nevertheless substantial nutritional requirements and it is difficult to fertilize this type of plantations being cost effective and without risk of pollution to the environment [2]. In this context, the spreading of residues has a priori the double advantage to meet the nutrient needs of these tree plantations at lower cost while recycling residues. Intensive tree plantations have also the particularity to be intermediate between agriculture and forestry, combining properties of both ecosystems.


res, Route d'Amance, * INRA Nancy, UMR 1137 Ecologie et Ecophysiologie Forestie F-54280 Champenoux, France. E-mail address: [email protected]. http://dx.doi.org/10.1016/j.biombioe.2015.07.025 0961-9534/© 2015 Elsevier Ltd. All rights reserved.

The used species notably exhibit very high evapotranspiration and accumulation potential in woody biomass, and are thus very good candidates for phytoremediation processes [3,4]. In many countries, short-rotation tree plantations are established on agricultural lands where the application of residues is regulated by the laws prevailing in agriculture, not in forest. However, because the production of short-rotation coppice plantations is not dedicated to human or animal feeding, the effects of very diverse kinds of residues have been tested and described in the scientific literature. Review papers about residue application in forest have already been published [5e8]. In this contribution, I more specifically focus on short-rotation coppice species. More precisely, I attempt to compile the results of studies about the effects of land applications of various kinds of residues (principally organic), including sewage and industrial sludge, wastewater, manure, compost, ashes, biochar, and landfill leachates, in plantations, under natural conditions, or under controlled pot conditions of the three species mostly used for short-rotation coppice (SRC): willow, poplar, and eucalyptus. Agronomic (at plant and soil levels) and environmental effects

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(soil and water contaminations) are reviewed (Fig. 1). Two tables, classifying and summarizing the 288 cited references (Appendix 1) and attempting to synthetize agronomic and environmental effects on plant, soil, and cultural systems of the different categories of residues (Table 1), are presented. In addition, when data in literature were available and sufficient, a quantitative analysis of plant (growth and N content) and soil (N, nitrates, and heavy metal contents, and nitrification and ammonification rates) responses to residue application, as compared to unfertilized controls, was realized. Studies presenting either no control conditions, or control conditions based on a mineral fertilization were not taken into account. Literature about the spreading of residues in forest plantations in general covers the period from 1976 to present, with a net increase in 1998 and up to 2011 (Fig. 2). This is probably due to the general increase of scientific literature, but also to the development of forest plantations dedicated to the production of biomass during this period. From 2012 on, a slight decrease of the number of studies is observed. Literature comes from all continents, Europe being leader (51% of the references; Fig. 3A). The reduction of greenhouse gas emissions, including through the substitution of fossil fuels by biomass, is a particularly significant issue in Europe and North America, which probably explains why nearly threequarters of the studies about the spreading of residues in SRC come from these two continents. Studies dealing with the response of willow trees account for almost half of the references (Figs. 3B and 4). Within the Populus, Salix, and Eucalyptus genus, a wide

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range of species and hybrids have been studied, resulting in a limited number of studies about each species (Fig. 4). The most frequently described species are Eucalyptus globulus, Eucalyptus grandis, Populus deltoides, Populus
euramericana, and Salix viminalis. The residues considered in the literature are from very diverse origins (Fig. 3C). Contrarily to agriculture, where manure is primarily used, two thirds of the studies about land applications in SRC plantations concern sewage sludge and wastewater (including industrial effluents). Overall, the effluents are for a quarter of industrial origin and three quarters of municipal origin (Fig. 3D). The industries involved are various: textile, tannery, paper mill, dairy, pharmaceutical, pesticide, wood industry, distillery, steel, etc. However, studies concerning each of the different types of industries are very few; each type remains finally rather anecdotal in the literature. The quantities of land applied residues are also very variable and are often expressed in different terms: dry weight, fresh weight, volume, content of an element (N, P, etc.) or a pollutant (Cu, Zn, etc.) (Appendix 1), which makes comparison between studies difficult. The spreading of residues in shortrotation tree plantations presents some specificities as compared to the spreading in agriculture. Notably, in some cases, the collateral accumulation/sequestration by fast growing trees of undesirable elements present in the residues is expected in addition to the fertilizing effect. This may have an impact on the range of residues applied in SRC, including highly contaminated materials (landfill leachate, polluted industrial effluents, etc.). 2. Agronomic effects of the spreading of residues in shortrotation tree plantations 2.1. Impact on tree yield and physiology

Fig. 1. Main study objects, at plant, soil, and cultural system levels, of the studies about the effects of the land application of residues in short-rotation tree plantations.

Most studies about the spreading of sludge from municipal wastewater treatment plants (WWTP) show significant stimulation of the growth of willow, poplar and eucalyptus (Fig. 5), greater than that obtained in response to mineral fertilization [9e13]. Some studies mention performances multiplied by two or three in response to the effluent application [14,15]. On average, in literature, a two-fold growth increase in response to sludge application is observed (Fig. 5), with extreme values corresponding to an increase of more than 600% as compared to the unfertilized control [16] and up to almost 3000% [12] (not represented on Fig. 5). Limed sludge gave the best results, while heated sludge gave the worst results [17e19]. Composted sludge were also recommended to be used as 30e60% of the substrate to result in a beneficial effect on growth [18,20]. However, it was shown that non-composted sewage sludge (anaerobically digested) released more nitrogen than composted sludge [21]. In this sense, other studies have shown little effect of composted sludge on willow yields, sludge being not sufficient to meet the nutritional needs of trees [22]. Besides the production of biomass and growth, the addition of sludge has been shown to enhance tree survival [23], to increase leaf area [24], to stimulate root colonization by mycorrhizae (ectomycorrhizae and arbuscular mycorrhizae; [12]), and to increase the absorption of phosphorus and nitrogen by the trees [25,26] (Fig. 6). In terms of wood anatomy, sludge did not affect the size of fibers and vessels, cellulose and lignin contents, and calorific values [27], but they had varying effects on the density of the wood: increase in Ref. [28] or decrease in Ref. [29]. The contradictory results obtained in these two studies on eucalyptus may be due to differences in the age of the tested plant material (2 years in Ref. [28] and 5 years in Ref. [29]). The interest of sludge application also lies in the fact that they gradually release their nutrients. So, the stimulation of growth

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Table 1 Synthesis of the effects of the different categories of organic residues on the soil, tree, and cultural system found in literature: (þ) increase, () decrease, (¼) no effect, (þ/) uncertain effect.

was sometimes observed one year or more after application [30]. Moreover, the fertilizing effect of sludge was more observed when the soil is well drained [31]. In willow as well as in poplar, a wide genetic variability has been observed in terms of the ability to use different types of slurries for the production of biomass [17,32e34] and in terms of their ability to accumulate in wood or bark heavy metals that may be present in effluent [35e37]. The potential to accumulate metals depended on the productivity of willows and on the type of metals, Cd and Zn being mainly absorbed, Ni, Hg, Cu and Pb being less absorbed [35,38]. The beneficial effect of the sludge application on tree growth can be reduced by the increased

development of herbaceous vegetation, increasing the competition with trees, especially in agroforestry systems [23,39]. The application effects of sludge or residues derived from diverse and various industries have been studied. The studies can be roughly classified into two categories depending on the purpose of the application: (1) to fertilize the trees while valorizing a residue, or (2) to get rid of industrial residues, often polluted, trying to limit the impact on the environment and to sequester in trees, for more or less long periods, the undesirable elements present in the effluents. The distinction between these two categories is not always clear as a fertilizing effect is often observed even when this is

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Fig. 2. Time course of the number of studies dealing with land application of residues in short-rotation tree plantations between 1978 and 2015.

Fig. 3. Share of the scientific literature about residue spreading in short-rotation tree plantations in terms of (A) geographic origin (continent), (B) studied species, (C) studied organic residues, and (D) origin of the studied organic residues (industrial vs. municipal). n ¼ 288 references.

not the primary goal of the experiment. It is important to note that the experiments of the second category, sometimes using highly polluted sludge, were all conducted in pots under controlled conditions, and not in the field. With the exception of sludge from the paper industry, the effects of sludge originating from the different industries are described in a very small number of studies. (1) Sludge spreading with the goal to fertilize while valorizing a residue: - Experiments in controlled conditions showed that the addition of 30% of pulp mill sludge to the substrate caused a six-fold increase in biomass production of willows [40]. However, such a stimulation of growth was not observed when the experiments were conducted in plantation (possibly because of the nutritional status of the site where the experiment was conducted, or the leaching of the nutrients contained in the sludge; [41]).

Moreover, an additional nitrogen fertilization was often needed because of the low nitrogen content of the pulp mill sludge [42,43]. Dilution with water of the pulp mill effluents (50e50) caused the accumulation and precipitation of sodium near the roots of poplar, but without toxicity for the plant [44]. Growth was more stimulated by the application of the undiluted effluent [45]. - Leaf area, biomass production, nutrient uptake and the ratio stem/root of eucalyptus were stimulated by meatworks effluent. Temperature was the main factor influencing the absorption of nutrients, not the amount of nutrients provided [46]. - The use of lignite washery sludge resulted in lower leaf N content and higher levels of B and Cd. This kind of sludge did not stimulate the growth of poplars the first years after application, perhaps due to soil acidification caused by the pyrite they contained and to their limited levels of organic substances [47].

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Fig. 4. Number of studies dealing with land application of residues for the different species and hybrids of Eucalyptus, Populus, and Salix. Species are indicated when they are the object of at least two studies. For the complete list of species and hybrids, see Appendix 1.

Fig. 5. Relative growth variations (%) reported in literature in response to residue applications as compared to unfertilized controls in Populus, Salix, and Eucalyptus. Genus are pooled. Aboveground woody biomass or total stem data height were used. Each box represents the quartile below (Q1) and above (Q3) the median value. Vertical bars represent minimum and maximum values except for individuals that are away 1.5 times from the top of the interquartile (Q3eQ1) range. The numbers of values and papers used for the calculation, and the general means ± standard deviations are indicated.

Fig. 6. Relative plant N variations (%) reported in literature in response to residue applications as compared to unfertilized controls in Populus, Salix, and Eucalyptus. Genus are pooled. Total N contents in aboveground biomass were used. Each box represents the quartile below (Q1) and above (Q3) the median value. Vertical bars represent minimum and maximum values except for individuals that are away 1.5 times from the top of the interquartile (Q3eQ1) range. The numbers of values and papers used for the calculation, and the general means ± standard deviations are indicated.

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- Growth of coppiced eucalyptus (cut late in the season to stimulate growth during the next growing season) was inhibited by effluents from a food processing factory, but not in the case of non-coppiced trees, probably because of the stump waterlogging by the effluent [48]. (2) Sludge spreading with the goal to evaluate the effect of the residue on trees and environment: - Sludge from tanneries, even if they were contaminated with heavy metals, caused an increase in the growth of willows (Italy, pots; [49]) and in the net assimilation and growth of poplar, but plants accumulated only low amounts of heavy metals [50]. - Steel effluents (released after washing the metal plates with nitric acid, hydrofluoric acid, and sulfur) caused the death of eucalyptus seedlings due to high concentrations of metal ions and low concentrations of Ca, Mg, K, Na, N, and P (India, pots; [51]). The mixing of this type of effluent with municipal effluent and/or effluent from the textile industry had a positive effect on growth. - Residues from the zinc industry caused the accumulation of large amounts of metals in willow leaves and phytotoxicity symptoms related to Zn and Cd (Brazil, pots; [52]). - Effluents from the textile industry (released after washing excess dyeing) reduced the mortality rate of eucalyptus seedlings, but these effluents also led to lower growth in comparison with municipal and steel effluent applications (India, pots; [51]). Once more, the mixture of the two types of effluents gave the best results in terms of productivity stimulation. - Industrial sludge rich in heavy metals (Zn, Cu, Cr, and Cd) had no toxic effect on poplars. The sludge caused an increase in the production of biomass and leaf area, and changes in biomass allocation between roots and stems (Italy, pots; [53]). Copper present in excess was never toxic for the plant; toxic from 137 mg kg1 for mycorrhizae; and toxic regardless of its content for soil microorganisms. The increase in Zn levels caused a decrease in productivity, root colonization by mycorrhizae and soil microorganisms (Australia, pots; [54]). - Harbor sludge contaminated with tributyltin (antifouling agent present in cheap paint) did not cause willow mortality even at the highest doses, although the growth and transpiration of willows were very limited. Toxicity was greater at pH 7 than at pH 4 (Denmark, laboratory; [55]). - More than 5% of powder of brick air scrubber byproduct negatively affected the biomass production, leaf area, and chlorophyll fluorescence of poplar trees. In comparison, for corn, 12.5% were required to observe these effects (USA, pots; [56]). - Effluents from the production of the fungicide Mancozeb (containing large amounts of sulphates) caused inhibition of growth of eucalyptus (India, pots; [57]). - Liquid residues from the extraction of bitumen rich in sodium, sulfate and chloride, led to the rapid fall of the leaves of poplars and willows, which, however, were quickly replaced by new leaves, morphologically different. Poplar showed a high tolerance to all treatments (Canada, hydroponics; [58,59]). In light of these results, it appears that the mixture of different types of residues (e.g. municipal, steel and textile industry effluents) or dilution with water was often the most effective in stimulating the survival and growth of trees and in reducing the toxic effects on plants [51]. On average, the result of industrial sludge application is a slight growth stimulation (þ16%; Fig. 5). However, due to the variety of the industries from where originates the residues, the effects are diverse (huge standard deviation on Figs. 5 and 6). N accumulation by plant was highest in response to

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application of meatworks effluent (about 9-fold as compared with the control; not shown on Fig. 6; [46]), while it was reduced by zinc, steel, and textile industry effluents (45% on average; [51,52]). Most studies dealing with the spreading of wastewater in intensive forest plantations focused on the supply of nutrients provided by the water, not on the “irrigation” aspect (Fig. 6). In general, wastewater did not cause short-term damage on plants and stimulated the growth of poplar, willow and eucalyptus [60e64] (Fig. 5). Notably, wastewater rich in nutrients and organic matter caused a gain in biomass of 143% for eucalyptus, 54% for poplar, and 274% for willow [65]. Similarly, a dose increase from 10 g m3 to 40 g m3 of N in secondarily treated wastewater caused a gain in height growth of over 85% and leaf area index (LAI) over 55% in eucalyptus during the second year, the effect being not significant during the first year [66]. Nevertheless, these results have to be nuanced for hyper saline wastewater reducing from 60 to 70% leaf and stem growth of eucalyptus [67]. Willow and poplar have been shown to be sensitive to moderately tolerant to salinity [68]. Salinity also caused a 50% reduction in the efficiency of conversion of carbon to biomass, but this effect disappeared three weeks after the leaching of salt. The salt had no effect on the use of water by eucalyptus. The fertilizing effect of wastewater depends on their origin. Domestic wastewater stimulated growth of poplars more than municipal wastewater and control water, due to more favorable nutrient and organic matter contents and lower levels of pollutants [69]. The beneficial effect of wastewater on tree growth also depends on the initial soil composition. For example, in Ref. [70], nitrogen found in the aboveground biomass (335 kg ha1) and litter (19 kg ha1) of eucalyptus in response to an application of secondarily treated wastewater (N dose: 508 kg ha1) after five years was only slightly different than that found in eucalyptus irrigated with normal water (N in biomass 301 kg ha1 and in litter 34 kg ha1). Similarly, despite a growth stimulation for poplar and eucalyptus in response to the addition of pretreated wastewater, only 31 and 35%, respectively, of the amounts of nitrogen and phosphorus present in the water were absorbed by trees [71]. The wastewater from the effluent mixture of hundreds of different industries in Hudiara (Pakistan) resulted in an accumulation of Na, Cd, and Cr in the tissues of eucalyptus [72]. K and P increased in roots, while Fe increased both in roots and stems. The mixture of wastewater with water (50/50) was most beneficial for the growth of eucalyptus [72]. As for sludge, it generally seems that the mixture of effluents from various sources or their dilution with water is more favorable for the growth of trees and less harmful for the environment. The number of leaves and biomass of eucalyptus increased with increasing amounts of municipal wastewaters [73]. Seedlings accumulated Na, K, Ca and Mg. Many studies particularly refer to the absorption and accumulation of Cd by the fast-growing woody species used for short-rotation plantations [61,69,72]. Manure from pigs, cattle and poultry significantly increased the productivity of willows, poplars and eucalyptus, filling the deficiencies in N and K of the trees [19,74e77] (Figs. 5 and 6). The highest growth stimulation was observed in response to the application of digestate from pig slurry, with biomass of plants receiving the effluent being more than 7 times higher than the control (Fig. 5, [78]). Carbon sequestration was also improved [77]. It was also shown that the effluents from dairy farming (including urine and feces and possibly the chemicals used to clean the areas of stalling and milking) increased biomass and transpiration of willows. The highest doses (N dose: 558 kg ha1) led nevertheless to chlorosis related to an excess of chlorine. Application of this type of effluent may also cause a leaf deficiency in sulfur [79]. In addition, the highest doses of these dairy farm effluents caused a stimulation of root growth (coarse and fine) in willows and eucalyptus in the upper soil horizons, which

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may have implications in the use of heavy machinery in the field [80]. The combination of paper sludge with pig manure gave the best results in terms of poplar growth stimulation compared with the use of each of the two residues separately [81]. Compared with sewage or municipal sludge, it was also shown that diluted human urine (approximately 1e3% urine diluted in pure water on one hectare in Sweden) showed the best results in terms of growth stimulation in willow SRC [82]. This type of application was, however, associated with an increase in pathogen and pest infections (mites, leaf rust, leaf beetles, etc.), but the negative effects of pathogens on biomass production were limited [82,83]. A few studies have investigated a collateral consequence of the spreading of manure: the effect on tree physiology of the presence of antibiotics used to treat animals. Four kinds of antibiotics have been studied: sulfamethoxine, trimethoprim, sulfonamide, and sulfadiazine. Sulfadimethoxine present in feces of treated calves spread in a willow plantation caused a reduction of the electron transport rate and net CO2 assimilation for the highest dose. Alterations of root morphology were also observed. Willow roots had a high potential to accumulate antibiotics, demonstrating that willow can absorb and tolerate high doses of antibiotics [84]. Willow accumulated and withstood without major damages sulfadiazine better than corn. The antibiotic, mainly accumulated in the roots, caused an alteration of root geotropism, an increased number of lateral roots, and a decrease of the water absorption. High doses caused a reduction in leaf C/N and chlorophyll contents [85]. Trimethoprim was toxic for the willows at a concentration of 100 g m3 [86]. In the case of sulfonamide, acclimation mechanisms were observed when willow exposure to the antibiotic increased, suggesting that this species could be utilized for the phytoremediation of sulfonamide [87]. Studies on the effects of various types of compost on tree production are quite disparate and highly variable (Fig. 5). Composted manure did not increase root development or water status in poplars, but it increased soil water retention properties. This type of compost also caused a growth gain [88]. Compost of municipal solid residues had no effect on willow rooting [89], but stimulated the growth of poplar and eucalyptus [90]. Compost or mulch of Southern fern (boiled and washed to remove possible allelochemicals) moderately stimulated the growth of eucalyptus seedlings (þ8 to 20%) [91]. Compared with doses of 0, 10 and 50% of waste compost from landfill (metal, plastic, and glass were removed), 25% (75% soil) caused the best height growth of willows. Composting during two years was more effective than during one year [92]. It was also shown that a mixture of domestic compost and wood chips caused a natural recolonization in polluted environments with heavy metals, including willow seedlings [93]. Data about the effects of leachate from the composting of green waste and municipal organic residues are scarcer and results are variable: in some cases, they reduced up to 62% aboveground biomass of poplars and willows [94]; while in other cases, an increase in height and diameter of poplar and black locust was observed [95]. The use of these leachate was associated with increases in leaf Na contents of the trees, which nevertheless caused no visual effect of toxicity or deficiency. Other foliar nutrients (N, P, K, Ca, and Mg) were little affected [95]. Vermicompost leachate increased by more than two or three times the percentage of emerged seedlings of eucalyptus. The authors recommended vermicompost leachate as a complement of a chemical fertilization [96]. Landfill leachate could bring very large quantities of N, P, and K to the crop system (up to 2144 kg ha1, 144 kg ha1, and 709 kg ha1, respectively; [94]). However, a phosphorus complement may be needed [97]. Landfill leachate increased to 155% the

production of biomass in willows and poplars [94]. The development of lateral roots was stimulated, but not basal roots [98]. Willow selectively absorbed heavy metals in this type of effluent, particularly Cd. Due to the very high evapotranspiration, the rapid growth and extensive root systems of poplars and willows (especially highly productive hybrids), heavy polluted landfill leachate doses could be used [3,99]. In particular, it was shown that the use of willow with high transpiration could multiply by 1.3e5 evaporation compared to bare ground. Nevertheless, transpiration efficiency was not sufficient to vaporize entirely the spread landfill leachate, and groundwater had to be isolated to avoid the risk of contamination [100]. The addition of sludge made the willow trees more resistant to the toxic effects of landfill leachate [101]. Ash spreading caused increases in soil pH, exchangeable cations, and extractable phosphorous [102]. The effects on the germination of eucalyptus seeds were often null or even negative; the germination time increased with increasing doses until complete inhibition [102e104]. Similarly, the effects on the productivity of willow and eucalyptus were either low [105,106] or negative [103] (Fig. 5). When an increase in productivity was nevertheless observed after the spreading of peat ash, additional K or N fertilization was required unless large quantities of ash were used [107] [108], (Fig. 6). In contrast, the mixture of ash with sludge [109,110], manure and/or a bacterial solution (Pseudomonas/Azotobacter) had a beneficial effect on growth [109,111]. The ashes alone tended to form an impenetrable film on the soil surface inhibiting the growth of willow roots, while gradually adding sludge to ashes allowed the roots to continue growing [110]. In Ref. [112], the authors recommended the addition of 20% of coal ashes and 20% of sludge to a sandy soil; this mixture led to a gain of poplar growth by 55% in height, 33% in diameter, and more visually healthy leaves, lost later than trees grown on a bare soil. The metal concentrations in plant tissues did not exceed those resulting from a chemical treatment [109]. Recently, a few studies have investigated the effects of biochar application in tree plantations dedicated to biomass production. In eucalypts as well as in poplar plantations, biochar application was beneficial for stand yield, stimulating both aboveground biomass production [113] and the number of stems produced [114]. Soil C sequestration was greatly improved [115]. On average, all kinds of residues result in a growth stimulation and an improvement of the tree N status (ranging from þ16% to þ102% and from þ10% to þ40%, respectively; Figs. 5 and 6). A very wide range of variation can be found in literature in terms of growth and tree N variations in response to residue applications as shown by the huge standard deviations in Figs. 5 and 6. Sewage sludge and manure are the most effective in stimulating growth (þ102% and þ62% on average, respectively) with the most extreme positive effects for these two categories of effluent. Negative effects on growth and tree N content are mainly observed in response to industrial sludge and manure applications, probably due to the fact that these effluents can be polluted or contain antibiotics. Ash and industrial sludge applications are the less effective in improving the N status of the trees (þ16% and þ10%, respectively). 2.2. Impact on soil composition and properties The spreading of residues in short rotation plantations is not always associated with a soil enrichment in nitrogen and organic matter. In most cases, the spreading of sludge, pretreated wastewater, manure, compost, and industrial effluents actually caused an increase in organic carbon, organic matter, and nitrogen in the soil [19,39,46,94,116e118] (Fig. 7). However, in some cases, the spreading of ashes (because of their low nitrogen content) and

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limed or anaerobically digested sludge (due to their slow decomposition) had no effect on soil nitrogen and organic matter [14,105,119,120]. The distribution of organic carbon molecules was shifted toward smaller sizes (inferior to 14 000 Da) in response to the spreading of sludge; in summary, the sludge could increase the mobilization of hydrophilic low molecular weight compounds in soils [121]. The spreading of residues may lead to increased levels of soil elements other than nitrogen. Ash spreading can lead to increases in P, K, Ca, Mg, and Fe in soils, with a marked effect on K [102,106,107]. Poultry manure greatly increased the levels of P in soil (13 fold as compared to the control), K (3 fold), and Mg (2.4 fold) in the first ten centimeters of soil [19]. Increases in soil P content following the spreading of sludge and wastewater were often reported in the literature, sometimes with contamination of groundwater [109,116,122,123]. This is probably linked to the fact that sludge doses used were generally calculated in terms of potentially available nitrogen for the plant. These doses correspond, however, to doses of phosphorous much superior to the needs of the plants and can lead to eutrophication risks if phosphorous is leached into water bodies. It was also shown that after six years of application of anaerobic digested sludge, total phosphorous significantly increased up to 25-cm depth under the poplars (45% in the first five centimeters) and that the amount of phosphorous absorbed annually by the switchgrass was five times higher than that absorbed by the poplar. In contrast, the amount of phosphorous in the mobile leached soil solution was two times higher in the case of switchgrass relative to poplar [124,125]. Sludge (from paper mills or not) induced Ca, Na, and Cl content increases in poplar and eucalyptus plantations [10,81,126,127]. Increases in Al and Mn contents of soil and eucalyptus leaves (due to the reducing

Fig. 7. Soil N variations (%) reported in literature in response to residue applications as compared to unfertilized controls in Populus, Salix, and Eucalyptus. Genus and residues are pooled. Total N contents, nitrate contents, and nitrification and ammonification rates in the upper soil layer were used. Each box represents the quartile below (Q1) and above (Q3) the median value. Vertical bars represent minimum and maximum values except for individuals that are away 1.5 times from the top of the interquartile (Q3eQ1) range. The numbers of values and papers used for the calculation, and the general means ± standard deviations are indicated.

385

conditions induced by waterlogging) were also observed in response to spreading of sludge and residues from the food industry [48,127]. Activated and limed sludges also led to increases in sulfur contents of leaves and soil in poplar and eucalyptus plantations [44,120]. Sludge (limed, composted, or not), ash and poultry manure caused an increase in soil pH of tree plantations [10,19,81,102,107,120,122,127]. In contrast, meatworks effluents or effluent from a food processing factory caused acidification of the soil, linked, in the second case, to the nitrification of ammonium [46,48]. Electrical conductivity [23,107] and cation exchange capacity (CEC; [39,102,120,122]) also increased in response to the spreading of ash, compost, or sludge, with notably an increase by a factor of five observed following land application of sludge in an eucalyptus plantation [126]. When leaching was low, soil salinity also tended to increase following the spreading of paper mill effluent [43], composted sludge [123], and pretreated wastewater [118]. Changes in the porosity and texture of the soil in response to land application of residues were also reported in the literature. The spreading of wastewater in the long term (20 years; [128]) or wastewater compost [129] led to a development of soil water repellency. A six-year recovery period (without land application) was not sufficient to eliminate this effect. The addition of kaolinite could be a way to improve this in sandy soils [128]. The use of paper mill sludge or wood chips in a poplar plantation led to a clear insulating effect of the soil, which could increase the risk of winter drought [130]. Finally, it was shown that the addition of 20% of coal ash and 20% of sludge in a sandy soil resulted in a lower bulk density and higher porosity, water content, and content of finegrained minerals [112]. In the same way, pretreated wastewater caused an increase in the macroporosity and the total porosity of the soil of poplar and eucalyptus plantations [118]. Stimulation of the soil biological activity and biodiversity (especially animal but also plant) was reported by many studies. Most groups of trace and macro-trophic bacteria, filamentous fungi, cellulolytic and proteolytic bacteria and fungi were stimulated in abundance, in quantity and in proteolytic and cellulolytic activities in response to land application of municipal and industrial sludge and wastewater [107,131e135]. These effects were still noticeable several years after land application [135,136]. Nevertheless, sludge polluted with Cu (Cu doses from 12 to 226 mg kg1) were toxic from 137 mg kg1 for mycorrhizae and toxic whatever the Cu content for other soil microorganisms [54]. Soil respiration was also stimulated by the spreading of paper mill sludge and pig manure [81,137]. Willows did not improve the leaching of the Salmonella typhimurium bacteriophage present in wastewaters, which was retained at the rhizosphere level [138]. The phage was diffusing much faster in clay soil than in sandy soils. The land application of secondary treated effluents from WWTP in an eucalyptus plantation stimulated the abundance of protozoa and alters the species composition of all groups of protozoa and nematodes. Large (superior to 50 mm) amoebae and ciliates were observed in soils that received these effluents [139]. In willow SRC, the application of biochar induced an increase of soil bacterial biomass, with an increase of the Gram-negative bacteria and actinobacteria [140]. The predaceous Mesostigmatid mites benefited from application of sludge, while the mycophagous Oribatida were most adversely affected by this treatment. Composted chicken manure highly stimulated populations of both groups in abundance and diversity [141]. On the other hand, the performance of the Chrysomela scripta beetle, leaf pest of poplar, was negatively affected by wastewater [142]. Willow SRC fertilized with sewage sludge has a wider range of herbaceous weed species (higher ShannoneWiener diversity index and stronger uniformity index) than SRC plantation having

386

N. Marron / Biomass and Bioenergy 81 (2015) 378e400

not received land application [143]. 3. Environmental contamination due to the land application of residues in short-rotation tree plantations 3.1. Soil and water contamination The presence of heavy metals in the soil following the spreading of sewage sludge, wastewater, compost, manure, or ash has been shown by numerous studies, mainly in the upper soil horizons [74,127,144e147]. Cu and Zn were mostly accumulated (þ26% and þ37% on average, respectively; Fig. 8). Very diverse responses have been observed in the literature due to the extreme diversity of the applied residues (Fig. 8). However, all studies were unanimous on the fact that the levels found (1) were under the limit of the regulatory pollution thresholds (thresholds of the different countries where the experiments were carried out; [30,146,147]), (2) did not present a risk for the environment [148,149] or health [145], and (3) were not leached to deep soil horizons or into groundwater [150,151] even for the application of high doses of sludge (up to 625 Mg ha1; [123]). These low risks identified in short-rotation plantations were linked to the fact that willows, poplars, and eucalyptus were able to efficiently extract most soluble/exchangeable metals (Cd, Ni, and Zn) present in the sludge or manure and, to a lesser extent Cr, Pb, Hg, and Cu [38,74,76,146,152e155] (Fig. 8). Willow absorbed more heavy metals than poplar because of its more developed root system [156,157]. Furthermore, the different willow genotypes and species were more or less specific to one or more metals [158,159]. Adding a chelating agent (EDTA, ethylene diamine tetra acetic acid) did not affect the uptake of heavy metals by poplar, both

Fig. 8. Relative soil heavy metals variations (%) reported in literature in response to residue applications as compared to unfertilized controls in Populus, Salix, and Eucalyptus. Genus and residues are pooled. Heavy metal contents in the upper soil layer were used. Each box represents the quartile below (Q1) and above (Q3) the median value. Vertical bars represent minimum and maximum values except for individuals that are away 1.5 times from the top of the interquartile (Q3eQ1) range. The numbers of values and papers used for the calculation, and the general means ± standard deviations are indicated.

essential (Cu, Fe, Mn, Zn) and non-essential (Cd, Ni, Pb), in the soil after the application of sewage sludge [152]. It has to be noted that the studies about the polluting potential of residues are often short-term studies without repeated applications and/or without large doses. Other undesirable elements were observed in the soil after application of sludge in short-rotation plantations such as sulfides [150], bromides [160], and polycyclic aromatic hydrocarbons (PAH ¼ naphthalene, phenanthrene, acenaphthalene) [161,162]. Nevertheless, these elements were not leached and their levels in soils decreased with time. Willows and poplars were much more efficient to absorb them than the various cereals tested [160,163,164]. Due to the high evapotranspiration of willows, very large amounts of wastewater could be used without risk of pollution of the water table. Sludge application corresponding to N dose of 300 kg ha1 and P dose of 220 kg ha1 did not cause groundwater pollution [15]. However, it was also observed that when the willows were very productive and showed a high transpiration, dissipation of hydrocarbons was lower than in the absence of plant. This could be due to competition for nutrients between the willows and soil microorganisms that may have hindered the microbial degradation of hydrocarbons in the rhizosphere of the most productive plants [165]. The application of dairy manure (including urine, feces, and chemicals used to clean the areas of stalling and milking) caused the accumulation of chlorides which could have adverse effects [79]. A linear relationship was also found between the rate of spread sludge and the chemical oxygen demand (used as an indicator of the pollution load of the water table), suggesting the existence of a risk of the sludge application especially for doses superior to 50 MgDW ha1 [166]. In China, wastewater treatment systems planted with willow nevertheless allowed a 96% reduction of the chemical oxygen demand [167]. The spreading of sludge, wastewater, manure, or industrial effluents often caused an increase of the nitrate levels in the soil, due to a stimulation of ammonium nitrification [48,81,168]. On average, in literature, an increase by 140% in soil nitrates and by 299% in the nitrification rate have been observed in response to residue application (Fig. 7). In some cases, a nitrate leaching to the water table or into deeper soil layers was observed [62,74,166]; this leaching was nevertheless lower for willow SRC than for cereals or grasslands [169]. The risk of nitrate leaching could be reduced (1) when the root system of the tree species (willow/poplar) was well established (almost no nitrates were found in drainage water following wastewater and sludge spreading; [64,160]), (2) using a medium dose of dried sludge granules (N dose of about 100 kg ha1; [148,149]), (3) according to the nature of the soil (after wastewater spreading in willow SRC, nitrate leaching was about 70 kg ha1 in a clay soil and 90 kg ha1 in a sandy soil; [62]), and (4) as a function of time (nitrification was reduced in the years following application [74,135,137,166]). In the case of pig manure application in SRC, increases in nitrate (and ammonium) levels were visible from the first months after spreading, while in the case of paper mill sludge application, the effect was visible at the end of the growing season only [170]. Compared with herbaceous species (including reed canary grass), willow used primarily the ammonium present in the sludge and thus was less effective in preventing the risk of nitrate leakage [153]. This is, however, inconsistent with the observations in Ref. [171] stating that woody species, including willow, absorbed nitrates more efficiently than herbaceous species, while ammonium was more efficiently absorbed by the association of herbaceous and woody species. Enhanced denitrification after effluent spreading has also been observed. Nitrogen losses by denitrification were estimated to be between 42 and 78 kg ha1 for a coppiced eucalyptus plantation and between 17 and 64 kg ha1 for an uncoppiced plantation

N. Marron / Biomass and Bioenergy 81 (2015) 378e400

irrigated with municipal effluents. These rates were much higher than in the case of a conventional irrigation [172]. Willow is known for its high capacity to filter nitrogen, favoring denitrification at the root level [3]. The spreading of sludge and municipal wastewater also induced an increase in ammonium levels in soil, but no leaching and no stimulation of ammonification, often with rather an inhibition of that process and a stimulation of nitrification [62,81,131,135,168,173]. On average, ammonification is reduced by 27% in literature in response to residue application (Fig. 7). These effects were still noticeable even four years after effluent application [136]. Only few studies have described the impact of effluent spreading on soil phosphates. Nevertheless, it has been shown that the spreading of wastewater from diverse origins induced an increase in phosphate levels and in the activity of alkaline phosphatase (not in the activity of acid phosphatase) in plantations of willow and poplar [134,153,168,174]. In contrast, in response to a spreading of limed or anaerobically digested sludge, orthophosphates as well as total phosphates were weakly leached and in a similar way as compared to a conventional phosphorous fertilization [175]. The authors concluded that, for this type of effluent, phosphate mobility should not be a risk for the quality of groundwater. Finally, the spreading of pig manure did not cause significant changes in concentrations of soil phosphate in a poplar SRC plantation [77]. Sludge or wastewater could also be vector of infection by pathogens. It has been observed in plantations of eucalyptus that the accumulation of fecal coliforms after a composted sludge application was substantial when the leaching is low [123]. On the other hand, poplars and willows allowed an almost complete disinfection (99.9%) of fecal bacteria in wastewaters [176]. It was also shown that fecal bacteria were not washed out even with copious irrigation with effluent from oxidation ponds and residence times inferior to one day [177]. Effluent application may also have an indirect effect on infestation by leaf pathogens: it has, for example, been shown that the spreading of wastewater changed the microclimate and increased the density of the canopy in willow plantations, which consequently decreased biomass production due to the increased impact of leaf rust (Melampsora epitea) [178,179]. Moreover, the impact of the canopy density on the abundance of rust was willow clone-specific [178]. 3.2. Atmospheric emissions In terms of harmful emissions to the atmosphere in short rotation plantations receiving residues, the scientific literature is very scarce. It was observed that the emission of nitrogen oxides (NOx) during combustion of wood from willows fertilized with compost from municipal sludge was only slightly (0.2%) influenced by the type of fertilization. The combustion temperature, age of wood, the interaction between these factors, and the harvest date were the main factors of influence [180]. 4. Conclusion The spreading of most residues causes an enrichment of the soil in nutrients (mainly N and P in the case of organic residues or other nutrients such as Ca and Mg in the case of inorganic residues like ashes) and a subsequent increase in the growth of plants. Manure, compost, sewage sludge, and wastewater seem most effective in stimulating growth. Ashes have less impact on growth (Table 1). Few negative effects on the plant have been highlighted in response to spreading, except in the case of very rich effluents in salt in response to which growth reduction and leaf loss nevertheless did not lead to plant death [67]. The high transpiration potentials of the

387

fast growing species dedicated to intensive tree plantations (compared to other tree species) allow them to absorb and tolerate, without major damages, nutrients in excess, most heavy metals, as well as antibiotics [85,123]. Some studies have shown heavy metal accumulation in soils following the spreading of residues, but few of them showed leaching or water pollution [151] (Table 1). Nevertheless, the used doses and the intervals between applications were of primary importance to avoid leakage of undesirable elements in the environment. Based on simulations associated with a review of the literature [181], it has been estimated that the contribution of sludge in forest should not exceed N dose of 0.4 Mg ha1 every three years during the growing season to avoid contamination of groundwater and surface water [181]. Studies dealing with the subject have rarely highlighted N leak, most of which was absorbed by plants [182,183]. Most studies, however, admit to not having the necessary long term perspective to conclude clearly, and they often suggest that a longer monitoring or additional experiments are needed. A rough analysis of the tendency of the findings of the articles shows that nearly two thirds of the studies observed increases in plant growth and soil enrichment in nutrients in response to the spreading (Appendix 1, Table 1). About ten percent of the studies showed the same type of positive effects of spreading, but moderated their conclusions by indicating doses to not exceed or instructions to follow in order to that spreading becomes not toxic or dangerous to the environment. Fifteen percent of the studies did not show a significant effect of spreading on the physiology of the plant or an improvement of the nutritional status of the soil (ash and compost are well represented in this category). Finally, 14% of studies have shown contamination effects of land application for the plant or the environment. For the latter, it should be noted that this is, in general, in studies about the application of industrial and/ or highly polluted effluents.

Acknowledgments This review work was done under the framework of the French scientific collective expertise (ESCo) about “the impacts of land applications of residues” coordinated by CNRS, INRA, and Irstea for the French Ministries of Agriculture and Ecology (2013e2014). Within the framework of this expertise, I would like to thank Sabine €lle Pons (CNRS Nancy), Houot (INRA Versailles-Grignon), Marie-Noe Marilys Pradel (Irstea Clermont-Ferrand), Anaïs Tibi (INRA Paris), Marc-Antoine Caillaud (INRA Paris), and Laurent Augusto (INRA Bordeaux-Aquitaine) for their comments on early versions of this manuscript. The Research Unit “Forest Ecology and Ecophysiology” (UMR 1137 EEF) is supported by the French National Research Agency through the Laboratory of Excellence ARBRE (ANR-11LABX-0002-01).

Appendix 1. Review of literature on residue applications in short-rotation plantations, and more globally on willow, poplar, and eucalyptus. For each study, country where the experiment was done, plant material, residue used, dose applied (when clearly indicated in the article), main study objects of the paper, and global effect of the application (þ, positive effect; ¡, negative effect; ¼, no effect; þ/¡, uncertain effect), are indicated. References used for the quantitative analysis calculations are indicated with asterisks (presented on Figs. 5e8).

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N. Marron / Biomass and Bioenergy 81 (2015) 378e400

Residues

Plant material

Applied dose

Antibiotics Sulfadiazine

Salix fragilis

10 and 200 mg kg1 Plant composition

Sulfonamide

Salix fragilis

0.01, 0.1, 1, 10 mg L1

Sulfadimethoxine Trimethoprim

Salix fragilis Salix

ASH Ash Ash Ash Ash

Ash Ash Ash

Italy/ Germany Italy

[85]

Italy Czech Republic/ Denmark

[84] [86]

*

2012 2010

Leaf abscission Germination Plant growth

¼ e

1984 1997 2002

Australia

[184] [102] [185]

*

þ

2004

USA

[105]

*

¼

2005

USA

[106]

*

¼ þ

1998 1998

Spain Finland

[104] [107]

*

þ

2009

India

[111]

*

þ/

1996

Australia

[103]

¼

2003

USA

[108]

*

þ þ þ þ

2004 2008 2004 2008

USA China Chile Brazil

[109] [112] [186] [187]

* *

Carbon sequestration Plant growth and þ composition þ Plant growth, Soil composition, Biodiversity Soil composition and biodiversity

2013 2014

Israel USA

[115] [113]

2015

Australia

[114]

2014

UnitedKingdom

[140]

Plant growth and germination Root Plant growth

þ

1998

Australia

[91]

¼

1999 2007

Germany

[89] [188]

e

2008

Hungary

[147]

Populus deltoides
P. trichocarpa Salix 50 Mg ha1 Salix viminalis

Soil composition, Phytoextraction Leaching Plant growth Plant growth

þ

2011 2014 2009

France Hungary Poland

[189] [190] [32]

Salix

NOx emissions

2011

Poland

[180]

Poland Poland Poland Brazil

[20] [33] [34] [191]

Populus Eucalyptus Eucalyptus tereticornis, Acacia auriculiformis Short-rotation willow coppice, S. purpurea Short-rotation willow coppice, S. purpurea Eucalyptus globulus Short-rotation willow coppice, S.
dasyclados

10 and 20 Mg ha1 year1 (3 years) 10 and 20 Mg ha1 year1 (3 years) 0.5e5 g L1 10 to 640 Mg ha1

Ash, Sewage sludge Ash, Sewage sludge Ash, Sludge Ash, Sludge Biochar Biochar Biochar

Short-rotation poplar Populus Eucalyptus globulus, Pinus radiata Eucalyptus

Biochar

0, 1, 3, 6 Mg ha1 Eucalyptus camaldulensis, E. microcarpa, E. obliqua, E. ovata, E. viminalis Short-rotation willow coppice, 0.5 or 2% S. viminalis

Compost of post-use wood waste Compost of municipal solid waste Compost, wood chips

2012

þ

Populus deltoides

Compost Compost Compost from municipal sediments Compost from municipal sewage sludge Compost from sewage sludge Compost from sewage sludge Compost from sewage sludge Compost from urban waste and from agro-industrial residue Compost leachate

þ

2014

Ash, Paper mill sludge

Compost

Reference Used for the quantitative analysis

þ/

Populus deltoides

Compost Bracken mulch, Bracken compost Compost Compost

Global Year Country effect published

Plant composition, Phytoextraction Plant composition

Ash, Distillery waste, Farmyard manure Ash, Harvest residues

Biochar

Study objects

Eucalyptus obliqua

N dose: 100 kg ha1

Bioenergy plantations Populus nigra
P. maximowiczii 0, 25%

Eucalyptus fastigata, Leptospermum polygalifolium Salix purpurea Populus spp., Salix viminalis, Robinia pseudoacacia Short-rotation willow coppice

Salix Salix Salix Eucalyptus grandis

Robinia pseudoacacia, Populus spp., Fraxinus pennsylvatica Salix purpurea

N dose: 100 kg ha1

10 Mg ha1

25, 75, 100%

0, 10, 25, 50%

Salix viminalis, Eucalyptus nitens N dose: 250 to 10 000 kg ha1 Salix

Soil and plant composition, Plant growth Plant growth, Soil composition Germination Plant composition and growth, Soil composition Plant growth, Mortality Plant growth, germination and mortality Plant composition and growth Plant growth Soil composition Plant growth Energy balance

[87]

growth growth growth growth

¼

þ

2011 2010 2010 2014

Plant growth

þ

2012

Plant growth

þ

2008

Poland

[92]

Plant growth, Phytoextraction Plant growth, germination and mortality

þ/

2014

[192]

þ

2007

UnitedKingdom Finland

Plant Plant Plant Plant

[95]

[93]

*

*

*

N. Marron / Biomass and Bioenergy 81 (2015) 378e400

389

(continued ) Residues

Plant material

Composted anaerobic biosolids Composted biosolids

Eucalyptus viminalis Populus deltoides
P. nigra

Salix geyeriana, Alnus incana, S. drummondiana Composted biosolids, Digested Salix miyabeana, S. purpurea dairy manure Composted sewage sludge Salix Composted sludge Short-rotation willow coppice Manure compost Populus Municipal solid waste Populus deltoides, E. amplifolia, compost Eucalyptus grandis Olive mill waste Populus
euramericana, P.
generosa
P. nigra Sewage sludge compost, Salix Sawdust Slurry compost Populus alba
glandulosa

Applied dose

Fe dose: 420 mg kg1

Composted biosolids

Manure Cattle manure Cattle manure Dairy effluent (urine, faeces)

N dose: 150 and 200 kg ha1 N dose: 300 kg ha1 N dose: 100 kg ha1 10e20 kg per tree

80 m3 ha1 year1

0 to 40 Mg ha1 50 Mg ha1 N dose: 0 e558 kg ha1 Salix viminalis, Eucalyptus nitens 150e300 m3 ha1 Salix viminalis N dose: 5 g L1

Eucalyptus citriodora Short-rotation poplar coppice Salix kinuyanagi

Short-rotation willow coppice Short-rotation poplar coppice

N dose: 100 kg ha1 N dose: 0 e80 kg ha1

Liquid swine manure Livestock lagoon wastewater

Populus Populus deltoides

30e40 Mg ha1 25 mm per week

Manure, Coconut bark powder Organic manure, Ash Organic manure, Rice straw Pig slurry Tanned cattle manure, Green residues Industrial effluents Brick air scrubber by-product

Eucalyptus urophylla exotic Eucalyptus Salix viminalis Salix Eucalyptus grandis

Contamined dredged harbor sludge, Tributyltin Contamined dredged sediments Dredged sediment contaminated by heavy metals High salinity tailings waters High salinity tailings waters

Salix

30e120 m3 ha1

Populus trichocarpa
P. deltoides, N dose: P. deltoides
P. nigra 1100 mg kg1

Plant growth and nutrition Leaf chlorosis Plant growth, Phytoextraction Plant growth, Soil composition Plant growth Plant growth Plant growth Plant growth

2002

Brazil

[18]

2010

USA

[193]

2012

USA

[194]

¼

2013

USA

[195]

*

þ ¼ þ þ

2013 2003 2011 2012

Estonia Canada Canada USA

[13] [22] [88] [90]

* * *

2012

Italy

[196]

2009

Russia

[197]

2012

Korea

[76]

2011 2012 2012

Brazil [75] Italy [198] New Zealand [79]

þ þ/

2002 2014

Estonia

[80] [78]

*

þ

2012 2012

Canada Canada

[199] [ [77]]

*

¼ þ

2009 2008

Canada USA

[200] [168]

*

þ þ þ e þ

2011 2000 2004 2011 2008

Brazil Nigeria Canada Brazil

[201] [202] [203] [74] [204]

e

2007

USA

[56]

þ

2004

Denmark

[55]

2008

USA

[165]

Transpiration

Plant growth Life cycle analysis Plant composition and growth, Transpiration Plant growth, Root Plant growth and mortality Soil composition Plant growth and nutrition, Soil composition Water quality Plant growth, Soil composition Plant growth, Root Plant growth Plant growth Plant growth

Reference Used for the quantitative analysis

þ

*

*

*

*

*

*

Salix nigra

Plant growth, germination and physiology Plant growth and transpiration Phytoextraction

Salix fragilis
S. alba

Plant physiology

þ/

2014

Mortality Plant composition

þ/ þ/

1998 1999

Canada Canada

[58] [59]

Plant growth

e

1998

India

[57]

2011

Australia

[48]

þ

2010

Pakistan

[72]

*

þ/

2004

Italy

[53]

*

þ/ þ

2006 2006 2004

Portugal Italy Italy

[206] [49] [50]

* *

þ/

2008

Canada

[45]

*

¼

2009

Serbia

[47]

*

Salix, Populus Populus tremuloides, P. deltoides
P. balsamifera, Pinus banksiana, Picea glauca High sulfate content pesticide Eucalyptus globulus effluent Industrial effluent from food Eucalyptus moluccana, E. processing factory tereticornis Industrial effluent of the Eucalyptus camaldulensis Hudiara drain, Wastewater Industrial organic waste, Populus Sewage sludge deltoides
P. maximowiczii, P.
euramericana Industrial waste Eucalyptus globulus Industrial waste Populus
euramericana Industrial waste Populus

Lignite washery sludge

Global Year Country effect published

þ 200e1200 Mg ha1 Soil composition, Phytoextraction Plant physiology and e transpiration

Dairy farm pond effluent Digestate from pig slurry anaerobic digestion Green manure Hog manure

Kraft pulp mill effluent

Study objects

Populus deltoides
P. petrowskyana Populus

Mortality

63%

Plant growth and composition Plant growth and composition

Carbon sequestration 4.8, 9.6, 19.2 kg m2 Plant composition 63% Plant growth and physiology 6 to 9 mm per day Plant growth, Soil composition Plant growth, Soil 0 to 112 Mg ha1 composition

[205]

*

(continued on next page)

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N. Marron / Biomass and Bioenergy 81 (2015) 378e400

(continued ) Residues

Plant material

Applied dose

Meatworks effluent

Eucalyptus globulus

N dose: 0.28e1.12 g Plant growth, Nutrient uptake, per pot Soil composition

Munitions waste Populus Paper mill biosolids, Pig slurry Populus

Paper mill biosolids, Pig slurry Short-rotation poplar coppice Paper sludge

Populus deltoides

Study objects

N dose: 70 kg ha1

N dose: 65 e140 kg ha1 0 to 80% 1

Paper sludge, Manure

Populus, Pinus

Sewage sludge

Eucalyptus

10, 20, 40 Mg ha1

Reference Used for the quantitative analysis

Plant growth, Soil microorganisms, Soil composition Soil nutrient budget

þ

1997 2007

USA Canada

[207] [81]

*

þ

2010

Canada

[170]

*

Plant growth and composition Plant growth and composition Phytoextraction Soil composition Plant growth

þ/

2006

Canada

[42]

*

¼

2011

USA

[41]

*

þ þ þ

2013 2004 2009

USA Canada Canada

[208] [209] [44]

*

e

1998

Australia

[67]

þ

2011

India

[154]

þ

2007

Italy

[210]

þ/

2014

Brazil

[211]

2015

Poland

[212]

þ/

2010

Brazil

[43]

þ

2014

Pakistan

[213]

þ

2000

USA

[122]

e

2001

Finland

[130]

2013

Brazil

[214]

2011

Brazil

[52]

2007 2007

Poland Poland

[100] [101]

¼ þ ¼

2012 2012 2010 2010 2011 2009 2010

Poland Poland UK UK USA USA Slovenia

[215] [216] [217] [218] [98] [99] [94]

*

e

2010

Slovenia

[129]

*

þ

2011

þ

2013

Australia

[219]

þ

2003

USA

[19]

þ/

2014

Ireland

[220]

þ

1991

Hungary

[17]

e ¼

2010 2012

[221] [222]

1984

Poland Germany, Estonia, Poland USA

[223]

2005

Brazil

[119]

Short-rotation willow coppice, N dose: 100 kg ha S. dasyclados Paper mill sludge, Ash Populus
canadensis Pulp and paper mill biosolids Short-rotation tree species Pulp mill wastewater Populus 1.5e6 mm per day deltoides
P. petrowskyana Salt-enhanced effluent Eucalyptus grandis, Pinus radiata Salt dose: 9 Mg ha1 Plant growth, physiology, and composition Tannery sludge Populus alba, Eucalyptus Plant growth and tereticornis composition Tannery waste Salix alba 150e300 g Plant growth, Phytoextraction Tannery sludge containing Eucalyptus urophylla 0 to 6 g dm3 Plant growth, Soil chromium composition Tannery waste containing Populus
canescens Plant composition, chromium Antioxidants Plant growth Treated bleached kraft pulp Eucalyptus Na dose: mill effluent 6.49 Mg ha1 Textile effluent Eucalyptus camaldulensis Plant growth, Phytoextraction Uncomposted de-watered Populus spp. 5 to 14% Soil composition pulp sludge Waste paper slurry, Sheet Populus tremula, Betula pendula, Weed control mulch, Wood fiber slurry Picea abies Eucalyptus saligna Plant growth and Waste lime sludge from the composition, Soil production of bleached composition kraft paper Zinc industry waste Salix humboldtiana Phytoextraction Landfill leachate Landfill leachate Salix amygdalina 1 to 5 mm per day Transpiration Landfill leachate Salix amygdalina 1 to 5 mm per day Plant growth and transpiration Landfill leachate Salix N removal Landfill leachate Salix N removal Landfill leachate Salix Root Landfill leachate Salix Soil composition Landfill leachate Populus Root Landfill leachate Populus Root Landfill leachate, Compost Populus deltoides, Salix viminalis, Plant growth from wastewater S. purpurea Landfill leachate, Compost Populus deltoides Soil composition wastewater Vermicompost leachate Eucalyptus dunnii, E. nitens, E. Plant growth and smithii germination Sewage sludge/biosolids Heavy metal-contaminated Eucalyptus polybractea, E. Phytoextraction, Plant sludge cladocalyx growth and mortality Plant growth, Soil Lime stabilized sewage sludge, Salix 69.3 Mg ha1 composition (manure)/ Composted poultry manure 1 129.5 Mg ha (sludge) Water quality Municipal sludge, Distillery Salix viminalis, S. schwerinii P dose: 0, 7.5, effluent 15 Mg ha1 Municipal and industrial Salix eriocephala, S. lucida, S. Plant growth, sludge exigua Nutrient uptake 1 Phytoextraction Municipal sewage sludge Short-rotation willow coppice 10 Mg ha Municipal sewage sludge Salix P dose: 60 Soil organic matter 1 e120 kg ha Municipal sewage sludge

Global Year Country effect published

Plant growth and composition Soil organic matter, Soil composition

þ

¼

[96]

*

*

*

N. Marron / Biomass and Bioenergy 81 (2015) 378e400

391

(continued ) Residues

Plant material

Sewage sludge

Salix geyeriana, Salix monticola

Sewage Sewage Sewage Sewage

Populus spp. Eucalyptus Populus
euramericana Salix
reichardtii, Populus balsamifera Populus deltoides
P. yunnanensis

sludge sludge sludge sludge

Sewage sludge

Sewage Sewage Sewage Sewage Sewage

sludge sludge sludge sludge sludge

Populus Salix matsudana, S.
reichardtii Populus deltoides
P. nigra Populus deltoides
P. nigra Eucalyptus cladocalyx

Sewage sludge Sewage sludge

Short-rotation coppice Eucalyptus grandis

Sewage Sewage Sewage Sewage Sewage

Populus
euramericana Populus Salix Eucalyptus globulus Eucalyptus globulus

sludge sludge sludge sludge sludge

Sewage sludge

Eucalyptus grandis

Sewage sludge Sewage sludge Sewage sludge

Salix viminalis Eucalyptus Salix

Sewage sludge

Eucalyptus grandis

Sewage Sewage Sewage Sewage

Eucalyptus Eucalyptus Eucalyptus Eucalyptus

sludge sludge sludge sludge

citriodora citriodora grandis globulus

Sewage sludge Sewage sludge

Salix viminalis Salix

Sewage Sewage Sewage Sewage

Salix Salix Energy crop Eucalyptus grandis

sludge sludge sludge sludge

Applied dose

Study objects

380 Mg ha1 0 to 100 Mg ha1

Plant growth, Phytoextraction Plant growth Plant growth Soil organic matter Phytoextraction, pH

þ þ e þ

2008 2010 1999 2008

USA

Australia

[225] [24] [121] [157]

*

[54]

þ þ/

USA

þ þ

2011 2012 2003 2011 2012

USA USA Australia

[175] [155] [152] [11] [12]

0 to 40 Mg ha1

Plant growth, Soil composition Soil composition 0 to 13 Mg ha1 Soil composition 0 to 450 Mg ha1 Water quality 0 to 8% Plant growth 1 0 to 80 g kg Plant growth, Soil composition 1 Plant growth and 0 to 40 Mg ha composition 60 cm sludge depth Phytoextraction

þ

1998 2004

UK Brazil

[226] [10]

1999 1999 2008 2009 2009

USA USA Chile Chile

[125] [124] [166] [25] [26]

þ

2007

Brazil

[29]

þ

60e120 mm, 10 times per year 10 to 30 Mg ha1

Soil composition

þ

2001 2003 2012

Poland Zimbabwe Poland

[227] [228] [229]

Plant growth and composition Soil composition Soil composition Soil composition Soil composition, Soil organic matter Wood quality Biodiversity, Soil composition Soil composition Biodiversity Life cycle analysis Soil composition, Plant nutrition Plant growth Plant composition, Phytoextraction Life cycle analysis Removal characteristics Microbiological activity Microbiological activity Plant growth Plant growth Sludge composition Biodiversity Plant growth

þ

2008

Brazil

[230]

þ þ þ e

2008 2011 2008 2010

Brazil Brazil Brazil Spain

[231] [117] [14] [127]

þ/

2011 2009

Poland Poland

[27] [132]

þ

2007 2007 2011 2006

Poland Poland UK Brazil

[137] [131] [232] [120]

¼

1988 1999

France Sweden

[233] [234]

þ þ

2003 2010

USA

[235] [236]

þ

2008

Poland

[136]

*

þ

2010

Poland

[135]

*

þ þ ¼ þ e ¼ ¼ ¼

2009 2000 2007 2009 2007 2004 2007 2001

Poland Germany Poland Poland Latvia China UK UK

[40] [237] [238] [133] [30] [9] [239] [61]

*

*

þ

2011

Spain

[39]

*

2010 2001

UK

[153] [240]

30 or 60 Mg ha1 30 or 60 Mg ha1 10 to 40 Mg ha1

30 to 600 Mg ha1 30 to 600 Mg ha1 30 to 600 Mg ha1 10 to 160 Mg ha1

Sewage sludge

Salix viminalis

30 to 600 Mg ha1

Sewage sludge

Salix viminalis

30 to 600 Mg ha1

Sewage Sewage Sewage Sewage Sewage Sewage Sewage Sewage

Salix Populus deltoides Salix viminalis Salix viminalis Short-rotation willow coppice Eucalyptus paniculata Short-rotation willow coppice Short-rotation poplar coppice

20e30% 30%

Salix Short-rotation willow poplar coppice

[224]

Australia

Salix Salix babylonica

Sewage sludge Sewage sludge

USA

2010

Sewage sludge Sewage sludge

Populus canadensis

2009

e

Populus Short-rotation willow coppice

Sewage sludge

Reference Used for the quantitative analysis

Cu dose: 12 Biodiversity, e226 mg kg1 Mycorrhiza Zn dose: 25 1 e686 mg kg 213 to 656 Mg ha1 Leaching Phytoextraction Nutrient uptake 22.7 or 44.5 Mg ha1 Soil composition 100 or 500 Mg ha1 Plant growth, Soil composition

Sewage sludge Sewage sludge

sludge sludge sludge sludge sludge sludge sludge sludge

Global Year Country effect published

2.5e20 Mg ha1 year1

Phytoextraction 100 m3 ha1 year1 Plant growth, Phytoextraction Plant growth, Soil N dose: 0, 200, 1 1 composition 400 kg ha year (2 years) Leaching Plant growth

e þ

* *

* *

*

*

* * * *

*

(continued on next page)

392

N. Marron / Biomass and Bioenergy 81 (2015) 378e400

(continued ) Residues

Plant material

Applied dose

Study objects

Global Year Country effect published

Reference Used for the quantitative analysis

Sewage sludge

Salix

0 to 600 Mg ha1

þ

Sewage sludge

Salix

0 to 600 Mg ha1

Polycyclic aromatic hydrocarbons Polycyclic aromatic hydrocarbons Polycyclic aromatic hydrocarbons Plant growth and mortality, Phytoextraction Water quality, Plant composition Plant composition, Wood quality Soil composition Bromide leaching Biodiversity Biodiversity Plant and soil composition Plant composition Plant growth, Leaching Plant growth, Phytoextraction Plant growth and nutrition, Leaching Plant growth, Wood quality Plant growth, Phytoextraction Plant growth and composition Plant growth

Sewage sludge

Salix viminalis

Sewage sludge

Salix

Sewage sludge

Salix viminalis, Populus canadensis Eucalyptus grandis

Sewage sludge

1

0 to 600 Mg ha

Sewage sludge Sewage sludge

Salix 10 to 200 Mg ha1 Salix, Populus Short-rotation willow coppice 20 Mg ha1 Short-rotation willow coppice Robinia pseudoacacia, Populus
albus, P.
canescens Populus tremula
P. tremuloides Short-rotation willow coppice N dose: 150 kg ha1

Sewage sludge

Salix discolor, S. viminalis

Sewage sludge

Short-rotation willow coppice

Sewage sludge Sewage sludge

Salix discolor, S. viminalis, S. petiolaris Populus
euramericana

N dose: 0 e200 kg ha1 N dose: 0 e300 kg ha1 N dose: 0 e300 kg ha1 10e20%

Sewage sludge

Eucalyptus grandis

15 Mg ha1

Sewage sludge

Short-rotation willow coppice

18.3, 20.1, 20.6 Mg ha1

Sewage sludge Sewage sludge Sewage sludge

Salix
reichardtii Short-rotation willow coppice Short-rotation willow coppice, Salix viminalis

Sewage sluge

Salix viminalis

Sewage sludge, Ash

Short-rotation willow coppice

Sewage sludge, Ash Sewage sludge, Ash

Salix viminalis Salix viminalis, Betula pendula, Pinus sylvestris Salix viminalis Short-rotation willow coppice

Sewage Sewage Sewage Sewage Sewage

sludge sludge sludge sludge sludge

Sewage sludge, Ash Sewage sludge, Chicken manure, Compost Sewage sludge, Compost Sewage sludge, Composted poultry manure Sewage sludge, Distillery effluent Sewage sludge, Lime

2006

Poland

[164]

2005

Poland

[163]

2005

Poland

[161]

þ

2002

UK

[35]

e

2004

Poland

[156]

þ

2009

Brazil

[28]

þ

2009 2006 2011 2012 2008

New Zealand Poland Poland Hungary

[162] [160] [143] [241] [242]

þ þ

2003 2001

Sweden Canada

[243] [149]

*

þ

1995

Canada

[38]

*

þ/

1998

Canada

[148]

*

1997

Canada

[31]

*

2003

Greece

[145]

*

þ/

2014

Brazil

[244]

¼

2014

[245]

*

þ/ þ/ þ

2015 2014 2013

Estonia/ Germany/ Poland Australia Ireland Canada

[246] [247] [248]

*

2014

Poland

[249]

¼

2012

Sweden

[169]

þ/ þ/

2010 2009

Poland

[250] [110]

2008 2004

Sweden USA

[251] [141]

*

þ

Plant growth

2005

Australia

[23]

*

N mineralization

2003

USA

[21]

* *

Phytoextraction Life cycle analysis Plant growth

N dose: 362 kg ha1 in total during 3 rotations 90 Mg ha1 Plant and soil composition, Heavy metals P dose: 22 kg ha1 Water quality year1 Biodiversity, Root Plant growth 8.6e17.2 Mg ha1 N dose: 1400 kg ha1 N dose: 821 e1798 kg ha1 250 m3 ha1

Wood quality Biodiversity

P dose: 24 e48 kg ha1 N dose: 0, 160, 320 kg ha1 year1 N dose: 0, 60, 120, 240, 360 kg ha1 N dose: 0, 60, 120, 240, 360 kg ha1 N dose: 125 e187 kg ha1 4.32e8.64 Mg ha1

Water quality, Leaching Plant growth

e

2013

Ireland

[151]

þ

2008

Spain

[252]

Plant growth

¼

2014

Denmark

[253]

*

N leaching

þ/

2014

Denmark

[254]

*

Plant growth, Soil composition Nutrient uptake

e

2001

Canada

[144]

*

þ

2006

Sweden

[146]

Populus

Economy

þ

2009

Canada

[255]

Eucalyptus globulus

Plant growth, Soil composition Soil composition

þ

2014

Chile/Spain

[256]

2014

Spain

[257]

Eucalyptus botryoides, E. tereticornis, E. occidentalis Salix Short-rotation willow coppice Populus
euramericana

Sewage sludge, Manure

Short-rotation willow coppice

Sewage sludge, Manure

Short-rotation willow coppice

Sewage sludge, Tree pruning residues Sewage sludge, Woodeash mixture Treated municipal sewage sludge Sewage sludge contaminated with aluminum Sewage sludge, Paper mill residues

Salix discolor Short-rotation willow coppice

Eucalyptus globulus

N. Marron / Biomass and Bioenergy 81 (2015) 378e400

393

(continued ) Residues

Plant material

Sewage sludge, Paper mill residues Sewage sludge, Paper mill residues Sludge from wastewater treatment plant and paper mill Wastewfater Fruit and vegetable processing wastewater

Eucalyptus globulus

Secondary treated municipal effluent Secondary treated municipal effluent Secondary treated sewage water

2014

Spain

[258]

Soil composition

2013

Spain

[259]

Soil composition

2013

Spain

[260]

15.4 or 30.8 mm per Plant growth, day Phytoextraction, Soil composition Plant growth and composition

þ

2015

USA

[261]

þ

2003

India

[73]

1.5e6 mm per day

Soil composition

þ/¡

1992 2008

Canada Canada

[262] [126]

Plant growth and composition Soil composition Water quality Pathogens Economy Economy

þ

2003

India

[51]

Poland UK

þ

2011 2003 2012 1998 1997

Sweden Sweden

[174] [263] [264] [265] [266]

þ

2010

Estonia

[15]

2011

Greece

[267]

2012

Greece

[268]

2009

Greece

[71]

2011

Greece

[118]

þ

1998

Sweden

[97]

þ

2014

Brazil

[269]

-

2003

Australia

[172]

1996

Australia

[270]

*

¼

2011

India

[271]

*

þ

2009

Estonia

[134]

*

þ þ þ/¡

2010 2010 2006

¼

1998 2007 2007

Australia Australia Israel

[139] [173] [177]

Leaching, Denitrification 94 m ha day (N Phytoextraction, Plant þ dose: 2.73 mg L1) growth Plant growth, Water N dose: 10 relations e40 mg L1 Plant growth, Water quality Economy þ

1999

Australia

[272]

2012

USA

[273]

2004

Australia

[66]

2007

Chile

[63]

1999

Sweden

[60]

þ

2010

Pakistan

[69]

þ

2012

Sweden

[274]

Salix spp., Populus spp. Short-rotation willow coppice Short-rotation willow coppice Short-rotation willow coppice Short-rotation willow coppice Short-rotation willow coppice

N dose: 104 kg ha1 year1 N dose: 16.5 mg L1 Plant growth and transpiration (170 mm) e 300 kg ha1 724 mm

Eucalyptus camaldulensis, Populus nigra Eucalyptus camaldulensis, 724 mm Economy, Plant Populus nigra physiology Eucalyptus camaldulensis, Plant growth, Populus nigra Phytoextraction Eucalyptus camaldulensis, 724e1212 mm Soil composition Populus nigra, Acacia cyanophylla Short-rotation willow coppice 0e20 mm per day, 2 Plant growth, Water quality e12.5 Mg ha1

Eucalyptus grandis

Plant growth, Soil composition Denitrification

Eucalyptus globulus Eucalyptus grandis, Pinus radiata Eucalyptus tereticornis, Populus deltoides

Secondary-treated municipal Short-rotation willow coppice wastewater Sewage effluent Salix Sewage effluent Salix viminalis Sewage effluent Eucalyptus camaldulensis Sewage effluent Sewage effluent Sewage effluent (oxidation pond effluent) Sewage effluent, Bore water

Carbon sequestration

Populus deltoides
P. nigra

Populus Populus deltoides
P. petrowskyana Eucalyptus camaldulensis

Pre-treated wastewater, Sewage sludge, Methanogenic landfill leachate Reclaimed wastewater

Reference Used for the quantitative analysis

297 Mg ha

Municipal effluent Municipal effluent, Pulp mill effluent Municipal effluent, Textile effluent, Steel effluent Municipal wastewater Municipal wastewater Municipal wastewater Municipal wastewater Municipal wastewater

Pre-treated wastewater

1

Global Year Country effect published

Eucalyptus globulus

Eucalyptus camaldulensis

Pre-treated wastewater

Study objects

Eucalyptus globulus

Municipal effluent

Municipal wastewater, Composted wastewater sludge Partially treated domestic wastewater Pre-treated effluent

Applied dose

0, 25, 50, 100% of daily net evaporation potential

Biodiversity, Soil composition Phytoextraction Phytoextraction Leaching

125 and 625 Mg ha1

Eucalyptus Eucalyptus globulus Eucalyptus camaldulensis Eucalyptus grandis

Treated municipal wastewater Eucalyptus grandis, Populus deltoides, E. amplifolia Treated sewage effluent Eucalyptus robusta Treated wastewater

Eucalyptus

Untreated municipal wastewater Urban wastewater

Salix Populus deltoides

Wastewater

Salix

Plant growth, Water relations Plant growth

Biodiversity Water quality Soil organic matter

3

1

¼

¼

1

Plant growth, Nutrient uptake Plant growth

*

*

[158] [159] [123]

*

*

(continued on next page)

394

N. Marron / Biomass and Bioenergy 81 (2015) 378e400

(continued ) Residues

Plant material

Wastewater Wastewater

Salix babylonica Populus

Wastewater

Salix

160 mm per year

Wastewater

Eucalyptus camaldulensis

Wastewater

Short-rotation willow coppice, S. viminalis Populus Short-rotation willow coppice Salix Salix Short-rotation willow coppice Short-rotation willow coppice Eucalyptus Short-rotation willow poplar coppice Salix spp., Populus spp. Salix

1 to 1.36 times the month evapotranspiration 42 to 370 m3 per year

Wastewater Wastewater Wastewater Wastewater Wastewater Wastewater Wastewater Wastewater Wastewater Wastewater

Wastewater Wastewater Wastewater Wastewater Wastewater Wastewater

Short-rotation plantation Populus fremontii, Fraxinus velutina, Salix spp. Salix Salix americana Salix spp. Short-rotation willow coppice

Wastewater

Populus

Wastewater

Salix viminalis

Wastewater

Populus alba

Wastewater Wastewater

Salix nigra Eucalyptus, Salix alba, Populus deltoides

Wastewater Wastewater Wastewater Wastewater Wastewater Wastewater

Short-rotation willow coppice Eucalyptus grandis Short-rotation forestry Eucalyptus grandis Populus Short-rotation willow coppice

Wastewater

Short-rotation willow coppice

Wastewater

Populus deltoides

Wastewater

Eucalyptus tereticornis

Wastewater from swine activities, Textile residue Wastewater sewage sludge

Eucalyptus Salix, Populus, Pinus

Wastewater, Landfill leachate Short-rotation willow coppice Wastewater, Landfill leachate, Short-rotation willow coppice Sewage sludge Wastewater, Sewage sludge Wastewater, Sewage sludge Wastewater, Urine, Sewage sludge

Short-rotation willow poplar coppice Short-rotation willow coppice Salix viminalis

Applied dose

Study objects

Global Year Country effect published

Phytoextraction

2011 1978/ 1980 2010

China Hungary Estonia

[167] [275]/ [276] [277]

2002

Mexico

[278]

2002

Sweden

[279]

1997 1999 2006 2005 2000 2004 1979 2009

France Sweden Sweden Denmark Sweden Sweden Australia Canada

[142] [280] [281] [282] [138] [62] [283] [284]

2001 2001

Denmark

[176] [285]

þ þ

2007 2001

Poland USA

[286] [287]

þ þ þ þ

2007 2009 1994 2001

Poland Poland Poland Estonia

[288] [289] [116] [290]

þ

2000

USA

[291]

þ

2003

UK

[292]

2011

Spain

[128]

2008 2011

USA India

[171] [65]

2005 2006 1998 1999 2000 2010

Ireland Australia UK Australia Hungary Estonia

[293] [294] [295] [70] [296] [179]

2010

Estonia

[178]

þ/

2013

Iran

[297]

þ

2015

India

[298]

þ

2009

Brazil

[299]

þ

2007

Latvia

[150]

þ/¡

2001

Sweden

[3]

þ

1999

Sweden

[300]

-

2011

Sweden

[64]

þ

2011

Sweden

[301]

þ/¡

2008

Sweden, Ireland, France, Greece

[83]

Plant growth and physiology Plant growth

Plant growth Pathogens Economy

Bacteriophages N dose: 320 kg ha1 Leaching Phytoextraction Plant growth and mortality Phytoextraction Plant growth, Phytoextraction, Transpiration Economy Nutrient uptake Soil composition Nutrient uptake 0, 2000, 4000 mm Nutrient uptake Water quality, Plant growth 3 5 m per day Water quality, Economy Plant growth, Water quality up to 6000 mm per Water repellency year Nutrient uptake Plant growth, Phytoextraction, Nutrition Economy 180 mm ha1 year1 Root N dose: 508 kg ha1 Water relations Water quality N dose: 16.5 mg L1/ Specific Leaf Area, Leaf 180 mm per season rust Canopy density, Leaf N dose: rust 17.5 mg dm3/ 175 mm per season Plant and soil composition 9.9 m during 10 Plant growth and years physiology, Soil composition N dose: 34 g kg1, Plant growth and 0.09 mg L1 germination Plant growth, Soil 10 Mg ha1 composition Plant growth, Phytoextraction Leaching, Biodiversity, Soil composition N dose: 34.7 mg L1 Plant growth, Soil composition Plant growth, Economy Leaf rust

Reference Used for the quantitative analysis

þ

þ þ

þ

þ

-

*

*

*

*

* *

*

*

*

N. Marron / Biomass and Bioenergy 81 (2015) 378e400

395

(continued ) Residues

Plant material

Applied dose

Water contaminated with chromium Biowaste

Salix viminalis

Cr dose: 10 mg L1, Phytoextraction 0.2 L min1 Plant growth

Short-rotation willow coppice

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Study objects

Global Year Country effect published

Reference Used for the quantitative analysis

þ

2014

Italy/Greece

[302]

2010

Denmark

[303]

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