Waste Management 30 (2010) 1587–1593

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Waste Management

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Phytotoxicity of landfill leachate on willow – Salix amygdalina L.

Andrzej Bialowiec a,*, Peter F. Randerson b

a The University of Warmia and Mazury in Olsztyn, Department of Environmental Biotechnology, ul. Sloneczna 45 G, 10-900 Olsztyn, Polandb Cardiff University, Cardiff School of Biosciences, Cardiff CF10 3AX, UK

a r t i c l e i n f o a b s t r a c t

Article history:Received 15 November 2009Accepted 24 February 2010Available online 21 March 2010

0956-053X/$ - see front matter � 2010 Elsevier Ltd. Adoi:10.1016/j.wasman.2010.02.033

* Corresponding author. Tel./fax: +48 895234131.E-mail address: andrzej.bialowiec@uwm.edu.pl (A

Because of low investment and operational costs, interest is increasing in the use of willow plants in land-fill leachate disposal. Toxic effects of leachate on the plants should be avoided in the initial period ofgrowth and phytotoxicological testing may be helpful to select appropriate leachate dose rates. Theaim of this study was to determine the phytotoxicity of landfill leachate on young willow (Salix amygd-alina L.) cuttings, as a criterion for dose rate selection in the early phase of growth. Over a test period of6 weeks plants were exposed to six concentrations of landfill leachate solutions (0%; 6.25%; 12.5%; 25%;50% and 100%), under two different regimes. In regime A willow plants were cultivated in leachate solu-tion from the beginning, whereas in regime B they were grown initially in clean water for 4 weeks, afterwhich the water was exchanged for leachate solutions. The lowest effective concentration causing toxiceffects (LOEC) was calculated (p < 0.05). In regime A LOEC was between 5.44% and 6.50% of leachate con-centration, but slightly higher in regime B (5.32–6.59%). Willow plants were able to survive in landfillleachate solutions with electrical conductivity (EC) values up to 5.0 mS/cm in regime A, whereas inregime B plants were killed when EC exceeded 3.0 mS/cm. This indicates an ability of willow plants totolerate higher strengths of landfill leachate if they are cultivated in such concentrations from thebeginning.

� 2010 Elsevier Ltd. All rights reserved.

1. Introduction

Despite the varied approaches to landfill leachate disposal, anon-site treatment facility has the advantage of being easy to oper-ate, and economical in terms of cost and energy (Bulc, 2006). Ow-ing to low investment and maintenance costs, there is growinginterest in utilising willows plants in constructed wetlands (CW)for landfill leachate treatment (Kowalik et al., 1996; Jones et al.,2006), and this approach has been widely practiced in severalcountries for many years. Treatment success has varied but re-moval efficiency of organic pollutants expressed as COD, BOD,and nitrogen has not exceeded 50% (Cossu et al., 2001).

Landfill leachate may provide a source of nutrients for plantgrowth, especially nitrogen, with values in the range from 50 to5000 mg/l. However, low phosphorus concentration, usually notexceeding 6 mg/l, can act as a limiting factor in applying landfillleachate as fertilizer (Andreottola and Cannas, 1992; Ehrig, 1989;Yildiz and Unlu, 2003). Until now, the nutritional needs of plantshave been a priority in selecting a leachate dose rate, which isappropriate when the aim of the leachate disposal is biomass pro-duction. Hasselgren (1998) proposed applying landfill leachate en-riched with phosphorus compounds to fertilize willow energyforest. Lysimeter studies on the application of landfill leachate as

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. Bialowiec).

fertilizer to Salix sp. revealed that leachate had a significant posi-tive effect on the yields (Alker, 1999; Brierley et al., 2001). Theuse of different kinds of landfill leachate for irrigating short rota-tion willow plantations has been tested in Sweden (Dimitriouand Aronsson, 2003, 2005; Dimitriou et al., 2006; Hasselgren,1992), Finland (Ettala, 1992), Great Britain (Alker et al., 2003)and in Poland (Agopsowicz, 1994; Białowiec, 2005). Plants irri-gated with leachate enhance evapotranspiration of the leachate,and accumulation of the pollutants in the soil and in plant tissues.But, this technology causes the risk of ground water pollution bymigrating compounds, mostly chlorides and nitrates (Białowiecet al., 2004).

A particularly important aspect of landfill leachate disposal insoil–plant CW systems is the considerable decrease in leachate vol-ume due to evapotranspiration (Dobson and Moffat, 1995). SuchCWs are typically planted with macrophytes such as willows, pop-lars and reeds. Agopsowicz (1994) determined that evapotranspi-ration by young (3-month) willow sprouts supplied with landfillleachate was 1.6–1.8 times higher than the average precipitationrate in Poland, (about 600 mm). Białowiec et al. (2003) confirmedthat evapotranspiration by 3-month old sprouts of Salix amygdalinaL. resulted in volume reduction between 80% and 90%. The use ofsoil–plant systems for landfill leachate disposal calls for an in-formed selection of plant species and soil types. Białowiec and Ago-psowicz (2007) tested the tolerance of different willow species topollutant concentration in landfill leachate. They determined the

Fig. 1. Construction of experimental stand.

Table 2Initial properties of the landfill leachate used in the experiment.

Parameter Unit Landfill leachate solution (%)

100.0 50.0 25.0 12.5 6.25

1588 A. Bialowiec, P.F. Randerson / Waste Management 30 (2010) 1587–1593

species S. amygdalina L., Salix viminalis L., Salix purpurea to have thehighest ability for evapotranspiration and high tolerance of pollu-tant concentrations in the soil solution. In such eco-technologiesfor landfill leachate treatment, plants are exposed to leachate con-taining not only nutrients but also many toxic compounds, such asammonium, and their response may differ with soil and climaticconditions. Phytotoxicological testing offers a solution to the prob-lem of selecting the optimum leachate dose rate.

In ecological engineering, phytotoxicological tests are used insoil remediation, waste management and wastewater treatmentin addition to chemical analysis (Wilson et al., 2002) and theymay be used for landfill leachate toxicity assessment. Many studiesindicate the utility of macrophytes in toxicological tests (Barberoet al., 2001; Kirk et al., 2002; Wang, 1987; Wang and Williams,1988), and involve measuring basic parameters such as seed sur-vival (germination), biomass growth, stem and root elongation.From a technological point of view the most important period inwillow cultivation is the initial phase, when young plants are mostsensitive to changes in environmental conditions. Successfulimplementation of a soil–plant system with willow irrigated byleachate depends on an appropriate dose rate.

This study aims to determine the phytotoxicity of landfill leach-ate to willow (S. amygdalina) cuttings, as a criterion for dose rateselection in the initial phase of growth.

2. Methodology

2.1. Experimental design

The experiment was carried out in a greenhouse (mean temper-ature ± SD: 25.4 ± 6.1 �C) located at the University of Warmia andMazury, Olsztyn, Poland. The independent variable was increasingconcentrations of landfill leachate; 0% (tap water), 6.25%, 12.5%,25%, 50%, and 100%. The dependent variables were morphologicalparameters of willow described below. Plants were exposed tothe range of landfill leachate solutions with one of two differentregimes:

A – willow cuttings placed directly in landfill leachate solutions,B – willow cuttings cultivated initially in tap water for 4 weeks,

after which the water was replaced by landfill leachate solutions.Every treatment was replicated five times (Table 1).

2.2. Experimental procedure

Plastic 1.5 l bottles were marked according to symbols shown inTable 1. Willow cuttings 25–30 cm long and 0.5–1.5 cm diameterwere taken from the University’s plantation of S. amygdalina L.(Białowiec and Agopsowicz, 2007). All cuttings were taken fromone willow plant to avoid the influence of genetic diversity onthe results. One willow cutting was placed in each bottle (Fig. 1)and the 55 bottles were divided into two groups depending onthe two regimes of exposure to landfill leachate: A – 25 bottlesand B – 30 bottles. Reference bottles both for regime A and B weremarked B015. Bottles from group A were filled with landfill leachatesolutions; bottles from group B with tap water. The water level (at3=4 of the bottle height) was marked, and used as a reference levelfor topping up with water to allow for water losses due to evapo-

Table 1Regimes of plants’ exposure to landfill leachate.

Regime Number ofreplicates (n)

Landfill leachate concentration (%)

0 6.25 12.5 25 50 100

A 5 A0n A6.25n A12.5n A25n A50n A100n

B 5 B0n B6.25n B12.5n B25n B50n B100n

transpiration. Landfill leachate used in the experiment came fromthe municipal solid waste landfill in Zakurzewo near Grudziadz,Poland. Initial chemical and physical properties of landfill leachateand diluted solutions used in the experiment are shown in Table 2.

All prepared bottles with willow cuttings were placed in agreenhouse. After 4 weeks of the experiment, in group B bottles,tap water was replaced by landfill leachate solutions and theexperiment was continued for a further 2 weeks. After removalfrom the bottle, each willow plant was gently dried with a papertowel, the roots, stems and leaves were separated from the originalcuttings and separately weighed using a balance with 0.1 g accu-racy. The following dependent variables were measured for eachcutting: total weight of leaves, total weight of stems, total weightof roots, and total weight of plant (sum of leaves, roots and stems).The analysis of variance between mean values of estimated willowparameters was carried out with the use of ANOVA test (Tukey’stest) at the significance level of p < 0.05. The normality of the dis-tribution was confirmed by Shapiro–Wilk’s test, whereas thehypothesis of the homogeneity of variances across the groupswas verified by Levene’s test. Statistica 8.0 software package forstatistical procedures was used.

At the end of the experiment, the electrical conductivity (EC)[mS/cm] was measured in each bottle by a conductivity meter HI87314 Hanna-Instruments, as an indicator of total ionic concentra-tion in the residual leachate solution.

Reaction pH 8.74 8.65 8.58 8.4 8.1Electrical conductivity mS/cm 4.46 2.9 1.8 1.1 0.72COD mgO2/l 997.0 592.0 229.0 170.0 82.0Chloride mg/l 131.0 63.1 32.6 16.9 10.1Kjeldahl nitrogen mg/l 680.0 339.0 168.3 85.4 35.8Ammonia nitrogen mg/l 576.0 286.0 143.0 85.4 32.2Dissolved solids mg/l 6040 2570 1515 982 514Residue after ignition mg/l 4805 2010 1170 727 375Loss on ignition mg/l 1235 560 345 255 139

0 20 40 60 80 100landfill leachate concentration [%]

-40

-20

0

20

40

60

80

100

Inhi

bitio

n [%

]

LOEC value

Fig. 2. Example of the function curve used (Eq. (2)) for LOEC estimation. The LOECvalue corresponds to point on the X axis where % inhibition is zero.

Table 3LOEC values for measured parameters.

Parameter Exposure regime A Exposure regime B

LOEC (%) R2 LOEC (%) R2

Total leaf weight 5.49 0.996 6.59 0.985Total stem weight 5.51 0.995 6.50 0.834Total root weight 6.50 0.964 5.32 0.213Total plant weight 5.44 0.971 6.50 0.962

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2.3. Toxicity evaluation – lowest effective concentration causing atoxic effect (LOEC)

On the basis of measured parameters the inhibition effectcaused by landfill leachate solutions was calculated according toEq. (1):

I ¼ 100ðC � TÞ

Cð1Þ

where I is the effect caused by each landfill leachate solution (%), Cis the mean value of measured parameter for reference variant withtap water, and T is the mean value of measured parameter for eachlandfill leachate solution. The calculated inhibition effects (I) foreach parameter of the willow plants were examined graphicallyin relation to leachate concentrations (e.g. Fig. 2), and LOEC valueswere determined using the function:

I ¼ a1 � ExpðLOEC�a2 �CrÞ ð2Þ

where Cr is the landfill leachate solutions used in the experiment(%) & a1 and a2 are the function parameters.

Because of the complex composition of landfill leachate, in thisstudy electrical conductivity (EC) [mS/cm] was measured in eachbottle, as an indicator of total dissolved ions in the leachate. Basedon measurements of EC in leachate solutions at the end of theexperiment, the values of EC which cause necrosis of the plantswith respect to each of the measured willow parameters were esti-mated using linear regression.

3. Results

3.1. Toxic effects on willows

The ability of willow plants to adapt to leachate may be indi-cated by the lethal and sub-lethal concentrations of pollutants.Landfill leachate (LL) solutions caused strong toxic effects on wil-lows. With 100% LL concentration, the lack of plant growth in cul-tivation regime A, and complete necrosis of plant tissues in regimeB occurred. For 50% LL solution, only four plants survived in regimeA whereas in regime B all plants died. In all other concentrations ofLL where all plants survived, it was possible to collect samples ofplant tissues for measurement.

Increase in landfill leachate concentration caused similar re-sponses in all the measured parameters, i.e. decrease of totalweights of leaves, stems, roots, and total plant weight (Fig. 3).

There were no significant (p < 0.05) differences for particularparameters between willows growing with exposure regime A inconcentrations 0% and 6.25% (but a slight stimulation of growthof each of the measured plant parts can be seen). Increase of land-fill leachate in the range 6.25–25% caused progressive decrease inthe values of all measured parameters whereas further increasefrom 25% to 50% had no further influence (p < 0.05). For willowsexposed to regime B, toxic effects for the same parameters wereobserved for landfill leachate concentrations from 0% to 12.5%. In-crease of leachate concentration between 0%, 6.25% and 12.5%caused progressive decrease of mean values of total weights ofleaves, stems, roots, and total plant weight whereas further in-crease from 12.5% to 25% had no further influence (p < 0.05) onthem.

Comparison of the two cultivation regimes indicated that theeffect of toxicants on plants was greater at a lower leachate con-centration in regime B, than in regime A for all measured parame-ters. Plants growing from the beginning of the experiment onlandfill leachate were more tolerant of toxicants contained in theleachate. For low leachate concentration growth stimulation wasfound. Willows grown in regime A with LL concentration 6% hadtwo times higher (p < 0.05) total weight of plants (10.632 g) thanwillow in regime B (5.983 g). At higher LL concentrations, mea-sured parameter values were slightly higher in the case of plantsexposed to leachate with regime B than in plants from group A,but this is an effect of pre-cultivation of willows in tap water dur-ing 4 weeks before leachate solutions were applied.

3.2. LOEC

LOEC values and coefficients of determination (R2) are shown inTable 3. It appears that LOEC value, for individual parameters dif-fers slightly with cultivation regime. For the following parameters:total leaf weight, total stem weight and total plant weight, LOECvalues are slightly higher in the case of irrigation regime B, thanfor willow growing on leachate solution from the beginning ofthe experiment (Table 3). But these differences of LOEC values be-tween regimes are small and not statistically significant (p < 0.05).In regime A, LOEC values ranged from 5.44% to 6.50% but, in regimeB, LOEC values were between 5.32% and 6.59% (Table 3).

3.3. Influence of EC on willow growth

Measured values of EC were much higher in many cases, thanthose obtained for raw leachate and prepared solutions. Valuesmeasured in solution at the end of the experiment, were affectedby evapotranspiration (reduction of water volume causing increaseof solute concentrations; data to be reported elsewhere). The influ-ence of EC on measured indicators of willow growth (leaf, stem,root and plant weights) was assessed.

For all irrigation regimes and all willow parameters, similar pat-terns were observed (Fig. 4). Generally, there were negative corre-lations between EC and willow growth parameters, but thestrength of the relationship depended on the range of EC. For lowvalues (0–6.5 mS/cm for cultivation regime A and 0–3.2 mS/cm

Tota

l lea

ves

wei

ght [

g]

0 6 12 25 50 100-1012345678

0 6 12 25 50 100

Leachate exposure regime A Leachate exposure regime BTo

tal s

tem

wei

ght [

g]

0 6 12 25 50 100-101234567

0 6 12 25 50 100

Leachate exposure regime A Leachate exposure regime B

Tota

l roo

t wei

ght [

g]

0 6 12 25 50 100-0.20.00.20.40.60.81.01.21.41.61.8

0 6 12 25 50 100

Leachate exposure regime A Leachate exposure regime B

Leachate concentration [%]

Tota

l pla

nt w

eigh

t [g]

0 6 12 25 50 100-202468

10121416

0 6 12 25 50 100

Leachate exposure regime A Leachate exposure regime B

Fig. 3. Changes in total leaf weight, total stem weight, total root weight and total plant weight of Salix amygdalina (p < 0.05) in response to landfill leachate concentration andexposure regime: (A) and (B) mean values, standard deviation (whiskers) and standard error (frame).

1590 A. Bialowiec, P.F. Randerson / Waste Management 30 (2010) 1587–1593

for regime B) the slope of the line was steeply negative. After abreak-point (indicated by an arrow) the relationship line becamealmost flat. The break-point value indicates a limit value of EC, be-yond which necrosis of the plants occurred. Estimated break-pointvalues indicated that in case of regime A, willow plants survivedonly where leachate was not stronger than 5.0–6.5 mS/cm EC,but for regime B, only with EC below 3.0–3.2 mS/cm. In regime A,EC had a different influence on each plant parameter. The mostsensitive to leachate were roots (5.0 mS/cm), then leaf (6.0 mS/

cm), and finally stem (6.5 mS/cm). Similarly, in regime B, the mostsensitive to leachate were roots (3.0 mS/cm), then leaf and stem(3.2 mS/cm).

4. Discussion

The highly variable composition and toxicity of landfill leachatepresents many problems for biological treatment in constructed

Fig. 4. The relationship between electrical conductivity and willow parameters (leaf, stem, root and total plant weights). Arrows indicate the break-point – lethal dose oflandfill leachate (LD).

A. Bialowiec, P.F. Randerson / Waste Management 30 (2010) 1587–1593 1591

wetlands and soil–plant systems. Alker et al. (2003) proposed theuse of a constant level of soil moisture in willow stands to controlthe rate of landfill leachate irrigation. In that case, landfill leachatecomprised only 11% of the total water inflow entering the willowstands. Because of the variable character and toxicity of differentlandfill leachates (concentration of pollutants such as ammonium)in relation to different soil and climatic conditions, as well as dif-ferences in uptake of pollutants by different plant species, there re-mains the problem of selection of leachate dose rate, with respect

to the tolerance of specific plants. Phytotoxicological testing maybe a useful tool for dose rate selection, in particular to assess themaximum leachate dose which causes no negative effect on plantgrowth. Maximum leachate dose rate can be based on the % shareof leachate in the total water supplied to the plant, or on electricalconductivity, a general parameter representing total ionic contentof dissolved pollutants.

The toxicity of landfill leachate is highly variable. In the resultspresented here, the LOEC values were around 6% of full strength

1592 A. Bialowiec, P.F. Randerson / Waste Management 30 (2010) 1587–1593

leachate. Białowiec et al. (2003) found that leachate with a lowerconcentration of nitrogen (148 mg/l), at 50% of full strength, stim-ulated the growth of (S. amygdalina), but that further increase to100% slowed it down. This shows the necessity of performing indi-vidual tests for each kind of leachate, because of the specific re-sponses of plants to different leachate properties. Białowiec andAgopsowicz (2007) conducted phytotoxicological tests using simi-lar methods and leachate from the same source but with three dif-ferent willow species. The LOEC of leachate was calculated, basedon weekly data, using DEBTox software tool (a body growth mod-el). The lowest leachate concentration causing a toxic effect was inthe range 20.7–24.2%, values which are much higher than thoseobtained in the present study (6%) for the same landfill leachatebut using different willow species. It appears that different willowspecies differ in their sensitivity to leachate, which indicates theneed to perform toxicity tests in every case.

From a practical point of view LOEC value indicates the mini-mum landfill leachate dose which causes a measurable toxic effect,and it is a good indicator of plant response to toxicants in the initialphase of exposure. However, the plant may be able to toleratehigher leachate concentrations, up to a lethal level of toxicity. Also,long term exposure to landfill leachate may enable the plant toadapt to toxic conditions, as shown by Białowiec and Kasinski(2009). Comparing results from laboratory and long term (2 years)field experiments indicated a strong adaptation capacity of reedgrowing in the same kind of leachate. The degree of opening of leafstomata, used as an indicator of physiological state of the reedplants, was the same for reeds growing in lab and field conditions.Leachate pollution, expressed as electrical conductivity (EC) in thefield was 10 times higher (10.8 mS/cm) than in the laboratory(1.1 mS/cm) (Białowiec and Kasinski, 2009). During the course ofthe experiment, as in the present study, ionic concentration wasfound to increase markedly, due to evapotranspiration. For thesereasons it is important to determine the leachate concentrationwhich is lethal to plants, especially during the initial phase ofgrowth.

The indication of the adaptation of willow plants to pollutantsmay be the position of a break-point in the response curve of wil-low biomass to electrical conductivity. For irrigation regime A(plants watered by leachate solution from the beginning of theexperiment), the lowest break-point was at 5 mS/cm, whereas forplants pre-cultivated in clean water the break-point was reducedto 3 mS/cm.

From a practical point of view, it is necessary to use the lowestdose rate, in order to avoid a negative influence on planted willowsafter leachate supply. For cultivation regime A this value is at5.0 mS/cm for roots (break-point in Fig. 4). Hence willow cultivatedfrom the beginning with leachate irrigation, should be suppliedwith solution characterized by EC, not exceeding 5.0 mS/cm.

For irrigation regime B the critical value (break-point) is at3.0 mS/cm, hence, willow cultivated initially in clean water, maybe exposed subsequently to landfill leachate, but with an EC valuenot exceeding 3.0 mS/cm.

5. Conclusions

At concentrations used in the experiment landfill leachateshowed toxic effects on willow plants (S. amygdalina). The maxi-mum landfill leachate dose rate, which can be used for cultivationof willow during the initial phase of growth is 6% of full strengthleachate. Hence the proportion of landfill leachate in the totalamount of water supplied to a willow plantation (leachate + pre-cipitation) should not exceed 6% (EC 0.7 mS/cm) in the initial phaseof growth.

The response of plants to toxicants contained in the landfillleachate differs with the mode of cultivation. Willows exposed tolandfill leachate from the beginning of the experiment were moreresistant to leachate than willows supplied with leachate after4 weeks of pre-cultivation in clean water.

From a practical point of view, for this unique combination ofwillow variety and leachate, these results suggest the optimumprocedure for willow cultivation in leachate:

� Willow should be grown in landfill leachate solution from thestart.� For the first 4–6 weeks of cultivation the maximum proportion

of landfill leachate in the total amount of supplied water shouldbe determined using a phytotoxicological test, as in the presentstudy. The selected dose of leachate, expressed as LOEC, shouldbe employed for the first 4–6 weeks period of plant growth.� After that, the landfill leachate dose may be increased up to

about 25% of full strength, but it is important to avoid exceedingelectrical conductivity values of 5 mS/cm.

Acknowledgements

This experimental work was done with help of Mrs. Monika Ko-pik, and with financial support of Polish Ministry of Science andHigher Education, Grant No. N3313/T02/2007/32. Data analysiswas carried out with financial support of the fellowship of Dr. And-rzej Bialowiec held at Cardiff University, School of Biosciences,granted by Polish Ministry of Science and Higher Education, No.219/MOB/2008/0.

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