energetic environmental and economic assessment of three

11
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This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institution

and sharing with colleagues.

Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third party

websites are prohibited.

In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further information

regarding Elsevier’s archiving and manuscript policies areencouraged to visit:

http://www.elsevier.com/copyright

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Energetic environmental and economic assessment of threetree species and one herbaceous crop irrigated with primarytreated sewage effluent

V.A. Tzanakakis*, M.K. Chatzakis, A.N. Angelakis

National Foundation for Agricultural Research (N.AG.RE.F.), Institute of Iraklion, Iraklion, Greece

a r t i c l e i n f o

Article history:

Received 23 September 2011

Received in revised form

16 September 2012

Accepted 17 September 2012

Available online 22 October 2012

Keywords:

Wastewater land application

Bioenergy crops

Energy analysis

Economic analysis

Water use efficiency

Nutrient use efficiency

a b s t r a c t

The energetic, environmental, and economic performance of four bioenergy plant species

(Acacia cyanophylla, Eucalyptus camaldulensis, Populus nigra, and Arundo donax), irrigated with

pre-treated effluent in a three-year-field trial, was investigated. Results showed that irri-

gation was more energy demanding compared to other practices. A. cyanophylla achieved

34, 83, and 189% higher above ground biomass energy yield than E. camaldulensis, A. donax,

and P. nigra, respectively. A. cyanophylla and E. camaldulensis had higher energy require-

ments but they achieved higher net energy yield and energy ratio. P. nigra (3.49 V GJ�1) and

A. donax (2.34 V GJ�1) were found to have higher energy production cost compared to E.

camaldulensis (1.65 V GJ�1) and A. cyanophylla (1.24 V GJ�1). P. nigra and A. donax had the

highest nutrient use efficiency for nitrogen (NUE-N) and phosphorus (NUE-P), respectively.

It was concluded that species with low NUE, which is opposite to current directions, and

high water use efficiency (WUE) (i.e. plant species with relatively low water demands and

great biomass allocation in leaves), are more suitable when irrigation with strong effluent

occur and N removal is primary objective. Such plant species have comparatively lower

energy requirements, which is consistent with the current trend for low energy inputs in

agriculture. To mitigate the losses in plant biomass and reduce the adverse environmental

impacts from nutrients, additional practices should be adopted. Our results help us to draw

important conclusions in order to set criteria in the selection of suitable bioenergy crops

and practices.

ª 2012 Elsevier Ltd. All rights reserved.

1. Introduction

Bioenergy crops have a key role to play in the development of

strategies to increase the use of the renewable energy

resources, mitigate climate change, and protect the environ-

ment in EuropeanUnion (EU) [1]. Currently, the contribution of

renewable energy sources in EuropeanUnion (EU) is quite low,

at 4.5% of the total energy consumption with 60% of it covered

by energy frombiomass; however, in an effort to increase their

use, it was set a target for 2020 of 20% of the energy

consumption and increase of biofuels at 10% of the total fuels

used in road transportations [1,2]. Lignocellulosic biomass

from certain herbaceous crops and some woody perennials

grown in short rotation coppice, is considered to be essential in

meeting EU targets, since it can contribute in all energy sectors

including electricity, heating/cooling and biofuel [3].

The use of wastewater effluent to bioenergy cultivations is

a cost-effective practice, known also as land treatment

* Corresponding author.E-mail address: [email protected] (V.A. Tzanakakis).

Available online at www.sciencedirect.com

http: / /www.elsevier .com/locate/biombioe

b i om a s s a n d b i o e n e r g y 4 7 ( 2 0 1 2 ) 1 1 5e1 2 4

0961-9534/$ e see front matter ª 2012 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.biombioe.2012.09.051

Author's personal copy

systems (LTS) or slow rate systems (SRS), meeting environ-

mental and renewable bioenergy goals [4,5]. Effluent can

supply bioenergy crops with considerable amounts of water

and nutrients stimulating plant growth and energy yield and

decreasing production cost through the substitution of water

and fertilizers [6]. In addition, effluent application can reduce

the competition for water between bioenergy and traditional

crops,which is important concern in arid or semi-arid regions.

On the other hand, the use of effluents may lead to significant

nutrient losses to the environment, commonly due to inap-

propriate plant species and practices applied [7e9]. The

management of nutrients and particularly N is of prime

concern in effluent irrigated lands since excessive N loading

can lead to nitrates accumulation in soil and increase in

greenhouse gases emissions (e.g. NOx). In general, bioenergy

crops with high water use efficiency (WUE) and nutrient (e.g.

N) use efficiency (NUE) have been recognized asmore suitable,

since they use more efficiently water and nutrients applied,

which in turn reduce economic and environmental cost [3].

However, in cases of irrigation with relative strong effluent,

specieswith highWUEmay accumulate excessive nutrients in

rhizosphere, suggesting that the effluent loading should also

be taken into account [7,8].

Energy analysis is a common practice in the assessment of

bioenergy crops and/or applied agronomic practices assessing

the energetic performance of plant species and indicating its

environmental and economic sustainability [6]. In general,

plant species with greater differences between energy output

and input, leading to higher net energy yield and energy ratio,

have greater potential to be used as bioenergy crops [10,11].

However, there seems to be important in bioenergy cultiva-

tions theminimization of energy inputs [12], as it is associated

with less adverse environmental impacts and economical

cost, indicating that high net energy yield and energy ratio

should be combined with lower energy inputs. Irrigation with

effluent probably would help in this task, enhancing biomass

and yield and eliminating the energy requirements for fertil-

ization in the field but the potential benefits have not yet

emphasized in literature.

Adoption of bioenergy crops by farmers presumes that

species are more economically favorable than the traditional

ones, with which normally compete for land use [13]. Among

bioenergy crops, lignocellulosic plant species, e.g. willow and

eucalyptus under short rotation coppice, have been identified

as more appropriate combining high biomass production

potentials under low production cost [14]. These species have

also great potential to be used as vegetative filters due to

several desirable attributes, such as broad adaptation in

a wide range of soil-climatic conditions, wide genetic base,

fast growth and high biomass production, nutrient cycling,

and reduction of greenhouse gases emissions [3,4] but because

of the particular interest only for biomass production this

issue is not adequately considered.

In this study the effect of bioenergy crops (three tree

species and an herbaceous crop) on energy requirements,

energy yield derived from the produced biomass, net energy

balance, energy ratio, and economical cultivation cost was

investigated. Furthermore, it was investigated the environ-

mental performance of these plant species based on the

assessment of NUE for N and P, expressing the efficiency with

which plant species use the applied, via wastewater effluent

irrigation, nutrients. The information provided in this study is

expected to bring out the benefits in energy cultivations

derived from the use of wastewater effluent and help in the

development of criteria for the identification of the more

suitable bioenergy plant species and practices based on

environmental and economic cost and benefits.

2. Materials and methods

2.1. Experimental set up and agronomic techniques

Plant specieswere established at Skalani village, located about

5 km south east of Iraklion city, Greece (at N 35� 16.80 and E 25�

11.20). The soil was characterized as a clay loam with high

calcium content (55% CaCO3). The climate is semi-arid with

relatively humid winters and dry and warm summers. More

detailed information concerning, experimental design, soil

properties, effective precipitation, temperature, and reference

evapotranspiration of the experimental area are given in our

previous studies [7,8]. One-year old trees of eucalyptus (Euca-

lyptus camaldulensis), acacia (Acacia cyanophylla or saligna) and

poplar (Populus nigra) were transplanted on October 2000.

Rhizomes of reeds (Arundo donax) were also excavated, cut into

small cuttings and transplanted at distances 0.50 m between

and within rows. Plant species were allowed to grow without

any treatment until June 2001, when the application of pre-

treated wastewater began. Plant species received septic tank

primary treated sewage effluent [15] and hydraulic loading

rate was based on their water requirements and evaporation

losses estimated from a simple balance on a daily-time step.

Average values of the composition of septic tank-treated

effluent are summarized in Table 1.

The applied pre-treated wastewater increased from the

beginning of spring until late summer, controlled by plant

growth, thereafter effluent application rate was declined.

During first period of operation (from June 6, 2001 to

November 30, 2001) A. donax exhibited higher water

consumption (736 mm), followed by P. nigra at 724 mm, A.

cyanophylla at 637 mm, and E. camaldulensis at 631 mm. During

Table 1 e Average values of the composition of septictank-treated wastewater effluent, applied in differentbioenergy plant species.

Parameters 2001 2002 2003

EC (dS m�1) 2.02 2.08 2.10

pH 7.26 7.36 7.40

TSS (mg L�1) e 93 106

COD (mg L�1) 553 386 510

Inorganic P (mg L�1) 5.89 6.64 6.73

TP (mg L�1) 10.09 8.37 9.84

T (Kjeldahl) N (mg L�1) 87.04 102.09 124.64

Nitrates (mg L�1) e e 1.07

Kþ (mg L�1) e e 29.53

Naþ (mg L�1) e 132.64 126.38

Mg2þ (mg L�1) e 14.65 26.49

Ca2þ (mg L�1) e 80.76 80.78

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the next period of LTS operation (March 1, 2002 to November

15, 2002), effluent loading were 1020, 1074, 975, and 725 mm

for A. donax, A. cyanophylla, E. camaldulensis, and P. nigra,

respectively. In 2003 (March 1, 2003 to October 30, 2003)

respective values were 1515, 1852 1822 and 1212 mm for each

system.

Following each growing season harvesting was carried out

and the above ground biomass yield and its distribution

among different plant tissues were determined. Details about

the sampling method, storage, and lab analyses are provided

in our previous work [7]. In brief, at the end of every growing

season (October), one representative tree from each plot was

harvested and separated into individual organs. The fresh

weight of leaves, shoots and trunk (old wood) were recorded.

For reeds, the whole plot surface was harvested each season

and separated into leaves and shoots. All sampleswere kept in

plastic bags and were transported to the lab for the appro-

priate analyses. Dryweights of vegetationwere determined by

drying (65 �C) to a constant weight. In 2002 and 2003 one

replicate plot was harvested from each treatment and the

tissue dry weights were determined. The dried samples were

ground to 1-mm and used in elemental analysis [7]. Weed

control was done only during the establishment year. The

analytical presentation of the cultivation practices considered

in this study during the experimental period is summarized in

Table 2.

2.2. Determination of net energy balance and energyratio

Net energy yield and energy ratio in different plant species

were determined for the three growing seasons taking into

account the energy input and output. More analytically, the

net energy yield was determined by subtracting energy input

from energy output (yield), while energy ratio by dividing the

energy output with the energy input. In order to determine

energy inputs across species, energy input for soil prepara-

tion, plants planting, wastewater effluent application, plant

harvesting, and weed control were considered. Energy

requirements for delivering the production outside the field,

for storage and drying as well as indirectly energy inputs by

the pump and pipeline for effluent transport in the field were

not included in the calculations. Energy requirements for

application of the wastewater effluent (or irrigation energy

requirements) included electricity consumption by electric

engine pump. The electricity consumption was considered

here equal to 4.8 MJ m�3 of effluent [16]. Energy input for

mechanization is usually determined taking into account fuel

and lubricant consumption of the tractor as well as energy

requirements for the fabrication and repair of the machinery

utilized during the cultivation of species [17]. The calculation

of fuel and lubricant energy requirements of various

management operations is based on fuel and lubricant

consumption and their energy content. In this study, it was

assumed that the energy requirements was 4.5 GJ ha�1 for

soil preparation [6,12,16e19], 4.3 GJ ha�1 for planting

[6,12,16,18,19], 3.2 GJ ha�1 for harvesting [16,18e21], 1.2 GJ ha�1

for weed control [11,12,16], and 0.2 GJ ha�1 for pesticides

[12,20].

2.3. Elemental content and energy yield

In order to determine C and H content in above ground plant

tissues and energy yield dried samples gathered at the end of

third period (Oct. 2003), were grounded, passed through No 4

sieve (4.75 mm) and burnt in an oxygen bomb calorimeter to

determine their calorific value. The energy yield of above

ground biomass was calculated by multiplying the calorific

value with the above-ground dry matter yield reported in our

previous study [7]. For the previous growing seasons (2002 and

2001), the calculation of the energy yield was based on the

produced biomass at the end of these periods [7], assuming

that respective calorific values had the same value as the third

period. Previous work has shown that the calorific value of

many plant tissues was not affected by the age as well as by

fertilization, or by plant density or harvest time [18,19,22].

Elemental content in plant tissues were determined in dried

samples using elemental analyzer (PerkineElmer). C:N andC:P

ratio calculations were carried out at the end of the third

growing season, based on C and H content as well as on N and

P content in tissues reported in our previous work [7].

2.4. Nutrient use efficiency (NUE)

The NUE and WUE are widely used in the selection of the

appropriate plant species, particularly whether these are to be

irrigatedwithwastewater effluent and/or where limitations in

the use of water and nutrients exist. In this study, the NUE for

nitrogen (NUE-N) and phosphorus (NUE-P) were determined

from biomass yield divided by the amount of N and P recov-

ered, respectively, expressed as kg�1 kg�1. The biomass

production, nutrient contents in tissues, and the amount of N

or P recovered by different species, used in this study, have

been reported in our previous study [7].

2.5. Energy crop production cost

Energy production cost was estimated based on capital and

operation and maintenance (O&M) cost and it was expressed

as cost per unit the produced bioenergy, in order to link

economical requirements of the plant species with energetic

profits. The capital costs were estimated based on the receipts

of the different constructionworks after transferred to refer to

2003 and they were free from value added taxes. Major works

Table 2 e Agronomic practices carried out in differentplant species during the three growing seasons(2001e2003).

Practices Growing season

2001 2002 2003

Soil preparation O e e

Planting O e e

Irrigation O O O

Weed control O e e

Plant protection O O O

Harvesting Oa Oa O

a Harvesting only for A. donax species.

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involved the installation of monitoring apparatus (electro

valves, electric panel, etc.), pumps, soil preparation, plant

purchasing, planting, and installation of irrigation network.

Operation and maintenance (O&M) costs were calculated

based on the 3 year cost data and were also transferred to

reflect 2003 prices. Major O&M costs involved pesticides, weed

control, electricity consumption for irrigation,maintenance of

the irrigation network, and harvesting. Because the irrigation

needs were different per plant this cost was different per

plant. The same was for the man work during harvesting

(calculations included annual harvesting for A. donax, as

shown in Table 2).

In this study, Total Annual Economic Cost (TAEC) was

calculated for all plant species to indicate their economic

performance [23]. The TAEC of the system was given by the

sum of the annuitized construction cost (Cc) and the annual

operation and maintenance costs (Ca) as reported by Eq. (1):

TAEC ¼ ðCc � CRFÞ þ Ca (1)

CRF ¼ rð1þ rÞtð1þ rÞt�1

(2)

where t is time in years and r is the opportunity cost of capital

(OCC). The energy crop production cost of each species was

calculated by dividing the TAEC by the total number of GJs

produced per year.

2.6. Statistical analysis

Statistical analysis was performed for data analysis using

SPSS v.19 program. The effect of the plant species and tissues

was carried out by using General Linear Model, Univariate

Analysis of Variance (UNIANOVA). Post hoc pair wise

comparisons were examined by Tukey’s honestly significant

difference (HSD) test. Furthermore, a correlation analysis was

carried out to determine the relationship between N and P

content across plant tissues and NUE.

3. Results

3.1. Energy input

The applied energy increased with the progress of time in all

species reflecting mainly the energy consumption during

wastewater effluent application, since the additional energy

inputs arising from the cultivation practices were fairly small

(Fig. 1a,b,c). Indeed, the average cumulative cost for effluent

application was about 70% of the total applied energy for the

establishment year increasing at 82% and 89% in the following

years. Plant species affected significantly energy inputs,

particularly in the second and third growing seasons, owing to

the application rates of the effluents which were different

along species. At the end of the first growing season (Oct. 2001)

A. donax and P. nigra species had similar energy input followed

by that of A. cyanophylla, and E. camaldulensis (Fig. 1a). The

following season (2002) energy consumption of A. cyanophylla

(51.8 GJ ha�1) approached that of A. donax (52.4 GJ ha�1) and

these species were followed by E. camaldulensis (47.0 GJ ha�1)

and P. nigra (35.0 GJ ha�1). Thus, the cumulative energy input

for the two sequent seasons (2001e2002) was higher for A.

donax followed by A. cyanophylla, E. camaldulensis, and P. nigra

(Fig. 1b). With regards to the last season (2003) A. cyanophylla

had the highest energy input (92.3 GJ ha�1) followed by E.

camaldulensis (90.9 GJ ha�1), the energy input of which excee-

ded that of A. donax (76.2 GJ ha�1) and remained higher than

that of P. nigra (61.6 GJ ha�1). Overall, at the end of the three

growing seasons, the cumulative energy consumption was

more in A. cyanophylla (184.9 GJ ha�1) followed by E.

A. cyanophylla E.camaldulensis P.nigra A. donax0

10

20

30

40

50

60

70

Ene

rgy

inpu

t (G

J ha

-1)

Plant protectionWeed controlHarvestingPlantingSoil preparationIrrigation

A. cyanophylla E.camaldulensis P.nigra A. donax0

20

40

60

80

100

120

Ene

rgy

inpu

t (G

J ha

-1)

A. cyanophylla E.camaldulensis P.nigra A. donax0

25

50

75

100

125

150

175

200

225

Ene

rgy

inpu

t (G

J ha

-1)

a

b

c

Fig. 1 e Cumulative energy inputs across species for 2001

(a), 2001and 2002 (b), and 2001e2003 (c) growing seasons.

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camaldulensis (178.4 GJ ha�1), A. donax (177.3 GJ ha�1), and

P. nigra (141.6 GJ ha�1) (Fig. 1c).

3.2. Elemental content and energy density in planttissues

A higher C content was assessed in the leaves ofA. cyanophylla

and E. camaldulensis compared to A. donax and P. nigra. In

contrast, no differences in C content of the trunk and shoots

were found among the four studied species (Table 3). Similar

to C content, plant species affected H content in the leaves but

not in the trunk and shoots. E. camaldulensis, A. cyanophylla,

andA. donax had higher H content in the leaves compared to P.

nigra (Table 3). Differences in C:N ratio were detected among

plant species with A. cyanophylla and P. nigra showing greater

value in the trunk compared to A. donax (Table 3). In shoots, E.

camaldulensis, A. cyanophylla had the highest C:N ratio and in

leaves E. camaldulensis and P. nigra. With regard to C:P ratio the

highest value was achieved by A. cyanophylla in the trunk and

by A. donax in the shoots and leaves (Table 3). Leaves had

lower C:N and C:P ratio in all species compared to the trunk

and shoots, as was expected indicating greater potential to be

used as substrate to anaerobic digestion.

With regard to energy density of trunk and shoots no

differences were detected among plant species, illustrating

the elemental similarity of these plant parts with respect to C

and H (Table 4). Unlike, significant differences in energy

density among species were registered in leaves, linked with

their differentiation in C and H content. In leaves, the highest

energy density was detected in species of E. camaldulensis and

the lowest in those of P. nigra (Table 4).

3.3. Energy yield

Energy yield increased with the age of species as a result of

biomass growth. Plant species affected substantially the

energy yield and its distribution among different plant tissues

over the entire experimental period (2001e2003) (Table 5). At

the end of the first season (Oct. 2001) A. cyanophylla had the

highest energy yield followed by A. donax, P. nigra, and E.

camaldulensis (Table 5). For the next season (Oct. 2002) the

additional energy yield was again higher in species of A. cya-

nophylla andA. donax attained energy yield of 621.9 GJ ha�1 and

534.6 GJ ha�1, respectively, but the additional energy yield

attained by E. camaldulensis (456.8 GJ ha�1) exceeded that of P.

nigra (280.9 GJ ha�1). As a result of these yields, species

followed the same ranking with the second season with

respect to the cumulative energy yield of the two sequent

growing seasons (Table 5). The last growing season (Oct. 2003)

the additional energy yield was still higher for A. cyanophylla

(1479.0 GJ ha�1) but E. camaldulensis (1218.8 GJ ha�1) attained

higher energy yield than that of A. donax (617.6 GJ ha�1), while

the lowest energy yield was observed in plants of P. nigra

(416.5 GJ ha�1). Thus, after three consecutive growing seasons

the cumulative energy yield was higher in species of A. cya-

nophylla followed by E. camaldulensis A. donax, and P. nigra

(Table 5). Differences in the distribution of energy yield in

tissues were also observed among plant species (Table 5 in

parenthesis). Tree species distributed a greater proportion of

energy yield in the trunk. An increasing trend in the propor-

tion of energy yield allocated to the trunk was registered in

trees of A. cyanophylla and E. camaldulensiswith the progress of

time and this trend was greater for A. cyanophylla. However, P.

nigra distributed a greater proportion of energy yield in the

trunk compared to other species. In contrast to the trunk, the

proportion of energy allocated to the leaves followed the

opposite trend for A. cyanophylla and E. camaldulensis and

remained constant for P. nigra and A. donax. Also, the

proportion of energy distributed in the shoots of plant species

remained constant during entire experimental period.

3.4. Net energy yield and energy ratio

Net energy balance increased with the time in all species

being highest in A. cyanophylla in all growing seasons (Fig. 2a);

in the 2001 season, A. cyanophylla was followed by other

species, which had similar values. Similar results were

Table 3 e Elemental content and C:N and C:P ratios of above ground plant tissues of the different plant species at the end ofthe third growing season (October 2003).

Plant species C (g kg�1) H (g kg�1) C:N ratio C:P ratio

Trunk Shoots Leaves Trunk Shoots Leaves Trunk Shoots Leaves Trunk Shoots Leaves

A. cyanophylla 463.8 461.7 470.7a 61.1 59.2 58.2a 99.3a 51.8 ab 17.5b 1158.7a 428.7b 207.3

E. camaldulensis 470.7 467.1 467.8a 59.2 59.2 59.4a 71.6b 60.8a 21.8a 420.4b 537.5ab 205.9

P. nigra 472.0 458.4 416.8c 60.8 59.7 52.7b 97.9a 37.2b 22.1a 773.5ab 240.0b 194.0

A. donax e 469.8 427.9b e 59.9 56.8a e 46.9ab 14.1b e 1492.4a 244.1

Significance n.s. n.s. **. n.s. n.s. ** * ** ** * * n.s.

ns: not significant. *P< 0.05, **P< 0.01, ***P< 0.001. Numberswith different letters differ significantly at P< 0.05 by Tukey’s significant difference.

Table 4 e Energy density of above ground plant tissues ofthe different plant species at the end of the third growingseason (October 2003).

Plant species Trunk(MJ kg�1)

Shoots(MJ kg�1)

Leaves(MJ kg�1)

A. cyanophylla 19.2 19.1 19.4ab

E. camaldulensis 19.1 19.1 19.9a

P. nigra 19.6 19.0 16.0c

A. donax e 18.1 18.7b

Significance n.s. n.s. **

ns: not significant. *P < 0.05, **P < 0.01, ***P < 0.001. Numbers with

different letters differ significantly at P< 0.05 by Tukey’s significant

difference.

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obtained for 2002 season, but it was observed a slight increase

in the range of differences among plant species. In this year

the ranking was A. cyanophylla, A. donax, E. camaldulensis, and

P. nigra. The last season (2003), the differences among plant

species were enhanced and E. camaldulensis species exceeded

that of A. donax resulting from the high rate of increase in net

energy yield in A. cyanophylla and E. camaldulensis species

(Fig. 2a). Thus, after three year experiment it was found thatA.

cyanophylla had 2181.6 GJ net energy yield followed by E.

camaldulensis (1584.6 GJ), A. donax (1125.7 GJ), and P. nigra

(639.4 GJ).

Energy ratio also tended to increase with the age of the

plant species; the A. donax reached its maximum value in the

second growing period and then leveled off (Fig. 2b). A. cya-

nophylla species showed the highest ratio, an effect attributed

mainly to its potential for greater biomass production in

comparison to the other three plant species. With regard to

these species, the ranking changed along growing seasons. In

2001 season, A. donax species showed higher values than P.

nigra and E. camaldulensis, with the previous two species

showing similar values. In the following period, a similar

influence was observed while energy ratio of E. camaldulensis

exceeded that of P. nigra. The last growing period the effi-

ciency of E. camaldulensis increased further and exceeded that

of A. donax and P. nigra species (Fig. 2b).

3.5. Nutrient use efficiency (NUE)

The NUE-N and NUE-P increased with time in all tree species,

achieving their maximum value at the end of the third

growing season. This was not the case for A. donax species

regarding NUE-N, in which maximum value was observed

after the second growing period and then leveled off (Table 6).

Regarding NUE-N it was higher in P. nigra species and lower in

A. donax in all growing seasons. With respect to other species,

NUE-N was higher in E. camaldulensis species than the A. cya-

nophylla ones for the first and second season but it was

reversed during the last growing season. The NUE-P was

higher in A. donax species in all seasons (Table 7). The ranking

of the other three species was: A. cyanophylla, P. nigra, and E.

camaldulensis. Detailed information regarding NUE-N and

NUE-P among plant species and plant tissues is provided by

2001 2002 20030

500

1000

1500

2000

2500

Net

ene

rgy

yiel

d (G

J ha

-1)

A. cyanophyllaE.camaldulensisP.nigraA. donax

2001 2002 20030.0

2.5

5.0

7.5

10.0

12.5

15.0

Ene

rgy

rati

o (G

J G

J-1)

Year

a

b

Fig. 2 e Cumulative net energy yield (GJ haL1) (a) and

energy ratio (GJ GJL1) (b) across plant species at the end of

three growing seasons.

Table 5 e Cumulative energy yields for different plant species and plant tissues at the end of the three growing periods.

Plant species Trunk (GJ ha�1) Shoots (GJ ha�1) Leaves (GJ ha�1) Total (GJ ha�1)

2001

A. cyanophylla 80.6a (30) 101.0a (38) 84.0a (32) 265.63a

E. camaldulensis 39.3b (45) 19.6b (22) 28.5bc (33) 87.42b

P. nigra 70.6a (59) 41.8b (34) 7.9c (7) 120.36b

A. donax e 105.7a (73) 38.9b (27) 144.59b

Significance ** *** *** ***

2002

A. cyanophylla 297.2a (33) 352.6ab (40) 237.6a (27) 887.5a

E. camaldulensis 243.4ab (45) 140.0b (25) 160.7ab (30) 544.2ab

P. nigra 178.4b (44) 190.08b (47) 32.8b (9) 401.7b

A. donax e 518.1a (76) 161.0ab (24) 679.1ab

Significance * ** ** *

2003

A. cyanophylla 1124.4a (48) 858.6a (36) 383.4a (16) 2366.5a

E. camaldulensis 855.0ab (48) 493.9b (28) 414.1a (24) 1763.0ab

P. nigra 501.0b (61) 262.2b (32) 54.6b (7) 817.8b

A. donax e 994.6a (77) 302.1a (23) 1296.7b

Significance * *** ** **

ns: not significant. *P< 0.05, **P< 0.01, ***P< 0.001. Numbers with different letters differ significantly at P< 0.05 by Tukey’s significant difference.

b i om a s s an d b i o e n e r g y 4 7 ( 2 0 1 2 ) 1 1 5e1 2 4120

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Tables 6,7, respectively. Both NUE-N, and NUE-P had strong

negative relationship with the concentration of N and P in

plant tissues, respectively, as shown in Fig. 3. The leaves had

lower NUE-N, and NUE-P than shoots and trunk, implying that

species with high proportion in leaves achieve low NUE-N and

NUE-P values.

3.6. Energy crop production cost

The capital, O&M, and TAEC for all plants (reference year is

2003) are summarised in Table 8. Fifteen years were used as

time period and opportunity cost of capital of 5%. The capital

cost was the same in all plant species which is referred to our

experimental area. As already reported, O&M cost differenti-

ated across species.A. donax species had the highest O&M cost

followed by A. cyanophylla, E. camaldulensis, and P. nigra

species.With regard to energy production cost (cost per unit of

GJ), it was higher in species that attained higher biomass and

energy yield. Thus, less cost was required by A. cyanophylla

and E. camaldulensis species, indicating greater potential to be

used as bioenergy crop.

4. Discussion

4.1. Energy input

The energy inputs in all species tended to increase from the

first year of the establishment of the experiment to the end of

the experimental period, owing mainly to irrigation energy

requirements. The differences in energy input among plant

Table 6 eNUE-N for different bioenergy plant species andplant tissues at the end of the three growing seasons.

Plant species Trunk(kg kg�1)

Shoots(kg kg�1)

Leaves(kg kg�1)

Total(kg kg�1)

2001

A. cyanophylla 163.7a 116.4 39.2b 76.1b

E. camaldulensis 117.8b 114.7 47.6a 79.9b

P. nigra 156.0a 105.1 45.0a 114.6a

A. donax 102.2 35.5b 67.7b

Significance * n.s. *** ***

2002

A. cyanophylla 208.3a 119.0ab 37.4b 83.0b

E. camaldulensis 138.9b 137.0a 49.7a 91.0a

P. nigra 181.9ab 100.0b 50.7a 111.0a

A. donax 107.1b 38.1b 74.7b

Significance * * *** ***

2003

A. cyanophylla 208.3a 111.1a 37.2c 101.2b

E. camaldulensis 151.5b 129.8a 46.7b 97.2b

P. nigra 200.0a 81.3b 52.9a 118.1a

A. donax 111.1a 35.4c 75.3c

Significance * *** *** ***

ns: not significant. *P < 0.05, **P < 0.01, ***P < 0.001. Numbers with

different letters differ significantly at P< 0.05 by Tukey’s significant

difference.

Table 7 e NUE-P for different bioenergy plant species andplant tissues at the end of the three growing seasons.

Plant species Trunk(kg kg�1)

Shoots(kg kg�1)

Leaves(kg kg�1)

Total(kg kg�1)

2001

A. cyanophylla 929.0a 715.2ab 701.8a 763.5b

E. camaldulensis 556.8c 453.3b 370.2b 459.3d

P. nigra 767.6b 493.3b 449.5b 614.9c

A. donax 1075.0a 624.6a 899.2a

Significance ** ** *** ***

2002

A. cyanophylla 1249.6a 1000.0ab 769.0 987.4b

E. camaldulensis 835.9b 909.3ab 555.6 741.1b

P. nigra 909.2b 624.6b 587.4 717.0b

A. donax 1498.6a 547.2 1058.1a

Significance * * n.s. **

2003

A. cyanophylla 2307.1a 909.1b 422.6 1013.6b

E. camaldulensis 909.0c 1111.1b 410.9 741.7c

P. nigra 1578.4b 491.8c 435.1 821.0c

A. donax 2056.7a 555.8 1285.0a

Significance * * n.s. ***

ns: not significant. *P < 0.05, **P < 0.01, ***P < 0.001. Numbers with

different letters differ significantly at P< 0.05 by Tukey’s significant

difference.

0 5 10 15 20 25 30 350

50

100

150

200

250

0.0 0.5 1.0 1.5 2.0 2.5 3.00

500

1000

1500

2000

2500

NU

E-N

(kg

kg-1

)

N content (g kg-1)

R2= 0.99

NU

E-P

(kg

kg-1

)

P content (g kg-1)

R2=0.98

a

b

Fig. 3 e Relationship between N and P content across plant

organs and NUE-N (a) and NUE-P (b), respectively.

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Author's personal copy

species are also attributed to this cost since the greater

proportion of the total energy input was for the application of

wastewater effluent in the field (Fig. 1). Opposite to the culti-

vation practices and harvesting, irrigation is considered as far

more energy demanding, contributing significantly to the total

energy requirements of plantations. In Portugal five poplar

production systems were analyzed reporting high annual

energy consumption (85 GJ ha�1) [12] attributed to the large

energy requirements for the application ofwastewater effluent

in the field (38 GJ ha�1), which are similar with those present in

the present study. It has been reported high energy consump-

tion (43.1 GJ ha�1) for the establishment year ofA. donaxmainly

causedbywastewater effluent application (22.1 GJ ha�1), which

accounted for 50% of the total energy requirements [24]. Even

lower energy requirements forA. donax rangedbetween7.7 and

22.7 GJ ha�1 has been found in literature [19]. The latter energy

requirements aremuch lower than what we found here due to

the lower water application rates.

4.2. Elemental content and energy density in plant tissues

The energy density in trunk and shoots was not affected by

species reflecting the elemental similarity of these plant parts

with respect to C and H. This was not the case for leaves since

they are more heterogeneous than wood and shoot [22]. The

energy density vary with the elemental content of the fuel,

particularly with the C, O2 and H content, as well as with fuel

physical properties such as moisture and ash content [24].

Differences in energy content have been observed mainly

among plants species, genotypes, and plant tissues, ranging

from 15 to 24 MJ kg�1on a dry basis [22,25] and our findings are

within that range, and are in accordance with those findings

reported in several previous studies. Also, results in this study

showed that C:N and C:P varied greatly with plant species and

plant tissues. Leaves had lower C:N and C:P in all plant

species, ranging from 14 to 22 and 181 to 238, respectively,

suggesting greater potential as feedback in anaerobic diges-

tion since for optimum microbial function a C:N:P ratio of

100e128:4e5:1 is recommended [26].

4.3. Energy yield

Energy yield constitutes an important factor which affects

significantly economic and environmental performance of

bioenergy cultivation. In the present study, energy yield

increased with the age of species due to biomass growth.

Furthermore, plant species affected significantly the energy

yield obtained by different plant tissues as well as the total

energy yield (Table 5). These results are in the same pattern

with biomass production [7], indicating that energy yield

should be more attributed to yielded biomass and its alloca-

tion among plant tissues and less to differentiation of plant

tissues in energy densities as it has been showed before. It has

been reported that biomass yield, and therefore energy yield,

vary greatly with plant species, clones, climatic conditions,

and management practices mainly irrigation, fertilization,

tree density and harvesting cycle [7,27]. For example, in

Europe, dense short rotation plantations (20,000 trees ha�1) of

Eucalyptus globules and E. camaldulensis produced 16 and

20 t ha�1 y�1 respectively 2 years after planting [28] and these

values, correspond approximately to 308 and 385 GJ ha�1 y�1.

With regard to poplar, it has been reported 8 t ha�1 y�1 dry

biomass which in our estimation corresponds

to155 GJ ha�1 y�1 [29] and this energy yield is much lower

compared to the yields obtained in this study for P. nigra. Great

variation in the yield of different clones of A. donax has been

reported with the average yield reaching about the 11 and

22 t ha�1 in the first and the second growing period, respec-

tively [30]. These values correspond approximately to 196 and

409 GJ ha�1 energy yields, lower than those obtained in this

study. Generally, energy yields achieved by the species of the

present study were higher than those reported in the litera-

ture, which is a presumable result considering the high water

and nutrient availability in soil and the climatewhere the field

experiments were carried out.

4.4. Net energy yield and energy ratio

In the present study, net energy yield and energy followed the

trend of energy yield, since both are directly proportional to

that, showing higher values in A. cyanophylla and E. camaldu-

lensis species. There is quite high variation in literature

regarding net energy yield and energy ratio due to different

species or genotypes, growing conditions, and processing

methods and assumptions, which makes it difficult for any

comparison of our results with earlier studies [6,12,16].

Generally, net energy yields presented in this study, particu-

larly for E. camaldulensis and A. cyanophylla, are considered

high, and ascribed mainly to the obtained energy yields.

Unlike, the energy ratio among the studied species were lower

than those reported for other energy species [6,12,16,18,24].

This indicates a relatively low efficiency in the use of the

energy inputs by the bioenergy plant species of the present

study ascribed to the great energy inputs. In Europe there is

a growing interest in low-inputs production systems in agri-

culture since these are friendlier to the environment [12].

From that point of view plant species and agronomic practices

with greater potential for lower energy requirements aremore

promising. However, the shift from high-input to low-input

production systems may decrease their potential for

biomass and energy production, indicating that more land is

required to compensate the losses. Indeed, in this study

depletion of energy inputs can be achieved by reducing

wastewater effluent application rates, which probably means

lower available water for plant species and hence lower

potential for biomass and energy yield. Also, this probably

suggests that suitable plant species are thosewith lowerwater

demands rather than those with higher biomass yield. This is

compatiblewith directions regarding nutrientmanagement in

effluent irrigated lands discussed below.

Table 8 e Production cost across the different plantspecies.

Plant species Capital2003

O&M2003

TAEC TAECGJ�1

A. cyanophylla 12627.4 1728.6 2945.1 1.2

E. camaldulensis 12627.4 1693.4 2909.9 1.6

P. nigra 12627.4 1633.9 2850.4 3.5

A. donax 12627.4 1812.2 3028.7 2.3

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4.5. Nutrient use efficiency (NUE)

NUE-N and NUE-P increased with time in all plant species

whereas differences were also observed among them. These

results are attributed to variations in the amount of plant

biomass and its allocation in the plant tissues across plant

species during the experimental period. The trunk had lower

nutrient content followed by shoots and leaves [7], and the

contributionof eachof plant tissue toplant biomass resulted in

variations in NUE-N and NUE-P, as shown in Fig. 3. Thus, the

increasewith timeof theseparameters is due to the increase in

plant biomassand its greater allocation in the trunkandshoots

than in leaves, particularly for the tree species. Similarly,

P. nigra, having greater allocation of biomass in the trunk and

lower in the leaves had the highest NUE-N compared to other

plant species. In contrast,A. donax species, having only shoots

and leaves, had the lowest NUE-N. However, the opposite

occurred forNUE-P ofA. donax, having thehighest value,which

is attributed to low P content in the shoots [7]. In this study, the

plant species with the lower NUE-N tended to accumulate less

nitrates in soil than thosewith higher NUE-N [8]. An important

factor for this result is the fact that the first ones assimilate

higher amounts of N in relation to their biomass, suggesting

that the plant species with low NUE-N are more suitable in

cases of irrigationwith liquids rich inN.However, this doesnot

seem to apply in cases of irrigation with fresh water and

application of commercial fertilizers, since plant species with

high NUE usemore efficiently fertilization inputs, whichmake

themmore economically and environmentally sustainable [3].

In addition, the impacts on environment from the use of

fertilizers in those plant species are minimized. In terms of

WUE, to avoid the nutrient accumulation, plant species should

have high WUE attributed, however, mainly to low water

demands rather than high biomass production, as has been

suggested [7]. The suggestion for lower effluent application

rates, in order to reduce the excessive nutrients in soils

exposed to strong wastewater effluent, coincide with that

derived from the energetic analysis of this study, demon-

strating that the reduction of effluent application rates can

serve both energetic and environmental management goals.

4.6. Energy crop production cost

Unlike the capital cost, O&M cost varied considerably across

plant species. A. donax species were clearly more expensive

than the other species, attributed to the annual biomass har-

vesting. In previous studies regarding perennial grasses, i.e.

switchgrass and miscanthus, harvesting was found to be an

expensive annual operation contributing significantly in the

overall annual operation cost [14], as also registered in the

present study.As a result ofO&Mcost, TAECwasalso greater in

A. donax species since it is directly proportional to that (See

Materials andmethods).With regard to energy production cost

(TAEC GJ�1), it was lower in A. cyanophylla and E. camaldulensis

species due to the energy yield produced by those species and

lower O&M cost. It has been found that the cost of production

per tonne or energy decline as yield increases [31]. Also, it was

reported that short rotation species, i.e. willow and eucalyptus,

had the lower production cost (about 3e5 V GJ�1 assuming 15

years of experience of large scale energy crop cultivation) than

that of perennial grasses (5e7 V GJ�1), i.e. miscanthus, switch

grass, and reed canary grass [14], due to the low annualized

costs for theharvestingof short rotationcoppice species (which

takes place every three or four years) and the establishment

cost. Also, it should be pointed out that calculations for O&M in

this study, referring to planting, use of pesticides,weed control,

and harvesting, included only man work which probably

caused an overestimated O&M cost, since the cost of the tradi-

tional farming is higher compared to that of mechanized [32].

However, our resultswere relatively lower than that reported in

previous studies concerning bioenergy plantations, i.e. willow,

poplars, switchgrass and miscanthus [14,33] which is predom-

inantly attributed to the high energy yields and the excluded

operations in the economic analysis such as land cost, cost of

risk, road transport, storage, overheads, wind-up etc.

5. Conclusions

This study showed that plant species can substantially affect

the total energy yield, energy requirements in the field, energy

ratio (energy use efficiency), net energy yield, and production

cost. Moreover, plant species differ in terms of NUE, which

influence the potential adverse environmental impacts

mainly due to excessive N loading. It was concluded that,

species with low NUE, which is opposite to current directions,

and high WUE (i.e. plant species with relatively low water

demands and great biomass allocation in leaves), are more

suitable when irrigation with strong effluent occur and N

removal is primary objective. Our suggestion for lower

effluent application rates coincide with that derived from

energetic analysis and is in agreement with the current trend

for low energy inputs in agriculture. However, this optionmay

lead to reduction of the biomass produced suggesting that

more land is required to compensate the losses. This might be

infeasible, particularly in areas with high needs in food crops

and/or with high land cost. To mitigate the losses in plant

biomass and reduce the adverse environmental impacts from

nutrients, additional practices should be adopted. Options

may include: a. more intense pretreatment particularly with

respect to N to meet crop needs, b. early planting, c. adjust-

ment of planting density, depended on plant species, envir-

omental conditions, and applied practices, to increase the

contribution of leaves in plant biomass, d. shortening of

harvest cycle or accelarated harvest for annual crops, also, to

ensure higher amount of leaves in plant biomass, e. optimi-

zation of dose-method-timing of irrigation according to plant-

soil capacity to assimilate the applied N (e.g. irrigationmethod

designed to deliver effluent to the area of maximum plant

uptake, multiple irrigation events that should be timed to

coincide to period of maximum plant uptake in daily basis,

decrease or interruption of irrigation late in growing period

when plant growth declines etc.). Extension of analysis to

road transport, storage, overheads, land cost and cost of risk

aswell as to environmental concerns such as gaseousN losses

in the field , in larger scale areas and in different regions, will

consolidate the necessary directions and support the multi-

role of plant species in effluent irrigated bioenergy crop

cultivations.

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Acknowledgments

This work was financed by the EU Coretech project: ICA 3-CT

1999-00012. Thanks are due to K.P. Tsagarakis (Department of

Environmental Engineering Democritus University of Thrace,

Xanthi 67100, Greece) for his contribution regarding the

economic analysis. Also, thanks are due to the Prof. Peter

Cornel (Institute IWAR, Technische Universitat Darmstadt,

Darmstadt, Germany) for his valuable comments and recom-

mendations concerning the manuscript and to Mr. K. Tsiotas

(CRES-Athens) for his contribution to analysis of samples.

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