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Journal of Environmental Management 95 (2012) S188eS192

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Journal of Environmental Management


journal homepage: www.elsevier.com/locate/jenvman

Chemical properties and biological activity in soils of Mallorca following twenty


years of treated wastewater irrigation
Maria Adrover*, Edelweïss Farrús, Gabriel Moyà, Jaume Vadell
Department of Biology, University of the Balearic Islands, 07122 Palma de Mallorca, Spain

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

Article history: On the Mediterranean island of Mallorca, the use of secondary-treated municipal wastewater in irriga-
Received 29 September 2009 tion was introduced with the construction of the first wastewater treatment plants in the 1970s. In this
Received in revised form study, the chemical properties and biological activity of 21 arable soils, irrigated for more than 20 years
8 June 2010
with secondary-treated wastewater, were tested in order to assess their quality. Soil quality was eval-
Accepted 14 August 2010
uated by measuring cation exchange capacity, pH, calcium carbonate equivalent, soil organic matter, total
Available online 19 September 2010
nitrogen, available phosphorus, water-soluble organic carbon, soil microbial biomass, soil basal respi-
ration, and the activities of the enzymes dehydrogenase, b-glucosidase and alkaline phosphatase. No
Keywords:
Wastewater reuse
negative effects of the irrigation treatment were observed on the measured soil parameters. Indeed, soil
Agricultural soils water-soluble organic carbon, soil microbial biomass and b-glucosidase and alkaline phosphatase
Chemical parameters activities increased under treated wastewater irrigation. Biological activity of soils irrigated with treated
Soil microbial biomass wastewater was affected mainly by soil organic matter content. Although the typical crop management
Enzymatic activities of alfalfa, and other forage crops associated with treated wastewater irrigation, may have contributed to
the increase of these parameters, the results suggest that irrigation with treated wastewater is a strategy
with many benefits to agricultural land management.
Ó 2010 Elsevier Ltd. All rights reserved.

1. Introduction reported an increase in soil salinity and Na accumulation, with


higher values associated with longer periods of treated municipal
The use of wastewater for irrigation is well established in arid wastewater irrigation. Such increases in salinity can lead to
and semiarid areas around the world (Hamilton et al., 2007; Qadir a decrease in aggregate stability and soil hydraulic conductivity
et al., 2007). The main advantage of wastewater irrigation, in (Qian and Mecham, 2005), however, the presence of Ca and Mg in
addition to the implied nutrient input, is the constant availability of calcareous soils can mitigate this deleterious effect (Lado and Ben-
this water resource (Toze, 2006; WHO, 2006). Irrigation with Hur, 2009). Schipper et al. (1996) did not observe any changes in
untreated wastewater may increase soil organic matter, nitrogen soil biological and biochemical parameters after 3 years of irriga-
and concentrations of major cations (Siebe, 1998; Angin et al., tion with a tertiary-treated domestic effluent, while Chen et al.
2005). However, it has been associated with negative impacts on (2008) found an enhancement of soil enzyme activities following
health (Gantzer et al., 2001; Rutkowski et al., 2007). Moreover, 10 years of treated municipal wastewater irrigation.
long-term irrigation with untreated wastewater could lead to On the Mediterranean island of Mallorca, irrigation of arable
a heavy metal accumulation, and a consequent loss of soil quality, soils with treated municipal wastewater was introduced in the
depending on the origins of the wastewater (Lucho-Constantino seventies, when the first wastewater treatment plants were built.
et al., 2005; Mapanda et al., 2005). For these reasons, treatment The use of secondary-treated wastewater made the support of
of wastewater is generally recommended before its use in irrigation traditionally irrigated lands possible in areas where the
(Jiménez-Cisneros, 1995; Toze, 2006). groundwater had become saline as a result of seawater intrusion
The effects on soil properties of irrigation with treated waste- into the aquifers (Mateos-Ruiz and Lopez-Garcia, 2003). Such
water over different lengths of time have been studied by several areas have been cultivated with crops destined for animal feed;
authors. Qian and Mecham (2005) and Rusan et al. (2007) each principally alfalfa (Medicago sativa), a pluriannual crop, usually
cultivated for 5e7 years, but also maize (Zea mais) and other
* Corresponding author. Tel.: þ34 971172525; fax: þ34 971173184. forage crops. Irrigation is typically carried out via a process of
E-mail address: maria.adrover@uib.es (M. Adrover). flooding.

0301-4797/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jenvman.2010.08.017
M. Adrover et al. / Journal of Environmental Management 95 (2012) S188eS192 S189

Soil management has an important influence on soil biological organic carbon using a Shimadzu TOC-5000A analyser. Soil micro-
activity: microbial biomass and enzymatic activities are sensitive to bial biomass was determined using a fumigation-extraction proce-
intensive cultivation (Riffaldi et al., 2002), but are stimulated by dure (Vance et al., 1987). Basal respiration was estimated using the
organic matter supply (Pascual et al., 2002). For these reasons, soil method described by Alef (1998), while dehydrogenase, b-glucosi-
biological parameters are considered to be good indicators of soil dase and alkaline phosphatase activities were determined as
quality (Bandick and Dick, 1999). reported by Tabatabai (1982). Dehydrogenase activity was measured
The objective of this study was to evaluate the quality of soils using triphenyltetrazolium chloride as a substrate; samples were
which had been subjected to irrigation by secondary-treated incubated for 24 h at 37  C. b-Glucosidase and alkaline phosphatase
municipal wastewater over a period of more than 20 years using activities were measured using p-nitrophenyl-b-D-glucoside and p-
selected soil chemical and biological indicators. nitrophenyl phosphate as substrates, respectively; samples were
incubated for 1 h at 37  C for both analyses. All measured parameters
were calculated on a dry matter basis.
2. Material and methods
The data generated from the analyses of soils irrigated with
treated wastewater for more than 20 years were compared with data
In July of 2006, one composite sample (consisting of four
from 23 non-wastewater treated agricultural soils that were
randomly collected sub-samples) was taken from the plough layer
sampled and analyzed in July of 2003 for a previous study (Farrús
(0e20 cm) at 21 sites on the island of Mallorca which had been irri-
et al., unpublished data). These agricultural soils included a variety of
gated with secondary-treated wastewater for more than 20 years. All
soil types, mainly Calcisols, but including Regosols and Luvisols, and
of the sites had been farmed conventionally, according to local
were generally cultivated with herbaceous crops. Soil samples from
practice. Although some of the fields were not under cultivation at
both studies were processed following the same methodologies.
the moment of sampling, alfalfa had been the main crop in all of them,
Descriptive statistics and Pearson’s correlations were calculated
and had been rotated with other crops such as maize, barley and oats.
using SPSS 15.0 for Windows. A Student’s independent sample t-test
The study sites were located in the four areas of Mallorca where
was used for comparisons between means when variances were
irrigation with treated wastewater was first introduced. In these
equal and an unequal variance t-test was used when variances were
areas, excessive extraction of local groundwater had led to the
unequal (Ruxton, 2006). The Levene’s test was performed to test for
intrusion of seawater into the aquifers (Lopez-Garcia and Mateos-
homogeneity of variances.
Ruiz, 2003), and secondary-treated wastewater is the only
available source of water, consequently there were no other non-
3. Results and discussion
wastewater irrigated sites available which shared similar
management and could therefore have been utilized as controls.
Data from non-wastewater treated soils were collected from
Calcisols, sometimes associated with Regosols and Luvisols,
different soil types and cropping systems and can be considered as
were the predominant soil types in all the areas of study. Sites were
reference values for a representative range of soils from the island
irrigated by flooding with secondary-treated wastewater from the
of Mallorca. However, the sampling of soils irrigated with treated
closest municipal wastewater treatment plant. Treatment of
wastewater was limited to the few locations where this type of
wastewater was performed with an activated-sludge system in all
irrigation had been established for more than 20 years. Conse-
cases. Selected physical and chemical characteristics of the
quently, less variation was observed in the chemical and biological
secondary-treated wastewater are reported in Table 1.
soil parameters of the soils irrigated with treated wastewater than
Field-moist soil samples were immediately sieved (2 mm),
in those of the non-wastewater treated soils (Table 2).
moistened to water holding capacity and incubated at 25  C for 10
With the exception of soil pH, available phosphorus and water-
days to permit uniform rewetting before the analysis of soil
soluble organic carbon, the chemical properties of soils irrigated
microbial biomass, basal respiration and soil enzymatic activities.
with treated wastewater were generally within the same ranges as
In addition, sub-samples of each soil were air dried and ground for
the non-wastewater treated soils (Table 2). Previous studies, con-
chemical analysis.
cerning soils under long-term irrigation with untreated wastewa-
Cation exchange capacity was measured by the ammonium
ters, have reported an increase in soil C and N contents (Siebe, 1998;
acetate method (Rhoades, 1982). Soil pH was determined in a soil:-
Friedel et al., 2000), and even an increase in cation exchange
water suspension (1:2.5) and percentage of calcium carbonate
capacity (Angin et al., 2005) which can be attributed to the high
equivalent was measured using a Bernard calcimeter. Soil organic
contents of organic compounds in the applied wastewater.
matter was determined by the wet oxidation method with dichro-
However, no such increase was observed when the wastewater was
mate (Nelson and Sommers, 1982), total nitrogen by the Kjeldahl
treated before use (Qian and Mecham, 2005).
method (Bremmer and Mulvaney, 1982) and available phosphorus
Soil pH was significantly higher in soils irrigated with treated
measured using the extraction method of Olsen et al. (1954). Water-
wastewater, compared to non-wastewater treated soils. Signifi-
soluble organic carbon was measured after shaking 8 g of soil with
cantly higher values of available phosphorus and water-soluble
40 ml of distilled water (soil:water; 1:5) for 30 min in an end-to-end
organic carbon were observed in the former group of soils,
shaker. The resulting suspension was centrifuged and the extract
compared to the latter. Such an observed increase in soil pH,
filtered to <0.45 mm. The filtrate was used to determine soluble
following treated wastewater irrigation, concurs with the findings
of other authors (Schipper et al., 1996; Qian and Mecham, 2005),
Table 1 and can be attributed to the additional input of exchangeable
Physical and chemical characteristics of secondary-treated wastewater. cations, mostly sodium, created by the irrigation water (Gelsomino
Mean Standard deviation
et al., 2006). An increase in available soil phosphorus was reported
by Mohammad and Mazahreh (2003), and also by Mandal et al.
pH 7.8 0.4
EC 25  C (dS m1) 2.32 0.77 (2008), in treated wastewater irrigated soils, reflecting the high
SS (mg l1) 17.0 16.6 phosphorus content in the wastewater used. Siebe (1998) and
NH4-N (mg l1) 8.67 11.47 Angin et al. (2005) obtained similar results with untreated waste-
NO3-N (mg l1) 5.42 5.25 water. The increased content of water-soluble organic carbon in the
EC, electrical conductivity; SS, suspended solids. soils irrigated with treated wastewater may be related to the
S190 M. Adrover et al. / Journal of Environmental Management 95 (2012) S188eS192

Table 2 and the soils of the other treatment (Table 2). These differences
Descriptive statistics of biological activity and soil properties. Comparison between could be attributed to the wastewater irrigation, as was observed by
treated wastewater (1) and non-wastewater irrigated soils (2).
Filip et al. (1999) who found higher enzymatic activities in soils
T n Mean Standard deviation Sig irrigated with untreated wastewater over 100 years compared to
CEC 1 21 15.3 4.7 non-irrigated soils. Friedel et al. (2000) observed a similar increase
2 23 17.2 6.1 in microbial biomass and dehydrogenase activity in Vertisols which
pH 1 21 8.5 0.2 <0.001
had been irrigated on a long-term basis with untreated wastewater.
2 23 8.2 0.2
CaCO3 1 21 39.6 14.7 Brzezinska et al. (2006) and Truu et al. (2009) reported a significant
2 23 41.0 20.7 increase of alkaline phosphatase in soils irrigated with treated
SOM 1 21 3.28 0.75 wastewater over shorter periods of time (4 and 3 years, respec-
2 23 3.14 1.66 tively) and Chen et al. (2008) observed an enhancement of various
N 1 21 0.20 0.04
2 23 0.18 0.08
enzymatic activities in soils irrigated with treated wastewater over
C/N 1 21 9.5 0.5 10 years. The positive effect of treated wastewater irrigation on soil
2 23 9.9 1.5 microbial biomass and its associated activities can be attributed to
P 1 21 86.2 36.0 0.034 the addition of easily decomposable organic matter and nutrients
2 23 55.1 55.0
(Friedel et al., 2000; Chen et al., 2008). Nevertheless, the effect of
WSOC 1 21 44.8 16.2 0.037
2 23 35.1 13.9 crop type on microbial biomass and enzymatic activities must also
MB 1 21 658 200 0.017 be taken into consideration. According to Dodor and Tabatabai
2 508 200 (2005), cropping systems that leave residues on the soil surface
BR 1 21 5.57 1.90 will enhance enzyme activity. The highest values of b-glucosidase
2 23 4.99 1.96
DH 1 21 1.60 0.55
activity obtained by these authors were found in soils directly
2 23 1.15 0.95 below an alfalfa crop. Similarly, Truu et al. (2009) suggested a co-
GL 1 21 2.44 1.13 <0.001 effect of municipal wastewater and vegetation on the soil microbial
2 23 1.04 0.62 community.
AP 1 21 7.66 2.99 <0.001
Some basic chemical properties of the soils irrigated with
2 23 3.33 1.63
treated wastewater were statistically correlated. The highest
T, treatment; n, number of samples; Sig, significance; CEC, cation exchange capacity correlation was found between soil organic matter and nitrogen
(cmol kg1); CaCO3, calcium carbonate equivalent (%); SOM, soil organic matter (%); N,
total nitrogen (%); P, available phosphorus (mg kg1); WSOC, water-soluble organic
content (Table 3) and this was also highly correlated in the non-
carbon (mg kg1); MB, soil microbial biomass (mg C kg1); BR, basal respiration wastewater treated soils (Table 4). Soil organic matter was also
(mg CO2 kg1 h1); DH, dehydrogenase activity (mmol tryphenylformazan kg1 24 h1); strongly correlated with cation exchange capacity and with all the
GL, b-glucosidase activity (mmol PNP kg1 h1); AP, alkaline phosphatase activity parameters related to biological activity in both groups of soils
(mmol p-nitrophenol kg1 h1).
(Tables 3 and 4). However, high correlations of soil organic matter
All values based on soil dry weight.
with available phosphorus and water-soluble organic carbon were
observed only in the non-wastewater treated soils (Table 4). This
suggests that the available phosphorus and water-soluble organic
presence of dissolved organic matter (cell fragments and macro- carbon in these soils are the result of soil organic matter mineral-
molecules) in the water (Shon et al., 2006). However, land use and ization, while the soils irrigated with treated wastewater may
management practices can also have a considerable effect on this receive these elements directly from the irrigation water itself.
parameter (Chantigny, 2003). For example, water-soluble organic Negative correlations between pH and calcium carbonate
carbon tends to increase under perennial crops such as alfalfa (Wu equivalent with soil organic matter and biological parameters were
et al., 2003), which is one of the most common crops in the soils found in soils irrigated with treated wastewater (Table 3). These
irrigated with treated wastewater on Mallorca. results indicate a soil type effect and can be explained by the low
Soil microbial biomass was significantly higher in soils irrigated biological activity of Calcareous Regosols (Adrover et al., 2007).
with treated wastewater, when compared to that found in the other Soil microbial biomass was highly correlated with dehydroge-
soils, although no differences were observed in basal respiration nase and b-glucosidase activities. Dehydrogenase is an intracellular
and dehydrogenase activity between the two treatments. In addi- enzyme which is involved in microbial oxidoreductase metabolism.
tion, there were strong differences in b-glucosidase and alkaline The high correlation of this enzyme with soil microbial biomass has
phosphatase activities between treated wastewater irrigated soils been widely reported (García-Gil et al., 2000; Taylor et al., 2002). b-

Table 3
Correlations between soil properties and biological activity in long-term treated wastewater irrigated soils of Mallorca.

pH CaCO3 SOM N P WSOC MB BR DH GL AP


CEC 0.608** e 0.851*** 0.821*** e e 0.860*** 0.707*** 0.521* 0.860*** 0.685**
pH 0.457* 0.540* 0.513* 0.509* e 0.470* 0.614** e 0.593** e
CaCO3 e 0.525* e e e 0.511* 0.578** 0.493* e
SOM 0.978*** e e 0.783*** 0.737*** 0.725*** 0.802*** 0.730***
N e e 0.778*** 0.714*** 0.759*** 0.791*** 0.740***
P e e e e e e
WSOC e e e e e
MB 0.650** 0.735*** 0.735*** 0.473*
BR 0.682** 0.745*** e
DH 0.636** 0.610**
GL 0.611**

CEC, cation exchange capacity; CaCO3, calcium carbonate equivalent; SOM, soil organic matter; N, total nitrogen; P, available phosphorous; WSOC, water-soluble organic
carbon; MB, soil microbial biomass; BR, basal respiration; DH, dehydrogenase activity; GL, b-glucosidase activity; AP, alkaline phosphatase activity.
***, **, *Correlations are significant at p < 0.001, p < 0.01, p < 0.05, respectively.
M. Adrover et al. / Journal of Environmental Management 95 (2012) S188eS192 S191

Table 4
Correlations between soil properties and biological activity in non-wastewater treated agricultural soils of Mallorca.

pH CaCO3 SOM N P WSOC MB BR DH GL AP


CEC e 0.812*** 0.669*** 0.670*** e 0.503* 0.581** 0.629** 0.547* e e
pH 0.466* e e e e e e e e e
CaCO3 0.454* 0.519* e e e e 0.500* e e
SOM 0.961*** 0.646** 0.845*** 0.553** 0.812*** 0.734*** 0.501* 0.772***
N 0.704*** 0.839*** 0.525* 0.770*** 0.659** e 0.679***
P 0.676*** e 0.506* e e e
WSOC 0.496 0.767*** 0,454* e 0.662**
MB 0.746*** 0.660** 0.601** 0.715***
BR 0.760*** 0.666** 0.734***
DH 0.754*** 0.777***
GL 0.636**

CEC, cation exchange capacity; CaCO3, calcium carbonate equivalent; SOM, soil organic matter; N, total nitrogen; P, available phosphorous; WSOC, water-soluble organic
carbon; MB, soil microbial biomass; BR, basal respiration; DH, dehydrogenase activity; GL, b-glucosidase activity; AP, alkaline phosphatase activity.
***, **, *Correlations are significant at p < 0.001, p < 0.01, p < 0.05, respectively.

Glucosidase is an enzyme involved in the degradation of cellulose, management at each location. Thus, treated wastewater use in
the main component of plant residues. The high correlation of b- irrigation can have positive effects, not only in aspects of soil
glucosidase and soil microbial biomass in both groups of soils, also quality, but also in social terms, as it allows the maintenance of
reported by Turner et al. (2002), suggests that the total and extra- irrigated agriculture in areas where groundwater has been polluted
cellular activity of this enzyme are mainly associated with microbial by seawater intrusion.
biomass in soils (Dodor and Tabatabai, 2005). b-Glucosidase was also
strongly correlated with cation exchange capacity and soil organic
matter (Table 3). These results are in agreement with Turner et al. Acknowledgements
(2002), who suggested that b-glucosidase activity can provide
a meaningful integrative measure of physico-chemical and biolog- The authors thank Dr. B. Jiménez and Dr. M. Truu for their
ical soil quality parameters, and who proposed the use of this constructive review, Dr. E. Baraza for her contribution, and Mr. K.
parameter in monitoring soil biological quality. Alkaline phospha- MacMillan for the English language revision.
tase was strongly correlated with soil organic matter and total
nitrogen content (Tables 3 and 4). Deng and Tabatabai (1997)
obtained significant correlations between organic carbon and References
phosphatases; suggesting that organic matter plays an important
role in protecting and maintaining soil enzymes in their active forms. Adrover, M., Moyà, G., Vadell, J., 2007. Efecto del riego con agua residual tratada
sobre la actividad biológica de tres suelos. In: Bellifante, N., Jordán, A. (Eds.),
The use of treated wastewater for agriculture has been imple- Tendencias Actuales de la Ciencia del Suelo. Universidad de Sevilla, Sevilla, pp.
mented in other areas affected by seawater intrusion into the aqui- 546e553.
fers (Anderson, 2003; Bixio et al., 2006), because, in addition to Alef, K., 1998. Soil Respiration. In: Alef, K., Nannipieri, P. (Eds.), Methods in Applied
Soil Microbiology and Biochemistry. Academic Press, San Diego, pp. 216e217
implying a reduction in groundwater extraction for agricultural (Chapter 5).
uses, it provides a groundwater recharge via percolation through the Anderson, J., 2003. The environmental benefits of water recycling and reuse. Water
soil and the vadose zone (Durham et al., 2002; Asano and Cotruvo, Sci. Technol: Water Supply 3, 1e10.
Angelakis, A.N., Marecos do Monte, M.H.F., Bontoux, L., Asano, T., 1999. The status of
2004). Moreover, treated wastewater is not only a low cost source
wastewater reuse practice in the Mediterranean basin: need for guidelines.
of water, but also a source of nutrients for plant growth (Vazquez- Water Res. 33, 2201e2217.
Montiel et al., 1996). Irrigation with treated wastewater may Angin, I., Yaganoglu, A.V., Turan, M., 2005. Effects of long-term wastewater irriga-
reduce the demand for synthetic fertilizers and may contribute to tion on soil properties. J. Sustain. Agric. 26, 31e42.
Asano, T., Cotruvo, J.A., 2004. Groundwater recharge with reclaimed municipal
a decrease in the level of nutrients in rivers. Moreover, it may wastewater: health and regulatory considerations. Water Res. 38, 1941e1951.
eliminate the need for expensive tertiary treatment and facilitate the Bandick, A.K., Dick, R.P., 1999. Field management effects on soil enzyme activities.
sustainable development of landscape and agricultural irrigation Soil Biol. Biochem. 31, 1471e1479.
Bixio, D., Thoeye, C., De Koning, J., Joksimovic, D., Savic, D., Wintgens, T., Melin, T.,
(Angelakis et al., 1999). For these reasons, the use of treated waste- 2006. Wastewater reuse in Europe. Desalination 187, 89e101.
water for irrigation should be expanded in order to preserve fresh Bremmer, J.M., Mulvaney, C.S., 1982. Nitrogen e Total. In: Page, A.L., Miller, R.H.,
water resources and increase waste recycling. The forage crops Keeney, D.R. (Eds.), Methods of Soil Analysis. Part 2. Chemical and Microbio-
logical Properties. Agronomy No. 9, pp. 595e624. Madison.
associated with treated wastewater irrigation contribute to the Brzezinska, M., Tiwari, S.C., Stepniwska, Z., Nosalewicz, M., Bennicelli, R.P.,
sustainability of an acceptable soil quality, however, more infor- Samborska, A., 2006. Variation of enzyme activities, CO2 evolution and redox
mation is needed concerning the consequences of utilizing this type potential in an Eutric Histosol irrigated with wastewater and tap water. Biol.
Fertil. Soils 43, 131e135.
of water in the irrigation of soils cultivated with other crops. Chantigny, M.H., 2003. Dissolved and water-extractable organic matter in soils:
a review on the influence of land use and management practices. Geoderma
4. Conclusions 113, 357e380.
Chen, W., Wu, L., Frankenberger, W.T., Chang, A.C., 2008. Soil enzyme activities of
long-term reclaimed wastewater-irrigated soils. J. Environ. Qual. 37, S-36eS-42.
After more than 20 years of treated wastewater irrigation, no Deng, S.P., Tabatabai, M.A., 1997. Effect of tillage and residue management on
negative changes have been observed in the evaluated soil prop- enzyme activities in soils: III. Phosphatases and arylsulfatase. Biol. Fertil. Soils
24, 141e146.
erties of the island of Mallorca, with the exception of an increase in
Dodor, D.E., Tabatabai, M.A., 2005. Glycosidases in soils as affected by cropping
soil pH caused by greater sodium supply. The enhancement in soil systems. J. Plant Nutr. Soil Sci. 168, 749e758.
microbial biomass, b-glucosidase activity and alkaline phosphatase Durham, B., Rinck-Pfeiffer, S., Guendert, D., 2002. Integrated water resource
activity, in addition to relatively higher values of water-soluble management e through reuse and aquifer recharge. Desalination 152, 333e338.
Filip, Z., Kanazawa, S., Berthelin, J., 1999. Characterization of effects of a long-term
organic carbon and available phosphorus, can be attributed to wastewater irrigation on soil quality by microbiological and biochemical
a combination of the irrigation regime and the agricultural parameters. J. Plant Nutr. Soil Sci. 162, 409e413.
S192 M. Adrover et al. / Journal of Environmental Management 95 (2012) S188eS192

Friedel, J.K., Langer, T., Siebe, C., Stahr, K., 2000. Effects of long-term waste water Qadir, M., Sharma, B.R., Bruggeman, A., Choukr-Allah, R., Karajeh, F., 2007. Non-
irrigation on soil organic matter, soil microbial biomass and its activities in conventional water resources and opportunities for water augmentation to
central Mexico. Biol. Fertil. Soils 31, 414e421. achieve food security in water scarce countries. Agric. Water Manage. 87, 2e22.
Gantzer, C., Gillerman, L., Kuznetsov, M., Oron, G., 2001. Adsorption and survival of Qian, Y.L., Mecham, B., 2005. Long-term effects of recycled wastewater irrigation on
faecal coliforms, somatic coliphages and F-specific RNA phages in soil irrigated soil chemical properties on golf course fairways. Agron. J. 97, 717e721.
with wastewater. Water Sci. Technol. 43, 117e124. Riffaldi, R., Saviozzi, A., Levi-Minzi, R., Cardelli, R., 2002. Biochemical properties of
García-Gil, J.C., Plaza, C., Soler-Rovira, P., Polo, A., 2000. Long-term effects of a Mediterranean soil as affected by long-term crop management systems. Soil
municipal solid waste compost application on soil enzyme activities and Till. Res. 67, 109e114.
microbial biomass. Soil Biol. Biochem. 32, 1907e1913. Rhoades, J.D., 1982. Cation Exchange Capacity. In: Page, A.L., Miller, R.H.,
Gelsomino, A., Badalucco, L., Ambrosoli, R., Crecchio, C., Puglisi, E., Meli, S.M., 2006. Keeney, D.R. (Eds.), Methods of soil analysis. Part 2. Chemical and Microbio-
Changes in chemical and biological soil properties as induced by anthropogenic logical Properties. Agronomy No. 9, pp. 149e152. Madison.
disturbance: a case study of an agricultural soil under recurrent flooding by Rusan, M.J.M., Hinnawi, S., Rousan, L., 2007. Long term effect of wastewater irri-
wastewaters. Soil Biol. Biochem. 38, 2069e2080. gation of forage crops on soil and plant quality parameters. Desalination 215,
Hamilton, A., Stagnitti, F., Xiong, X., Kreidl, S.L., Benke, K.K., Maher, P., 2007. 143e152.
Wastewater irrigation: the state of play. Vadose Zone J. 6, 823e840. Rutkowski, T., Raschid-Sally, L., Buechler, S., 2007. Wastewater irrigation in the
Jiménez-Cisneros, B., 1995. Wastewater reuse to increase soil productivity. Water developing world e two case studies from the Kathmandu Valley in Nepal.
Sci. Technol. 32, 173e180. Agric. Water Manage. 88, 83e91.
Lado, M., Ben-Hur, M., 2009. Treated domestic sewage irrigation effects on soil hydraulic Ruxton, G.D., 2006. The unequal variance t-test is an underused alternative to
properties in arid and semiarid zones: a review. Soil Till. Res. 106, 152e163. Student’s t-test and the ManneWhitney U test. Behav. Ecol. 17, 688e690.
Lopez-Garcia, J.M., Mateos-Ruiz, R.M., 2003. La intrusión marina en los acuíferos de Siebe, C., 1998. Nutrient inputs to soils and their uptake by alfalfa through long-
la isla de Mallorca. Tecnología de la intrusión de agua de mar en acuíferos term irrigation with untreated sewage effluent in Mexico. Soil Use Manage. 14,
costeros: Países mediterráneos. IGME, Madrid. 119e122.
Lucho-Constantino, C.A., Álvarez-Suárez, M., Beltrán-Hernández, R.I., Prieto- Schipper, L.A., Williamson, J.C., Kettles, H.A., Speir, T.W., 1996. Impact of land-
García, F., Poggi-Varaldo, H.M., 2005. A multivariate analysis of the accu- applied tertiary-treated effluent on soil biochemical properties. J. Environ. Qual.
mulation and fractionation of major and trace elements in agricultural soils 25, 1073e1077.
in Hidalgo State, Mexico irrigated with raw wastewater. Environ. Int. 31, Shon, H.K., Vigneswaran, S., Snyder, S.A., 2006. Effluent organic matter (EfOM) in
313e323. wastewater: constituents, effects, and treatment. Crit. Rev. Environ. Sci. Technol.
Mandal, U.K., Warrington, D.N., Bhardwaj, A.K., Bar-Tal, A., Kautsky, L., Minz, D., 36, 327e374.
Levy, G.J., 2008. Evaluating impact of irrigation water quality on a calcareous Tabatabai, M.A., 1982. Soil Enzymes. In: Page, A.L., Miller, R.H., Keeney, D.R. (Eds.),
clay soil using principal component. Geoderma 144, 189e197. Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties.
Mapanda, F., Mangwayana, E.N., Nyamangara, J., Giller, K.E., 2005. The effects of Agronomy No. 9, pp. 903e947. Madison.
long-term irrigation using wastewater on heavy metal contents of soils under Taylor, J.R., Wilson, B., Mills, M.S., Burns, R.G., 2002. Comparison of microbial
vegetables in Harare, Zimbabwe. Agric. Ecosyst. Environ. 107, 151e165. numbers and enzymatic activities in surface soils and subsoils using various
Mateos-Ruiz, R.M., Lopez-Garcia, J.M., 2003. Retroceso de la intrusión marina techniques. Soil Biol. Biochem. 34, 387e401.
debido a la substitución de aguas subterráneas por aguas residuales tratadas Toze, S., 2006. Reuse of effluent water e benefits and risks. Agric. Water Manage. 80,
para el regadío de una zona agrícola. El Pla de Sant Jordi. Tecnología de la 147e159.
intrusión de agua de mar en los acuíferos costeros: Países mediterráneos, IGME, Truu, M., Truu, J., Heinsoo, K., 2009. Changes in soil microbial community under
Madrid. willow coppice: the effect of irrigation with secondary-treated municipal
Mohammad, M.J., Mazahreh, N., 2003. Changes in soil fertility parameters in wastewater. Ecol. Eng. 35, 1011e1020.
response to irrigation of forage crops with secondary treated wastewater. Turner, B.L., Hopkins, D.W., Haygarth, P.M., Ostle, N., 2002. b-Glucosidase activity in
Comm. Soil Sci. Plant Anal. 34, 1281e1294. pasture soils. Appl. Soil Ecol. 20, 157e162.
Nelson, D.W., Sommers, L.E., 1982. Total Carbon, Organic Carbon, and Organic Vance, F., Brookes, P., Jenkinson, D., 1987. Microbial biomass measurements in forest
Matter. In: Page, A.L., Miller, R.H., Keeney, D.R. (Eds.), Methods of Soil Analysis. soils. The use of the chloroform fumigation-incubation method in strongly acid
Part 2. Chemical and Microbiological Properties. Agronomy No. 9, pp. 539e579. soils. Soil Biol. Bicochem. 19, 697e702.
Madison. Vazquez-Montiel, O., Horan, N.J., Mara, D.D., 1996. Management of domestic
Olsen, S.R., Cole, C.V., Watanabe, F.S., Dean, L.A., 1954. Estimation of Available wastewater for reuse in irrigation. Water Sci. Technol. 33, 355e362.
Phosphorus in Soils by Extraction with Sodium Bicarbonate. U.S. Dep. of Agric. WHO, 2006. Wastewater Use in Agriculture. In: WHO Guidelines for the Safe Use of
Circ., 939. Wastewater, Excreta and Greywater, vol. II.
Pascual, J.A., Moreno, J.L., Hernández, T., García, C., 2002. Persistence of immobilised Wu, T., Schoenau, J.J., Li, F., Qian, P., Malhi, S.S., Shi, Y., 2003. Effect of tillage and
and total urease and phosphatase activities in a soil amended with organic rotation on organic carbon forms of chernozemic soils in Saskatchewan. J. Plant
wastes. Biores. Technol. 82, 73e78. Nutr. Soil Sci. 166, 328e335.

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