impact of salinity on soil biological activities: a laboratory experiment

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Impact of Salinity on Soil BiologicalActivities: A Laboratory ExperimentAlessandro Saviozzi a , Roberto Cardelli a & Raffaella Di Puccio aa Department of Agricultural Chemistry and Biotechnology,University of Pisa, Pisa, ItalyPublished online: 06 Feb 2011.

To cite this article: Alessandro Saviozzi , Roberto Cardelli & Raffaella Di Puccio (2011) Impact ofSalinity on Soil Biological Activities: A Laboratory Experiment, Communications in Soil Science andPlant Analysis, 42:3, 358-367, DOI: 10.1080/00103624.2011.542226

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Communications in Soil Science and Plant Analysis, 42:358–367, 2011Copyright © Taylor & Francis Group, LLCISSN: 0010-3624 print / 1532-2416 onlineDOI: 10.1080/00103624.2011.542226

Impact of Salinity on Soil Biological Activities:A Laboratory Experiment

ALESSANDRO SAVIOZZI, ROBERTO CARDELLI, ANDRAFFAELLA DI PUCCIO

Department of Agricultural Chemistry and Biotechnology, University of Pisa,Pisa, Italy

In a laboratory study, the impact of sodium chloride (NaCl) on soil quality was exam-ined through the monitoring of soil biological activity. Artificially salinized sampleswere prepared from the nonsaline soil by adding NaCl at electrical conductivities (EC)2, 4, and 8 dS·m−1 in saturated extracts. The samples were kept at 25 ◦C and at 50%field capacity during an incubation period of 40 days. The ATP, soil basal respiration,protease, amylase, alkaline phosphatase, dehydrogenase, and catalase activities weremonitored. The biological index of fertility (BIF), the enzyme activity number (EAN),and the metabolic potential (MP) were calculated. A regression analysis was used tocalculate parameters from cumulative data of carbon dioxide (CO2) evolution. The sizeof microbial biomass, measured throughout the determination of ATP, was decreasedby increasing salinity. Increasing concentrations of salt up to an EC of 4 dS·m−1 led toan increase of soil respiration. During incubation, protease and dehydrogenase wereinhibited by NaCl; however, amylase, alkaline phosphatase, and catalase were notaffected by the salt addition. Between indices, EAN confirmed the general depressiveeffect of NaCl on the biological properties of soil, while MP showed a pattern similarto that of soil respiration. Results of this study chiefly indicate that ATP, soil respira-tion, protease, dehydrogenase, EAN, and MP were able to put in evidence the effectsof NaCl on soil biological activity and may be regarded as suitable tools to show thephysiological reaction of soil microbial biomass under saline stress.

Keywords Agricultural soil, ATP, NaCl, soil enzyme activities, soil respiration

Introduction

Formation of salt-affected soils is an important factor leading to soil degradation and yielddecline (Haynes and Hamilton 1999; Van Antwerpen and Meyer 1996).

Cultivation practices can result in changes in soil salinity because fertilizers, manures,soil amendments, and irrigation with water affected by salt may lead to an increase of saltconcentration in the soil (Levi-Minzi et al. 1998; Szabolcs 1986). An additional mechanismof salt accumulation in areas near marine coastlines is the supply of salts through sprayfrom the sea, carried inland by the wind (Ballantyne 1978).

Soil biological activity is often concentrated in the top few centimetres of soil(Murphy, Sparling, and Fillery 1998), and changes in soil, such as increased salinity, may

Received 16 June 2009; accepted 20 March 2010.Address correspondence to Roberto Cardelli, Department of Agricultural Chemistry and

Biotechnology, University of Pisa, Via del Borghetto 80, 56124 Pisa, Italy. E-mail: [email protected]

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Salinity and Soil Biological Activities 359

strongly affect soil biological properties. Because biological activity in soil is central to itsecological function, any reduction in activity is of particular concern.

The influence of salt as a major stress to soil microorganisms has been the subjectof several studies (Mamilov et al. 2004; Pankhurst et al. 2001; Sardinha et al. 2003;Sarig and Steinberger 1994). A decrease in carbon dioxide (CO2) production, enzymeactivities, or microbial biomass in soil has often been observed in the field (Pathak andRao 1998) and under laboratory incubations (Ghollarata and Raiesi 2007; Rietz andHaynes 2003; Wichern, Wichern, and Joergensen 2006). Soil enzyme activities werefound to decrease with increasing salinity but the degree of inhibition varied amongthe enzymes assayed and the amount of salt added (Frankenberger and Bingham 1982).The same authors observed that dehydrogenase (oxydoreductase) activity was severelyinhibited by salinity, whereas the hydrolases (amidase, urease, acid and alkaline phos-phatase, phosphodiesterase, inorganic pyrophosphatase, rhodanase, α-glucosidase, andα-galactosidase) showed much less inhibition. In contrast, Garcia and Hernandez (1996)reported that the activity of hydrolases, such as protease, β-glucosidase, and phosphatase,was more negatively affected by salinity than that of oxidoreductases (dehydrogenase andcatalase).

Increasing salinity thus has detrimental effects on biologically mediated processesin the soil, such as soil respiration (Ghollarata and Raiesi 2007; Pathak and Rao 1998).Despite this, soil microorganisms have the ability to adapt or tolerate osmotic stress causedby salinity (Sparling, West, and Reynolds 1989).

Some soil quality indices have been developed using biochemical properties to addressimportant ecological functions, such as decomposition and nutrient cycling. These includethe biological index of fertility (BIF) (Stefanic, Eliade, and Chirnogeanu 1984), the enzymeactivity number (EAN) (Beck 1984), and the metabolic potential (MP) (Masciandaro,Ceccanti, and Gallardo-Lancho 1998), which could be suitable tools for studying thephysiological reaction of the soil biomass under saline stress.

While the effects of salinity on soil chemical and physical properties and plant growthare well known, their effects on soil biological characteristics remain relatively unstudied,and there is limited information and poor consistency in studies of the salt effects on soilmicrobial activity. The objectives of this study were (i) to document the impact of gradientsin salinity by sodium chloride (NaCl) on selected biological activities of soil and (ii) toidentify the most meaningful indicators that could be used to evaluate salt effects on soilbiological activity.

Materials and Methods

A Typic Xerorthent soil was collected from the top 15 cm of the soil surface at theInterdepartimental Centre “E. Avanzi” of Pisa University. Selected chemical and physicalcharacteristics of the soil [pH, texture, carbonate content, cation exchange capacity (CEC),and total nitrogen (N)] were determined by standard methods (MAAF 1994); organic Cwas determined after removing carbonate C (Nelson and Sommers 1982) by dry combus-tion (induction furnace 900 CS, Eltra Gmbh, Germany). Results are reported in Table 1.

Artificially salinized subsamples were prepared from the nonsaline soil. For this pur-pose, three different independent replicates of the nonsaline soil were treated with NaClsolution up to EC 2, 4, and 8 dS·m−1 in saturated extracts. The soil samples, placed in250-mL beakers, were watered at appropriate intervals to maintain a constant moisturelevel (50% of water-holding capacity), closed with Parafilm to permit gaseous exchange,and incubated at 25 ± 1 ◦C for 40 days.

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360 A. Saviozzi, R. Cardelli, and R. Di Puccio

Table 1Main characteristics of the soil

Parameter Value

Sand (g·kg−1) 659Silt (g·kg−1) 226Clay (g·kg−1) 115Organic C (g·kg−1) 9.63Total N (g·kg−1) 1.02CaCO3 (g·kg−1) 56.1pH 8.2CEC (cmoles(+)·kg−1) 7.5C/N 9.4EC (dS·m−1) 0.8

No variations were observed on soil pH following the addition of NaCl.The activities were determined as follows: dehydrogenase activity (DHA, µg triph-

enylformazan g−1 h−1) was determined by the procedure described by Casida, Klein, andSantoro (1964); catalase activity (CA, % O2 g−1 3 min−1) according to Beck (1971); alka-line phosphatase activity (AF, µg paranitrophenol g−1 h−1) according to Tabatabai andBremner (1969); amylase activity (AM, µg glucose g−1 24 h−1) according to Cardelliet al. (2001); and protease activity (PR, µg tyrosine g−1 2 h−1) following the proceduredescribed by Ladd and Butler (1972).

Biological indices were calculated as follows:

BIF: (DHA + k CA) / 2, where k is a proportionality coefficient (Stefanic, Eliade, andChirnogeanu 1984).

EAN 0.2 (DHA + CA / 10 + AF / 40 + PR / 2 + AM / 20) (Beck 1984).MP: DHA / 1. 10−4 DOC (Masciandaro, Ceccanti, and Gallardo-Lancho 1998).

The dissolved organic carbon (DOC, µg g−1) was determined on a soil/watersuspension of 1:50 and measured by dichromate (Ciavatta et al. 1991).

ATP from soil samples was extracted using an acidic mixture consisting of 0.67 Mphosphoric acid (H3PO4), 2 M urea, 20% dimethylsulphoxide (DMSO), 20 mM ethylene-diaminetetraacetic acid (EDTA), and 0.02% (w/w) adenosine. The acidic mixture wasadded to the soil at the mixture ratio of soil/extractant 1:10 and sonicated at 60% of ampli-tude with a 500-W ultrasonic processor for 2.5 min; all extracts were buffered with 0.2 MTris and 4 mM EDTA solution. The light output was measured on a Luminoskan Tl Plusluminometer (Labsystems, Frankfurt, Germany), according to the procedure reported byCiardi and Nannipieri (1990).

The results reported are the means of determinations made on three replicates.Analysis of variance was performed, and means were separated with a least significantdifference (LSD) test at the 5% level. All data were expressed on the basis of oven-dryweight of soil.

Soil basal respiration was monitored in a laboratory aerobic incubation procedureover 6 weeks, through the daily measurement of CO2 evolution: 100 g of soil alone ormixed with NaCl solution were placed in 300-mL glass containers closed with rubberstoppers, moistened at 50% of the maximum water-holding capacity, and incubated at

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25 ± 1 ◦C. Glass vials holding 20 mL of 0.5 M sodium hydroxide (NaOH) to trap theevolved CO2 were placed in the containers. The excess alkali was titrated with standard 0.5M hydrochloric acid (HCl) after precipitating the carbonate with a 1.5 M barium chloride(BaCl2) solution. The bottles were opened daily to replenish the NaOH for CO2 absorptionso that composition was not inhibited by lack of O2. CO2-free water was added at appropri-ate intervals to maintain the moisture of the soil at the original level. The experiment wasperformed in two replicates; the mean coefficient of variation (i.e., the standard deviationas percentage of the average values) was always less than 3%.

A nonlinear least-square regression analysis was used to calculate parameters fromcumulative data of C mineralization. The first-order kinetics equation was used to calculatethe potentially mineralizable C (C0):

Cm = C0(1 − e−kt

)

where Cm is the organic C mineralized at any specific time t, and k is the first-order rateconstant. The coefficients of determination (R2) were used to evaluate the goodness ofmodel fit.

Results and Discussion

At the first sampling time (day 1), values of ATP, index of microbial biomass size, weresimilar within the salinized samples and slightly but significantly greater compared tothe not-salted treatment (Table 2). Several authors (Knight and Skujins 1981; Polonenko,Mayfield, and Dumbroff 1981; Sarig, Ruberson, and Firestone 1993; Garcia and Hernandez1996; Li et al. 2006) also noticed microbial increase with increased salinity. The signifi-cant increase in ATP of the treated samples in the early stage of incubation may be dueto the stimulation of osmotic stress, which is known to cause proliferation of microbialcells (Sarig and Steinberger 1994). However, already at day 20, ATP decreased with val-ues not different from the control. A significant reduction of ATP below control valuesoccurred on day 40, mainly in soil samples with the two greatest EC values, showing avalue of about 70% that of the control. The results suggest that soil ATP (i.e., the sizeof the microbial population) can be negatively affected by high levels of NaCl, confirm-ing a pattern found in naturally saline soils where the size of the microbial community isusually negatively related with the amount of soluble salts (Mallouhi and Jacquin 1985;Ragab 1993).

Table 2Changes in time of ATP content (ng·g−1) in the soil with different

levels of NaCl addition

Treatments 1 day 20 days 40 days

Control 30.16 cde 31.96 bcd 34.06 abcEC 2 37.55 a 31.19 cde 30.69 cdeEC 4 37.72 a 30.68 cde 24.38 fgEC 8 34.01 abc 28.40 def 24.14 g

Note. Different letters indicate the differences at a 5% probability level according to theLSD-F multiple-range test.

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Microbial activity, as measured by basal respiration, was influenced by the additionof saline solutions, even at the lowest concentrations (Figure 1). Increasing concentrationsof salt, up to an EC of 4 dS·m−1, stimulated the cumulative amount of CO2 released fromsoil. This pattern was only partially reversed at the greatest salt concentration. However, ascan be seen in Figure 1, the value of CO2-C production exceeded the value detected in thecontrol, although to a small extent, according to the finding of Nelson, Ladd, and Oades(1996), Pathak and Rao (1998), and Singh, Agarwal, and Kanehiro (1969). These resultsindicate that a greater proportion of substrate C is lost as CO2 through increased respiratoryactivity under salt treatment. Thus, it can be argued that the increasing salinity resultedin a smaller microbial community, as demonstrated by ATP (Table 2), which was morestressed and less efficient in using C resources. Probably, soil microorganisms expendedmore energy to maintain higher basal respiration. Similarly, Garcia, Hernandez, and Costa(1994) recorded a negative correlation between the metabolic quotient (soil respiration permicrobial biomass C) and salinity in arid soils of southeastern Spain, indicating that factorsthat cause stress to the microbial biomass also tend to reduce its size.

The trends of CO2 evolution from control and treated soils conformed well to theexponential first-order model Cm = C0(1 − e−kt). Parameters calculated according to themodel are shown in Table 3. As can be seen, the Co values ranged from a minimum of117.9 for control to a maximum of 132.1 mg·100g−1 for EC 4. The results confirm thepattern of the cumulative amount of CO2 released from soil (Figure 1).

Control E.C. 2 E.C. 4 E.C. 875

80

85

90

95

100

mg

C-C

O2

. g−1

soil

Figure 1. Cumulative CO2 evolution after 40 days from the soil with different levels of NaCladdition.

Table 3Parameter estimates according to the first-order model for C mineralization of

the soil with different levels of NaCl addition

Treatments C0 k R2

Control 117.9 0.032 0.986EC 2 124.6 0.031 0.990EC 4 132.1 0.033 0.989EC 8 124.3 0.032 0.983

C0 = potentially mineralizable organic C (amount present at t = 0)(mg C-CO2·100g−1).K = rate constant (day−1).R2 = coefficient of determination.

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Rate constants for C mineralization were similar among the treatments, with valuesfalling within a narrow range: from 0.31 for dose 1 to 0.33 day−1 for EC 4 (Table 3).This suggests that the tested NaCl concentrations were unable to change the pattern of soilrespiration over time.

Frankenberger and Bingham (1982) reported that dehydrogenase (oxidoreductase)was more inhibited by salinity than hydrolases. In contrast, Garcia and Hernandez (1996)reported that the activity of hydrolases, such as protease, β-glucosidase, and phosphatase,was more negatively affected by salinity than that of oxidoreductases (dehydrogenase andcatalase). Concerning the effect on hydrolases, in our study the activity of protease wasinhibited notably at the first sampling time with increasing salinity (Table 4), with valuesof 83, 63, and 42% lower, respectively, than those of the control. A substantial recoveryof activity was already observed on day 20, with values of samples treated with the twolow rates of salt addition similar to that of control. However, at the end of incubation onlythe sample treated with the lowest dose of NaCl was significantly similar to that of theuntreated sample, whereas at EC 4 and 8 the activities were 71 and 52% less, respectively,than that of the control.

In contrast to protease, little inhibitory effect of increasing EC was detected on bothamylase and alkaline phosphatase (Table 5). The activities of the amylase and alkalinephosphatase did not differ substantially from the relative controls during the whole incuba-tion period. This suggests that the tested NaCl concentrations were unable to affect thesehydrolytic activities, perhaps because the formation of humus complexes that may protectpreferentially some enzymes more than others.

In our work, two oxidoreductases have been determined: dehydrogenase, an endocel-lular enzyme indicative of microbial activity, and catalase, related to the number of aerobicmicroorganisms and soil fertility. Between the two activities, dehydrogenase was the onlyenzyme that was really inhibited throughout the incubation period, with small differencesof values regardless of the amount of the added salt (Table 6). A slight recovery towardthe value of control was also observed at the end of incubation. By comparing results ofdehydrogenase and soil respiration, both indicators of microbial activity, it can be notedthat they were affected differently by the NaCl, with a general decrease for the first anda general increase of the latter. This may indicate a different physiological response ofmicroorganisms to the stress induced by salinity. Catalase behaved differently than dehy-drogenase. Irrespective of the applied amount of NaCl, the activity of catalase did not showa consistent pattern, with a small stimulating effect of salinity in many cases (Table 6).

Table 4Changes in time of protease activity (µg tyrosine·g−1·2h−1) in the soil with

different levels of NaCl addition


Control 330 bc 380 ab 356 abEC 2 275 d 359 ab 385 aEC 4 209 ef 344 abc 253 deEC 8 149 g 301 cd 186 fg


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Table 5Changes in time of amylase and alkaline phosphatase in the soil with different

levels of NaCl addition


Amylase (µg glucose·g−1·24 h−1)Control 297 ab 285 bc 297 abEC 2 280 bc 270 c 280 bcEC 4 293 ab 293 ab 300 abEC 8 303 ab 320 a 300 abAlkaline phosphatase (µg nitrophenol·g−1·h−1)Control 275 abc 348 a 282 abcEC 2 253 c 329 ab 339 aEC 4 262 bc 319 abc 284 abcEC 8 257 bc 343 a 314 abc


Table 6Changes in time of dehydrogenase activity (μg TPF·g−1·h−1) in the soil with

different levels of NaCl addition


Control 1.40 c 2.28 a 2.15 abEC 2 0.53 e 1.54 c 2.03 abEC 4 0.75 de 1.38 c 1.98 bEC 8 0.73 de 1.63 c 2.04 ab


The overall results on enzyme activity confirm, as stated by Frankenberger andBingham (1982), that the degree of inhibition is enzyme-specific, but they are insufficientto state which type of enzyme hydrolase or oxidoreductase is more affected by salinity.

Protease and dehydrogenase activities are usually considered dependent on microbialbiomass level (Curci et al. 1997; Garcia, Hernandez, and Costa 1994). Accordingly, in thisstudy similar results were found between ATP (index of biomass size) and both proteaseand dehydrogenase activities.

Soil is a complex picture of microbial processes and often we use more than one indi-cator to estimate soil quality. Only one or two parameters may be not enough for suchestimation, especially if, as found in our work, the response of some parameters are differ-ent than others, even when they reflect the metabolic status of the soil microflora. For thisreason, three soil quality indices were calculated.

In Table 7 are reported the patterns of the BIF, EAN, and MP. The values of BIF, anindex based on the activities of dehydrogenase and catalase, were not significantly differentbetween control and treated samples during the whole incubation period, indicating thatsuch an index is unable to determine effects of salt on soil biological activity.

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Table 7Changes in time of biological index of fertility (BIF), enzyme activity number(EAN), and metabolic potential (MP) in the soil with different levels of NaCl

addition

Treatment 1 day 20 days 40 days

MPControl 1.278 4.217 4.678E2 0.409 2.879 5.268E4 3.253 22.65 35.93E8 4.229 20.37 21.78

EANControl 18.87 23.73 23.00E2 16.56 24.14 21.77E4 17.25 21.58 17.30E8 11.93 21.29 17.89

BIFControl 1.022 2.008 1.901EC 2 0.786 1.526 1.797EC 4 0.979 1.424 2.047EC 8 1.051 1.443 1.991

The EAN values, which represent the five enzyme activities singularly monitored inthis study, were generally less than those of control, although they did not show a defi-nite pattern over time. The values of EAN substantially confirm the observed inhibitoryeffect of NaCl on protease and dehydrogenase (Tables 4 and 6). This was reasonablyexpected because the two enzyme activities are those most heavily weighted in the for-mulation of EAN. Given that EAN and both protease and dehydrogenase activities gavesimilar responses, the additional complexity of the EAN does not justify its being chosenas a biological index, at least in the studies concerning the effects of NaCl on soil biologicalactivities.

The values of MP, an index relating dehydrogenase and DOC, apart from the lowerdose of NaCl, were notably greater than that of control during the whole incubation period.Both control and treated samples showed a parallel increase toward the end of incubation.With elevated salt content, values of MP on day 40 were about 8 (for the EC 4) and 5 (forthe EC 8) those of control, so reminding data of cumulative CO2 release.

Conclusions

The size of microbial biomass, measured throughout the determination of ATP, wasdecreased by increasing salinity.

Increasing concentrations of salt, up to an EC of 4 dS·m−1, led to increased soil res-piration, indicating that smaller, more stressed microbial community was physiologicallymore active and used substrate less efficiently.

Between the five enzyme activities examined, protease, amylase, alkaline phosphatase,dehydrogenase, and catalase, the only enzymes that were really inhibited throughout theincubation period were protease (hydrolase) and dehydrogenase (oxidoreductase). These

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results did not allow the distinction of which type of enzyme, hydrolase or oxidoreductase,was more affected by salinity.

Between the soil quality indices, EAN confirmed the depressive effect of NaCl on thebiological properties of soil as evidenced by protease and dehydrogenase. The MP indexshowed an increasing trend up to EC 4 dS·m−1, a pattern similar to that of soil respiration.

The overall results indicate that ATP, soil respiration, protease, dehydrogenase, EAN,and MP seem able to monitor the effects of salt on selected soil biological activity andmay be regarded as suitable tools for putting in evidence the physiological reaction of soilbiomass under saline stress.

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