Soil microbial indices as bioindicators of environmental changes in a poplar plantation pot

The ratio of biomass C to soil organic C Cmic:Corg, the metabolic quotient the specific soil respiration of the microbial biomass, qCO2, the C mineralization quotient the fraction of tot

Ecological Indicators 5 (2005) 171–179

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Soil microbial indices as bioindicators of environmental

changes in a poplar plantation M.C Moscatelli a,* , A Lagomarsino b, S Marinari a, P De Angelis b, S Grego a

Abstract

An understanding of microbial biomass and microbial activity as part of belowground processes as affected by elevated

CO 2 is crucial in order to predict the long-term response of ecosystems to climatic changes The ratio of biomass C to soil organic C (Cmic:Corg), the metabolic quotient (the specific soil respiration of the microbial biomass, qCO2), the C mineralization quotient (the fraction of total organic C mineralized throughout the incubation, qM), the microbial biomass change rate quotient (qC) and soil inorganic nitrogen content were determined on soil samples taken during 3 years (Fall 2000–Fall 2003) in a poplar plantation exposed to increased atmospheric CO2 by means of FACE (Free Air CO2 Enrichment) technique and nitrogen fertilization A competition for nitrogen between plants and microrganisms, stronger in FACE plots, induced a stress condition within microbial community FACE treatment provided C for microbial growth (Cmic:Corg), but reducing nitrogen availability, led to a higher microbial loss over time (qC) Nitrogen fertilization decreased microbial mortality lowering energetic maintenance require- ments (qCO2) and induced a short-term shift in favour of microrganisms more rapid in the use of the resources The C mineralization quotient (qM) was not affected by either FACE nor fertilization treatment meaning that the fraction of total organic carbon mineralized during the incubation period did not vary significantly.

# 2005 Elsevier Ltd All rights reserved.

Keywords: Soil; Elevated CO 2 ; N fertilization; Microbial biomass; Soil respiration; Indices; Poplar

1 Introduction

microbe– soil–plant root system indirectly by

modifying soil water content and by increasing root

growth and rhizodepositions rates (Hungate et al.,

1997; Janssens

* Corresponding author Tel.: +39 0761 357329;

fax: +39 0761 357242.

E-mail address: mcm@u n itus.it (M.C Moscatelli).

popula-tion, community structure and activity of soil- andrhizosphere-associated microrganisms are likely tooccur under elevated CO2 (Sadowsky and Schorte-

1470-160X/$ – see front matter # 2005 Elsevier Ltd All rights reserved.

doi:10.1016/j.ecolind.2005.03.002

172 M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179

are highly dependent

on the factors affecting

plant and microbial

growth and soluble C

the main energy source

organic matter The

reports that combining

microbial activity and

Ecophysiologicalindices (metabolic

generated by basing

performances(respiration, growth/

death, carbon uptake)

on the total microbialbiomass per unit time

impact which willaffect members of amicrobial communityshould be detectable atthe community level

by a change of a

microbial communityactivity which can bequantified (qCO2, etc.)

The ratio of biomass

C to soil organic C (Cmic:Corg)

microbial biomass tosoil organic carbon

a relative measure ofhow efficiently the soilmicrobial biomass is

utilizing C resourcesand the degree ofsubstrate limitation forsoil microbes (Wardleand Ghani, 1995; Dilly

quotient) expresses thefraction of total organiccarbon mineralized

FACE (Free Air CO2

Enrichment) techniqueand fertilized duringthe last 2 years Aim ofthis paper was toassess the validity ofthe microbial indices

Mate

174 M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179

plantation and FACE

facility are located in

central Italy, Tuscania

POPFACE site) are of14.1 8C and 818 mm,respectively Clones

Populus nigra andPopulus

euramericana weregrown, since 1999, insix 314 m2 plotstreated either withatmospheric (control)

or enriched (550mmol mol 1 CO2) CO2

Enrichment) Each plot

is divided into sixtriangular sectors, withtwo sectors per poplargenotype: three speciestwo nitrogen levels

Nitrogen fertiliza- tionstarted in July 2002, itwas executed once per

growing season andlasted for 16 weeks

Fertilizer was suppliedweekly in constantdose to a final totalamount of 212 kg N

ha 1 In the 2003growing season thefertilizer was suppliedweekly in amountsproportional to thegrowth rate for 20weeks and provided atotal amount of 290 kg

N ha 1

M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179 175

176 M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179

litter layer two soil

cores per genotype (10

cm wide, 20 cm long)

were taken inside each

of the three sectors in

each plot, for a total of

36 soil cores in not

June 2002 soil samples

were collected also in

fertilized sub-plots

although the addition

of nitrogen started the

however data related to

these samples are not

analyses

2.3 Chemicaland

microbiologica

l analysesInorganic nitrogenwas assessed as thesum of ammonium

extracted in

1 M KCl and wasdetermined following

Anderson and Ingram

portions of moist soil(20 g oven-dry soil)were weighed, the first

extracted with 80 ml of0.5 M K2SO4 for

30 min by oscillatingshaking at 200 rpmand filtered

(Whatman no 42); the

fumigated for

24 h at 25 8C withethanol-free CHCl3

and then extracted as

extracted from fumigated soils and

non-kEC = 0.38 POPFACEsoil characteristicsallow the use of thisfactor since caution is

and in organic layers

of forest soils (Scholle

respiration 20 g dry basis) of moistsample were placed in

(oven-1 l stoppered glass jars

The CO2 evolved wastrapped, after 24, 72,

calculated as follows:Cmic:Corg = mg ofbiomass C mg totalorganic carbon 1

0

3

(

DillyandMunch

M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179 177

processes since they

have been obtained

analyzing soils throughlaboratory standardprocedures (sieving,controlled temperatureand moisture) that donot necessarily reflect

in situ conditions

2.4.Statistical

analysisAnalysis of variance

performed to evaluatethe main effects ofFACE, fertilization,time and their

parameters analyzed

Data were tested fornormality with theShapiro-Wilk statisticand normalized with asquare root transfor-

plot were averaged andthe plot (three controlplots and three FACEplots) was the unit of

significance of FACE,

interaction between the

fertilized plots (years2000–2003, n = 36)

The significance offertilization and itsinteraction with FACE

determined in

174 M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179

M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179 175

fertilized plots from

2002 to 2003 (n = 72)

Because there were no

significant variations

due to the different

poplar species, data

from different poplar

genotypes were pooled

together When

significant they were

analysis In the results

section the effect of

fertilization treatments

has been reported as

percentage variation

with respect to the

control It has been

average values of all

sampling dates for

from October

fertilization effect:

June 2002 is, in fact,

not included since

fertilization was started

the following month

All statistical analysis

were per- formed with

nitrogen was observed,

in not fertilized plots

(FACE and control), as

from the year 2000;

0.001) (Fig 1A)

significant increase ofsoil inorganic nitrogen(+123% in FACE and

plots, p < 0.001)although it did not re-establish the originalvalues of October

shown by the linearregression on thesetwo parameters in Fig

significantly decreasesafter the first year andassesses its value toless than 2% until theend of

However, although thecontribution ofmicrobial biomass tototal organic carbon isvery low in this soil,

induced a significant

Cmic:Corg ratio innot fertilized plots(+35%, p < 0.001)

176 M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179

Table 1

Fig 1 Mean percentage effects of treatments (FACE and N fertilization) calculated from 2000 to 2003 as relative variation with respect to the control (A) Inorganic nitrogen (N-NH 4 + N-NO 3 ), (B) microbial quotient (Cmic:Corg), (C) metabolic quotient (qCO 2 ) and (D) microbial respiration (24 h).

M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179 177

respectively The mean

qC for FACE plots

period of study was

2.30 versus 0.60 mg

biomass C loss mg

biomass C 1

Fig 2 Linear regression

between inorganic nitrogen

and Cmic:- Corg measured

N and control + N,respectively) (Table 3)

quotient is negativelyand signifi- cantlyaffected by FACE and

treatments (Tables 1

qCO2 by 17% in notfertilized and by 23%

in fertilized plots whilethe addition of nitrogen

growth and

176 M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179

June 2002–October 2002 145 0.47 ( 0.64) 2.75 ( 1.60) 1.69 ( 0.50) 2.72 ( 1.22) October 2002–June 2003 220 1.36 ( 0.55) 2.20 ( 0.75) 5.70 ( 1.24) 3.82 ( 1.18) June 2003–October 2003 156 2.54 ( 0.53) 3.27 ( 0.49) 0.78 ( 0.73) 1.21 ( 0.67)

M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179 177 Microbial biomass change rate quotient (qC) ((mg Cmic t 1 mg Cmic t 2 )/mg Cmic t 1 /(t 2 t 1 )) 10

plots from Spring 2002 to Fall 2003

measured in FACE + N and control + N

Standard error is reported in parentheses.

maintenance In this study the correlation coefficient

between the two indices is r = 0.371 (n = 177;

p < 0.001) and indicates that to a low qCO2

corresponds a high Cmic:Corg ratio

In the attempt to get further insight into microbial

respiration activity, CO2 output after 24 h of

incuba-tion and the cumulative value of CO2 evolved after 10

days were considered This was to emphasize the

known difference between the flush of CO2 following

rewetting of soil and the basal respiration activity

(MR24 h) is not modified by FACE treatment whilethe fertilization caused a significant increase in bothFACE and control plots: the mean fertilization effectwas in fact +118 and +103% ( p < 0.001),respectively (Table 1 and Fig 1D)

The C mineralization quotient (qM) providesinformation on the fraction of total organic carbon

mineralized throughout

the incubation time (10

days in this study)

control plots (Table 1)

It was not affected by

para-meters have often been

used for evaluating the

change rate quotient)

to FACE and nitrogenfertilization treatments,

years, seemed to bestrongly affected bythe nutritional status ofthe soil In fact astrong reduction of soilinorganic nitrogen wasdetected and it was

physiological state ofmicrobes with changes

in microbial size overtime The decrease of

qC after fertilization

microbial nutritionalconditions as nitrogen

in easily availableforms was provided

efficient microbialcommunity Changes

in nutrient availabilitycan modify microbial

requirements The lowCmic:Corg and thehigh qCO2 reflect aless efficient use oforganic substrates by

efficient use of energy

in nutrient acquisitionactivity is permitted

environments it isassumed that, because

of faster root turnover

induced a significantincrease of soil labilecarbon fractions (+19%

of water soluble carbonand + 21% of K2SO4-

indicating a flux ofsoluble C forms thatcould lead to themicrobial immobiliza-tion process observed

conditions, the extra C

made available for

microbes has been used

in June 2003 when the

highest increase of this

purpose it should be

considered that June

2003 was just 1 month

after the beginning of

the fertilization and

this could be the reason

for the consistent flush

after the addition of

easily available organic

fertilizers to the soil

This phenomenon, the

efficient in the use of

the nutrient resources

hypothesis we haveevidence that microbial

signifi-cantly in June 2003after fertilization by61% in control + Nand 48% in FACE + N

communities (data notshown)

178 M.C Moscatelli et al / Ecological Indicators 5 (2005) 171–179

meaning that neither

FACE treatment nor N

fertilization did affect

the capacity of the soil

AcknowledgementsThe authors are

Giuseppe ScarasciaMugnozza coordinator

of EU EUROFACE(EVR1-CT-2002-40027) and MIURCentre of Excel- lence

‘‘Forests and climate’’

projects for allowingthe use of POPFACEexperimental station

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