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Soil Biology & Biochemistry 43 (2011) 520e530
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Soil Biology & Biochemistry
journal homepage: www.elsevier .com/locate/soi lbio
Nutrient dynamics in litter mixtures of four Mediterranean maquisspecies decomposing in situ
Giulia Maisto, Anna De Marco, Angela Meola, Ludovica Sessa, Amalia Virzo De Santo*
Department of Structural and Functional Biology, University Federico II Napoli, Via Cinthia, Napoli I-80126, Italy
a r t i c l e i n f o
Article history:Received 5 August 2010Received in revised form11 November 2010Accepted 17 November 2010Available online 1 December 2010
Keywords:Litter decompositionManganeseLigninInteractions among littersNon-additive effects of litter mixing
* Corresponding author. Tel.: þ39 081 679113; fax:E-mail address: [email protected] (A. Virzo De Santo
0038-0717/$ e see front matter � 2010 Elsevier Ltd.doi:10.1016/j.soilbio.2010.11.017
a b s t r a c t
In natural conditions, litters shed from different species become mixed with each other, and decomposetogether. Most studies deal with decomposition of individual species; few studies investigate theinfluence of litter mixing on decomposition and nutrient dynamics; the results are contradictory aspositive, negative, or no effect, of litter mixing have been observed. In this study we test the hypothesis:i) that litter mixing in the Mediterranean maquis, a nutrient poor, high diversity ecosystem, producesnon-additive effects on nutrient dynamics; ii) that the effects vary with the composition in species of themixture and with the relative amount of the species component the mixture. Two types of 3-speciesmixtures were set up; one contained three sclerophylls, Phillyrea angustifolia, Pistacia lentiscus andQuercus ilex; the other contained the first two species with the mesophyll Cistus. Litterbags, containingmonospecific litters and even and uneven mixtures, were incubated under natural condition in situ; evenmixtures had the 3 species in equal proportion, whereas uneven mixtures had one of the species asdominant (50%) and the other two species in equal proportion (25%:25%). Litterbags were retrieved after92, 188 and 403 days; litters from the mixtures were separately analyzed for mass loss and content ofnitrogen (N), potassium (K), sodium (Na), calcium (Ca), magnesium (Mg), manganese (Mn), iron (Fe),copper (Cu), and zinc (Zn). Results indicate that mixing influences the dynamics of N, Mn, Ca, Mg, Fe, Cuand Zn, but scarcely affects the dynamics of K and Na. The comparison of observed to expected values forchanges of nutrients in litterbags indicates the occurrence of non-additive effects of litter mixing onmovements of N, Fe, Cu, and Zn to or from the litterbags containing the mixtures. The effects depend onthe composition in species of the mixture, whereas the relative amount of the species component themixture is not relevant.
� 2010 Elsevier Ltd. All rights reserved.
1. Introduction
Litter decomposition is a fundamental process in ecosystemfunctioning as it regulates the cycle of matter, CO2 release into theatmosphere, carbon sequestration in the soil and nutrients miner-alization. The rate of decomposition is largely determined by litterchemistry, particularly lignin concentration and nutrient level. Inthe early stages of decomposition, nutrient-rich litters decomposefaster than nutrient-poor litters. As litter decomposes, concentra-tions of lignin and nitrogen increase (Berg andMcClaugherty, 2008)and litters with low initial nitrogen concentration may accumulatemore nitrogen than those with a high level (Berg and Staaf, 1981;Hobbie and Vitousek, 2000); moreover nitrogen accumulation inlitter may be enhanced by high N availability in the surroundingenvironment, as in the case of high soil N levels (Berg and Ekbohm,
þ39 081 679233.).
All rights reserved.
1983; Virzo De Santo et al., 1998). Limitation posed by litterchemical composition may be mitigated by nutrient availability inthe soil; thus mountain birch leaf litter incubated at nutrient-poortundra sites decomposed less than at nutrient-richer forest sites(Sjögersten andWookey, 2004). The onset of net loss of lignin massidentifies the start of late stages in which lignin and modifiedlignin-like humification products dominate litter decomposition(Fogel and Cromack, 1977; Berg et al., 1993) up to a limit value; thelimit value of decomposition, i.e. the litter remains, that have anextremely low decomposition rate, are related to litter concentra-tion of N, Mn, and Ca (Berg, 2000; Berg et al., 2003) which arenutrients regulating the lignin-degrading microflora (Erikssonet al., 1990). The role of Mn deserves a particular attention. Themost efficient degraders of lignin are white-rot fungi producingmanganese peroxidase (MnP) that is able to degrade lignin in vitro(Hofrichter et al., 2001). Mn availability has been found to limitlignin degradation in needle litter of Norway spruce (Berg, 2000), inleaf litter of common oak (Davey et al., 2007) and in several pineneedle litters (Berg et al., 2007, 2010; Virzo De Santo et al., 2009).
G. Maisto et al. / Soil Biology & Biochemistry 43 (2011) 520e530 521
Thus it seems reasonable that Mn availability may limit lignindegradation in many other litter species. Moreover in laterdecomposition stages, the concentrations of heavy metals, such asFe, Zn, Mn, Pb, and Cd, even in litters decomposing in unpollutedforests, may reach levels potentially inhibitory to microorganisms(Laskowski and Berg, 1993; Virzo De Santo et al., 2002).
In natural conditions, litters from different species occurring inthe canopy become mixed with each other after shedding, anddecompose together.
The factors controlling decomposition of individual litters havebeen extensively studied in many types of ecosystems. Fewerstudies have investigated how litter mixing influences decompo-sition and nutrient dynamics (Gartner and Cardon, 2004;Hättenschwiller et al., 2005). The results of such studies arecontradictory as positive, negative, or no effect, of litter mixing havebeen observed. The rationale behind litter mixing effect isthe possibility of nutrient transfer from the high-quality litter to thelow quality litter that leads to a more rapid decomposition of themore recalcitrant litter in the mixture. However observed changesin nutrient dynamics are not always concomitant to changes indecomposition (Blair et al., 1990; Briones and Ineson, 1996;McTiernan et al., 1997). Furthermore according to Hoorens et al.(2003) interactions in litter mixtures are not explained by thedifference in initial single litter chemistry parameters.
At the ecosystem level, non-additive effects of litter mixing onnutrient dynamics may involve changes in the availability ofnutrients to plants due to increased immobilization in litter or,quite the opposite, to increased release into the soil, as well as tothe timing of nutrient release (McTiernan et al., 1997) withconsequences on plant growth or on competitive relationshipsamong species (Finzi and Canham, 1998).
There is no study investigating the effects of litter mixing onnutrient dynamics in the Mediterranean maquis, a nutrient poor,high diversity ecosystem. In Mediterranean maquis biologicalprocesses are regulated by the seasonally contrasting climatepattern (i.e. hot-dry summers and mild to cool, wet winters), byfrequent fires that contribute to nutrient mineralization, and byallelopathic effects plant-to-plant and plant-to-soil microorgan-isms (Magiatis et al., 1999; Castaldi et al., 2009; Fiorentino et al.,2009). Sclerophyllous shrubs are dominant in the maquis,however gaps originated by fires are mainly covered by herbs andmosses and at the edge maquis/gap, mesophyllous shrubs of Cistussp. pl. are very common.
In this study we test the hypothesis that litter mixing producesnon-additive effects on nutrient dynamics; that the effects varywith the composition in species of themixture; that the effects varyaccording to the relative amount of the species component themixture. To elucidate litter interactions in the mixtures andnutrient exchanges of the mixtures, we analyze whole-mixtures aswell as, separately, the individual litters component the mixtures.We focus on Mn dynamics to contribute knowledge about a keynutrient, controlling lignin degradation, which has been overallvery poorly investigated in studies dealing with litter interactionsin mixture.
2. Material and methods
2.1. Study site
The study was carried out in the low maquis at the Castel Vol-turno Nature Reserve, southern Italy (40� 570 N, 13� 330E) whereplant cover encompasses a mosaic of different patches such as lowmaquis, highmaquis and, on small areas,Quercus ilexwood. The lowmaquis is characterized by a dense evergreen sclerophyllous shrubcover inwhich Phillyrea angustifolia L., Pistacia lentiscus L. and Q. ilex
L. are very common; gaps dominated by herbs and bryophytes,cover about 20% of the low maquis area; at the edge gap/maquismesophyllous shrubs of Cistus sp. pl. are common. The study site isa flat coastal area on stabilized dunes of alluvial deposits and loosesiliceousecalcareous sands of the late Quaternary. The slightlyalkaline (pH: 7.3), deep (>150 cm), well-drained soil is a CalcaricArenosol according to the FAO system of soil classification (FAO,1998). The area has a typical Mediterranean climate with drysummers and rainy autumns and winters. Mean annual rainfall is599 mm year�1; mean annual temperature is 17 �C, that of thewarmest month (August) is 24.3 �C and the coldest (January) is8.8 �C (nearest Meteorological Station Giugliano-Lago Patria, years2000e2008).
2.2. Experimental design
We collected senesced leaves of Ph. angustifolia, P. lentiscus,Q. ilex, and Cistus sp. during the period of maximum litter fall(MayeJuly) using 25 litter traps (1.5 mm mesh screen with 1.4 m2
collecting surface) suspended under the canopy of the shrubs. Alllitters were air dried at room temperature immediately aftercollection and stored until further use. Percent moisture content ofair dried litters was 6.820 � 0.003 for Q. ilex, 7.682 � 0.008 forP. lentiscus, 7.005 � 0.008 for Ph. angustifolia and 9.465 � 0.009 forCistus. Three sub-samples for each litter species were dried toa constant weight at 75 �C and used to calculate the correctionfactor for converting air dried mass to water-free dry mass. Litter-bags made of terylene net (1 mm mesh) were filled with a knownamount (weighing accuracy: 3 decimals) of litter. Two differenttypes of mixture were set up: one type with three species of thesame plant functional group, i.e. three sclerophylls such as Ph.angustifolia, P. lentiscus, Q. ilex; the other type with two sclerophylls(Ph. angustifolia and P. lentiscus) and a mesophyll (Cistus sp. pl.); thetwo types of mixture reflected respectively, litter composition inthe interior of the maquis and at the edge maquis/gaps. The studyincluded 3 sets of litterbags. The first set contained only one speciesof litter (in total 96 litterbags, i.e. 24 litterbags per each of the fourspecies). The second set comprised even mixtures of three speciesin equal proportions (in total 84 litterbags). The third set (in total192 litterbags) contained: i) 3 types of uneven mixtures of scle-rophylls, with one litter as dominant and the other two litters inequal proportions (50%: 25%: 25%), and ii) a sole uneven mixturewith Cistus dominant. The bags containing Q. ilex had the size15� 25 cm and were filled with 7 g of litter, those containing Cistushad the size 15 � 12.5 cm and were filled with 3.5 g of litter.
2.3. Litter incubation, determination of decompositionand chemical analyses
On October 10, 2006, in each of eight plots in the study area, thebags were placed on the litter layer and fastened to the ground by10e15 cm long pegs (fibreglass, PVC coated) through a 1-cm wideedge on the bags. Litterbags were retrieved after 92, 188 and 403days. The bags were transported directly to the laboratory andprocessed within 48 h. The litter remaining in each bag was gentlybrushed to remove adhering soil debris and the three speciescomponent the mixtures were carefully separated and analyzed fordetermination of mass loss and litter chemistry. To determine theash-free litter dry mass, a sub-sample was dried to a constant massat 75 �C (48 h) and then combusted at 550 �C (2 h) to get the ashcontent.
Litter chemical analyses were carried out before incubation andat each sampling of litterbags. All analyses were carried out onthree sub-samples. Litter samples were ground into a fine powderwith an agate pocket (Fristch pulverisette 00.502). Lignin, cellulose
Table 1Main characteristics of leaf litters and mass loss over the study period (403 days).Values are mean � standard error.
Ph. angustifolia P. lentiscus Q. ilex Cistus sp.
Lignin (% d.w.) 13.32 � 0.20 21.93 � 4.00 24.38 � 1.62 17.62 � 1.05Cellulose (% d.w.) 24.91 � 1.21 14.90 � 2.47 21.60 � 1.31 22.50 � 0.67ADSS (% d.w.) 61.90 � 5.56 59.60 � 0.98 52.01 � 0.80 55.60 � 1.73N (mg g�1 d.w.) 4.28 � 0.19 3.73 � 0.18 4.43 � 0.09 4.72 � 0.36C/N 127.52 139.69 106.89 110.45Ash (% d.w.) 0.62 � 0.00 0.67 � 0.008 0.42 � 0.02 0.67 � 0.02Mn (mg g�1 d.w.) 22.67 � 0.83 31.27 � 0.99 546.6 � 1.22 72.07 � 1.03
G. Maisto et al. / Soil Biology & Biochemistry 43 (2011) 520e530522
and acid soluble substances (ADSS) were determined as reportedby Van Soest and Wine (1968) with modifications according toFioretto et al. (2005). N content was measured by a C, N, S analyzer(Thermo Finnigan Flash EA 1112). To determine the concentrationsof K, Na, Mg, Ca, Mn, Fe, Cu and Zn, the samples were digested ina Milestone (mls 1200) Microwave Laboratory System witha mixture of hydrofluoric and nitric acid (HF 50% v/v: HNO3 65%v/v ¼ 1:2). Element concentrations of digested samples weremeasured by atomic absorption spectrometry (AAS; SpectrAA 20Varian) via flame (excepted Cu that was determined via graphitefurnace) using standard solutions (STD Analyticals, Carlo Erba),diluted in the same acid matrix.
2.4. Data analyses
At each sampling, for each sample, nutrient concentration wasmultiplied by litter dry mass to calculate the mass of nutrientpresent in each litter component the mixture. To calculate nutrientmovement to or from individual litters, as well as to or from littermixtures, during a specific decomposition period, nutrient masswas subtracted from the initial mass; nutrient release and nutrient
0 100 200 300 400
ggm(
N1-)
0
5
10
15
0 100 200 300 400
ggm(
gM
1-)
0
1
2
3
4
Days
0 100 20
ggm(
nM
1-)
0,0
0,5
1,0
0 100 200 300 4000
1
2
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D
0 100 200,0
0,5
1,0
1,5
0 100 20
ggµ(
uC
1-)
0
4
8
ggm(
aN
1-)
ggm(
eF1-)
PhQ
Fig. 1. Nutrient dynamics of four Mediterranean maquis species: Q. ilex (Q), Ph. angustifoliaamounts per gram of initial litter mass. Note the different scales on y-axes for Mn and Fe (
immobilizationwere reported respectively as negative and positivevalues.
To detect non-additive effects of litter mixing on nutrientdynamics at the litter mixture level, we calculated, for eachmixtureseparately, as well as for all Quercus mixtures (MQ) and all Cistusmixtures (MC) pooled together, the expected value as the sum ofeach monospecific litter’s performance, weighted by its proportionin the mixture.
Monospecific litters were compared for mass loss and changesof litter chemistry over the incubation period and the significanceof differences was checked by two-ways ANOVA, followed by Stu-denteNewmaneKeuls post hoc test.
To detect the effect of litter mixing on nutrient dynamics at theindividual litter level, we compared nutrient dynamics of eachmonospecific litter with nutrient dynamics of the same litter in allmixtures involving that species. Data were processed by one-wayANOVA.
The significance of the differences between observed andexpected values within each mixture and within the mixtures withQ. ilex as a whole, and the mixtures with Cistus as a whole, wasassessed by Student t-test.
3. Results
3.1. Differences among litters for initial chemical composition
The four litters differed for lignin, cellulose and ADSS (AcidDetergent Soluble Substances): lignin concentration was higherthan 20% in P. lentiscus and in Q. ilex; the litter of P. lentiscus had thelowest cellulose content (14.9%) while the values of the other littersranged from 21.6 to 24.9%; litter of Q. ilex had the lowest ADSS andash content as well as the lowest C/N (Table 1).
The four litters covered a narrow range of nitrogen content, from3.73 to 4.72mg g�1 d.w., respectively for P. lentiscus, the poorest litter,
0 300 4000
1
2
3
0 100 200 300 4000
4
8
ays
0 100 200 300 400
ggm(
aC
1-)
0
5
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15
ggm(
K1-)
0 300 4000
1
2
3
0 100 200 300 4000
1
2
Days
0 300 400
ggm(
nZ1-)
P C
(Ph), P. lentiscus (P) and Cistus sp. (C), decomposing in situ over 403 days. Values areCistus values are on the right scale).
G. Maisto et al. / Soil Biology & Biochemistry 43 (2011) 520e530 523
and Cistus, the richest litter (Table 1, Fig.1). The litter of P. lentiscushadthe highest K and Na content (6.22 and 1.54 mg g�1 d.w.) while thevalues of the other litters were around 4.5 for K and ranged from 0.7to 0.96mg g�1 d.w. for Na (Fig. 1). Ca andMgwere most abundant inCistus followed by P. lentiscus (Fig. 1). The litter of Q. ilex had Mnconcentration (0.55mg g�1 d.w.) one order ofmagnitude higher thanthe other litters (Table 1, Fig. 1). Fe content (Fig. 1) was highest inCistus and in Q. ilex (0.38 and 0.23 mg g�1 d.w., respectively) andmuch lower in P. lentiscus and in Ph. angustifolia (0.11 and0.09 mg g�1 d.w., respectively). Cu and Zn were highest in Cistusfollowed by Ph. angustifolia (Fig. 1). Differences in nutrient concen-trations were statistically significant (Table 2).
3.2. Nutrient dynamics of monospecific litters and of individuallitters in mixture
Nutrient concentrations changed significantly with incubationtime in all litters (Table 2). During decomposition N was accumu-lated by all monospecific litters in the early phase (0e188 days) andreleased thereafter; thus N dynamics had a biphasic pattern (Fig. 1).In mixture the litters showed the same temporal pattern as inisolation, however both N immobilization and N release weregenerally higher than in monospecific litters (Fig. 2A).
Table 2Levels of significance (P values) from the two-way ANOVA for comparison of effects of litdecomposition of monospecific litters of Q. ilex (Q), Ph. angustifolia (Ph), P. lentiscus (P) a
Variable Litter type(species)
Time(days)
Litter type � time Post-hoc comparison tests
Litter type within time
0 days
Ph P C
N <0.001 <0.001 0.059 Ph e e e
P 0.608 e e
C 0.909 0.787 e
Q 0.882 0.784 0.792Mn <0.001 <0.001 <0.001 Ph e e e
P 0.931 e e
C 0.871 0.681 e
Q <0.001 <0.001 <0.001Ca <0.001 <0.001 <0.001 Ph e e e
P 0.281 e e
C <0.001 0.002 e
Q 0.020 0.003 <0.001Mg <0.001 <0.001 <0.001 Ph e e e
P 0.056 e e
C <0.001 <0.001 e
Q 0.799 0.079 <0.001Fe <0.001 <0.001 <0.001 Ph e e e
P 0.917 e e
C 0.470 0.373 e
Q 0.759 0.548 0.457K <0.001 <0.001 <0.001 Ph e e e
P <0.001 e e
C 0.867 <0.001 e
Q 0.905 <0.001 0.700Na <0.001 <0.001 <0.001 Ph e e e
P <0.001 e e
C 0.028 <0.001 e
Q 0.272 <0.001 0.122Cu <0.001 <0.001 <0.001 Ph e e e
P <0.001 e e
C 0.617 <0.001 e
Q 0.003 <0.001 0.002Zn <0.001 <0.001 <0.001 Ph e e e
P 0.954 e e
C 0.788 0.942 e
Q 0.938 0.832 0.935
Terms for ANOVA model (degree of freedom in brackets) are: Litter types (3), Time (3), LStudenteNewmaneKeuls test. Bold indicates statistically significant differences between
Mndynamics in the four species had different patterns (Fig.1). InQ. ilex, the litter with the highest initial Mn concentration (Table 1),Mn was released from the earliest phase of decomposition (Fig. 1).Ph. angustifolia and P. lentiscus immobilized Mn throughout thewhole investigated decomposition period (Fig. 1). In Q. ilex litter Mnrelease proceeded in parallel with lignin degradation (Fig. 3) whileno lignin degradation occurred in Ph. angustifolia and P. lentiscus(Fig. 3). Mn dynamics in Cistus litter had a biphasic pattern (Fig. 1):a huge amount of Mn accumulated in litter in the period 0e188days; in the later decomposition phase (188e403 days) most of theaccumulated Mnwas released and, simultaneously, a large amountof lignin was degraded (Fig. 3). In mixture, Mn dynamics had thesame pattern as in monospecific litters, however the magnitude ofboth release and accumulation processes was somewhat higherthan in the monospecific litters (Figs. 2A and 3). Litter mixinginduces an increase of Mn release from Q. ilex and a fairly similarincrease of Mn immobilization in Ph. angustifolia and P. lentiscus. Asin monospecific litters, the net release of Mn was accompanied bylignin degradation (Fig. 3).
Ca was released by Ph. angustifolia and P. lentiscus, and accumu-lated byQ. ilex both inmonospecific litters and inmixture (Figs.1 and2A). Ca had a biphasic pattern in Cistus (Fig. 1); in mixture accumu-lation was enhanced but a release about similar in amount followed(Fig. 2A). Mg accumulated in Q. ilex and in Ph. angustifolia during
ter species and incubation time on N, Mn, Ca, Fe, K, Na, Cu, and Zn dynamics duringnd Cistus sp. (C).
92 days 188 days 403 days
Ph P C Ph P C Ph P C
e e e e e e e e e
0.654 e e 0.268 e e 0.985 e e
0.265 0.194 e <0.001 0.003 e 0.928 0.728 e
0.493 0.493 0.377 <0.001 0.004 0.628 0.235 0.151 0.128e e e e e e e e e
0.917 e e 0.925 e e 0.793 e e
0.777 0.570 e <0.001 <0.001 e 0.345 0.448 e
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.017 0.016 0.058e e e e e e e e e
0.299 e e 0.943 e e 0.357 e e
0.006 0.046 e <0.001 <0.001 e 0.063 0.013 e
0.679 0.282 0.009 0.806 0.937 <0.001 0.661 0.364 0.065e e e e e e e e e
0.022 e e 0.030 e e 0.026 e e
<0.001 0.001 e <0.001 <0.001 e <0.001 <0.001 e
0.053 0.977 <0.001 0.059 0.475 <0.001 0.769 0.034 <0.001e e e e e e e e e
0.968 e e 0.373 e e 0.916 e e
0.416 0.296 e <0.001 <0.001 e <0.001 <0.001 e
0.678 0.427 0.481 0.335 0.599 <0.001 0.003 0.005 <0.001e e e e e e e e e
<0.001 e e 0.195 e e 0.003 e e
<0.001 0.863 e <0.001 <0.001 e 0.006 <0.001 e
<0.001 0.073 0.053 0.025 0.159 <0.001 0.796 0.005 0.004e e e e e e e e e
0.063 e e 0.346 e e 0.178 e e
0.027 0.556 e <0.001 <0.001 e <0.001 <0.001 e
0.038 0.524 0.694 0.270 0.772 <0.001 0.599 0.205 <0.001e e e e e e e e e
0.518 e e 0.018 e e <0.001 e e
<0.001 <0.001 e <0.001 <0.001 e 0.853 <0.001 e
0.094 0.059 0.003 0.575 0.012 <0.001 0.510 <0.001 0.759e e e e e e e e e
0.552 e e <0.001 e e 0.828 e e
0.099 0.135 e <0.001 <0.001 e 0.964 0.920 e
0.901 0.750 0.129 0.004 0.089 <0.001 0.576 0.982 0.815
itter types � Times (9), Residual (32), Total (47). Pairwise multiple comparision byspecies.
-6
-3
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12N (mg)
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ss
am
re
tt
il
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6Fe (mg)
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Q UQ
UP
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EQ
Ph UPh
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P UP
UPh
UQ
EQ
C UC
EC
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UC
P EC
UC
0.1
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Q UQ
UP
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EQ
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UP
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UPh
UQ
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C UC
EC
Ph EC
UC
P EC
UC
Q UQ
UP
UPh
EQ
Ph UPh
UP
UQ
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P UP
UPh
UQ
EQ
C UC
EC
Ph EC
UC
P EC
UC
Q UQ
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EQ
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UP
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P UP
UPh
UQ
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C UC
EC
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UC
P EC
UC
Q UQ
UP
UPh
EQ
Ph UPh
UP
UQ
EQ
P UP
UPh
UQ
EQ
C UC
EC
Ph EC
UC
P EC
UC
N (mg)
Mn (mg) Mn (mg)
Ca (mg)
Mg (mg)
Fe (mg)
A
Fig. 2. (A and B) Accumulation (positive values) and release (negative values) of nutrients during decomposition of four Mediterranean maquis litter species incubated in situ inmonospecific litterbags (open bars) and in 3-species mixtures with different proportions of the component species (closed and striped bars). E indicates even mixtures with thethree species in equal proportion; U indicates uneven mixtures with a dominant species (50%) and the other two species in equal proportion (25%); subscripts refer to the dominantspecies (Ph: Phillyrea angustifolia; P: Pistacia lentiscus, Q: Quercus ilex; C: Cistus); within each litter species, the sequence used for mixtures reflects the decreasing proportion of thespecies in the mixture. MQ and MC indicate respectively all Quercus mixtures and all Cistus mixtures pooled together. Values are mean � SE. Different letters indicate statisticallysignificant differences, at the P < 0.05 level, between monospecific litter and individual litter in mixture (one-way ANOVA). Note the different scales on y-axes for Mn (Cistus valuesare on the left scale).
G. Maisto et al. / Soil Biology & Biochemistry 43 (2011) 520e530524
-3
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ab
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UC P E
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CQ U
QU
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PhU
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QP U
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C UC
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UC P E
CU
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PU
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PhU
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PU
PhU
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Q
K (mg)
Na (mg)
Cu (µg) Cu (µg)
Zn (mg)
ss
am
re
tti
ll
ai
ti
ni
ma
rg
re
pe
sa
el
eR
/n
oi
ta
lu
mu
cc
At
nei
rt
uN
B
Fig. 2. (continued).
G. Maisto et al. / Soil Biology & Biochemistry 43 (2011) 520e530 525
decomposition (Fig. 1). In Cistus and P. lentiscus Mg dynamics hada biphasic pattern (Fig. 1); in Cistus mixtures both Mg accumulationand release were higher than in monospecific litters (Fig. 2A).
Fe was accumulated in all monospecific litters during decom-position (Fig. 1); the accumulation in Cistus litter was massive anda relatively small release occurred in the late phase. In mixture, Feaccumulation was higher than in isolation in all litters with theexception of Q. ilex (Fig. 2A).
K (Fig. 1) was released by all litters with the greatest loss in theearly phase (0e92 days). No difference between monospecificlitters and litters in mixture was detected (Fig. 2B), with theexception of Ph. angustifolia that in the even mixture (EC) releasedsignificantly more K than in isolation.
Na had a pattern very similar to that of K (Fig. 1). However in themixtures with Cistus a release followed by immobilization wasobserved in all species with significant differences betweenmonospecific Cistus litter and the uneven mixture (UC; Fig. 2B).
Cu was accumulated by all litters (Fig. 1) at rates that in mixturewere higher compared tomonospecific litters with the exception ofPh. angustifolia (Fig. 2B).
Zn was accumulated by all monospecific litters during theperiod 0e188 days and released thereafter (Fig. 1). No significantdifference occurred between monospecific litters and litters inmixture (Fig. 2B) with the exception of Ph. angustifolia that in theuneven Cistusmixture (UC) accumulated significantly more Zn thanin isolation.
3.3. Mass loss and nutrient dynamics of litter mixtures: observedand expected values
Results for monospecific litters evidence that, after 403 days,Cistus lost 62% of its initial mass, compared to 45% for Ph. angusti-folia, 39% for Q. ilex and 36% for P. lentiscus; differences betweenspecies were all statistically significant (P < 0.001), except thedifference between P. lentiscus and Q. ilex.
In the mixtures with Quercus observed values of mass loss werehigher than expected (Fig. 4; P ¼ 0.001 for the mixtures pooledtogether, MQ), whereas in the mixtures with Cistus the observedmass loss were lower than expected (Fig. 4; P ¼ 0.035 for themixtures pooled together, MC). Student t-test revealed that within
-60
-50
-40
-30
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-10
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Q. ilex
Ph. angustifolia
gg
m(
tn
uo
ma
ni
ng
il
ni
se
gn
ah
C1
-
)s
sa
mr
et
ti
ll
ai
ti
ni
-60
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0
(e
sa
el
eR
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An
Mµ
gg
1-
)s
sa
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et
ti
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0
50
100
150
200
250Cistus sp.
-60
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0
20
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250P. lentiscus
Fig. 3. Changes, over 403 days litter incubation in situ, in lignin amount andconcomitant changes in Mn amount in four Mediterranean maquis species decom-posing alone (open bars) and in mixture (closed bars): dark grey and light greyrespectively for all Quercus mixtures and all Cistus mixtures pooled together. Positivevalues are accumulation; negative values are losses. Values are mean � SE.
G. Maisto et al. / Soil Biology & Biochemistry 43 (2011) 520e530526
a single mixture the difference between observed and expectedvalue was statistically significant in the uneven mixture withQuercus dominant (UQ; P ¼ 0.05), and close to statistical signifi-cance in the uneven mixture with Ph. angustifolia dominant (UPh;P ¼ 0.09), and with P. lentiscus dominant (UP; P ¼ 0.06).
Over the 403 days incubation period, a net N immobilization(Fig. 4) significantly higher than expected, occurred in the mixtureswith Q. ilex (P¼ 0.043 for the mixtures pooled together, MQ). As thepattern of N dynamics was biphasic (immobilization followed byrelease) in all litter species (Fig. 1), we show separately immobili-zation in and release from the mixtures in Fig. 5. The magnitude ofN immobilization in the mixtures with Q. ilex was significantlyhigher than expected (P ¼ 0.019 for the mixtures pooled together,
MQ) while the magnitude of N release was similar (Fig. 5). Observedand expected values of N immobilization and N release in themixtures with Cistus were not significantly different (Fig. 5).
In the mixtures with Q. ilex, the difference between observedand expected value for net changes of Mn (Fig. 4) was quite small inboth the uneven mixtures with Ph. angustifolia dominant (UPh) andwith P. lentiscus dominant (UP). In contrast in UQ, the mixture withlitter of Q. ilex dominant, the observed net release of Mnwas lowerthan expected; in the even mixture with Quercus (EQ), both Mn netexchanges and immobilization were significantly higher thanexpected (Figs. 4 and 5). In Cistus mixtures (Fig. 4) observed andexpected values for net Mn accumulation were not significantlydifferent.
Observed and expected Ca changes (Figs. 4 and 5) were notsignificantly different either in the mixtures with Cistus or in themixtures with Q. ilex.
A net Mg accumulation occurred in all mixtures (Fig. 4) but thedifferences between observed and expected values were notsignificant with the exception of Mg immobilization (P ¼ 0.044) inthe uneven mixture with Cistus (Uc; Fig. 5).
K and Na were released from all mixtures (Fig. 4) and observedvalues were quite similar to those expected with the exception ofUC and Ec that released Na, contrary to what was expected.
Over the 403 days incubation period, Cu immobilization washigher than expected in nearly all mixtures (Fig. 4) and the differ-ences were significant for the mixtures with Q. ilex (P ¼ 0.046 forthe mixtures pooled together, MQ). The pattern of Cu dynamics wasbiphasic in Cistus (Fig. 1); however in the mixtures only in theimmobilization phase, observed values were significantly higherthan those expected (Fig. 5).
Over the 403 days incubation period, a net accumulation of Znoccurred in the mixtures with Q. ilex (Fig. 4) with statisticallysignificant differences for MQ. Zn dynamics had a biphasic pattern(Fig. 1) and both accumulation and release (Fig. 5) were signifi-cantly higher than expected in the mixtures with Q. ilex (dominantMQ; Fig. 5).
4. Discussion
At the individual litter level, the comparison of nutrientdynamics of four common Mediterranean maquis litters, decom-posing alone and in two types of 3-species mixtures (Fig. 2A, B),indicates that mixing influences the dynamics of N, Mn, Ca, Mg, Fe,Cu and Zn, but seems to scarcely affect the dynamics of K and Na.
At the whole mixture level (Figs. 4 and 5), the comparison ofobserved to expected values reveals the occurrence of non-additiveeffects of litter mixing on movements of N, Mn, Fe, Cu, and Zn to orfrom the litterbags containing the mixtures. Both in Cistusmixturesand in Quercus mixtures, the effects are synergic for N, Fe, Cu, andZn. As for Mn, a synergic effect occurs only in Quercus mixtures.Thus the composition in species of the mixture affects nutrientdynamics, whereas the relative amount of the species componentthe mixture is not relevant.
The initial N concentrationwas low in all litters and Nwas takenup from outside the litterbags during the early stages of decompo-sition. Litter mixing increases the magnitude of the accumulationprocess even in Cistus mixtures where antagonistic effects for littermass loss have been detected (Fig. 4). In contrast littermixing seemsto not affect N release. The amount of N released in the later phasewas smaller than the amount of N accumulated in the early phase;thus most of the nitrogen taken up is still immobilized in the litterafter 403 days decomposition and will be likely slowly releasedthereafter as observed by Fioretto et al. (2005) in a 3 years researchon Q. ilex, C. incanus andM. communis at the Castel Volturno NatureReserve. As the N immobilization phase occurs during the rainy
gg
m(
N1
-
)
0
2
4
6
8
)%
(s
so
Ls
sa
M
36
48
gg
m(
aC
1-
)
-2
0
2
gg
m(
nM
1-
)
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gg
m(
eF
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)
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gg
m(
gM
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)
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0,0
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gg
m(
aN
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)
-1,0
-0,5
0,0
0,5
gg
m(
K1
-
)
-4
-2
0
gg
m(
nZ
1-
)
0,0
0,3
0,6
gg
µ(
uC
1-
)
0
1
2
3
UP
UPh
UQ
EQ
EC
UC
UP
UPh
UQ
EQ
EC
UC
MC
MQ
MC
MQ
a
b
a
b
a
b
ab
a
b
a
b
a
b
a
b
a
b
a
b
a
b
Fig. 4. Observed (open bars) and expected (closed bars) mass loss (ash free), and net nutrient changes per gram of initial litter mass, in 3-species mixtures (see Fig. 2 for legend) ofMediterranean maquis litters over 403 days decomposition in situ.
G. Maisto et al. / Soil Biology & Biochemistry 43 (2011) 520e530 527
season, the higher immobilization in litter mixtures compared tomonospecific litters increases the efficiency of N conservation in thesystem, that is nutrient poor, and avoids hazardous N losses. Non-additive effects for N release were reported by McTiernan et al.(1997) for seven tree leaf litter types in all possible two-littercombinations; N release from mixtures was significantly lower infourmixtures, and significantly higher in onemixture, and generallyoccurred later than expected. Salamanca et al. (1998) founda synergistic effect formass loss ofmixed litter of Pinus andQuercus;howeverN content of Pinus litterwas higher thanpredicted,while Ncontent of Quercus was lower than predicted due to interactiveeffect ofmixed litter; nutrient translocation fromnutrient-rich litterto nutrient-poor litter had occurred. Gartner and Cardon (2006)observed lower N accumulation in sugar maple and red oak littermixtures than predicted from observed dynamics in single-specieslitterbags, although the significance of the difference depended onthe site of origin of the litter.
After a review by Gartner and Cardon (2004), nutrient transferamong leaves of different species is strikingwith 76% of themixturesshowing non-additive dynamics of nutrient concentrations.
Most of the literature data deals with N, while Mn dynamics hasbeen scantly considered. The dynamics of Mn in the four mono-specific litters is related to the initial Mn concentration and in thecase of Cistus to its ability to accumulate huge amount of thisnutrient (Fig. 1). Mn is a nutrient known to influence lignindegradation as it is a cofactor of MnP, the most wide-spreadperoxidase produced by fungi (Hofrichter et al., 2001). Consistentwith the low initial Mn concentration, lignin degradation appearsto be inhibited in Ph. angustifolia and P. lentiscus (Fig. 3). In contrast,the high initial Mn concentration in Q. ilex litter results in highlignin degradation (Fig. 3). In Cistus litter a strong accumulation ofMn, in the early decomposition stage, up to values higher thanthose of Q. ilex (Fig. 1), is followed by Mn release and lignindegradation. Mn release may correspond to availability of the
gg
m(
N1
-
)
-6
-3
0
3
6
9
gg
m(
aC
1-
)
-2
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gg
m(
nM
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)
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)-2
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EC
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gg
µ(
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-2
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MQ
MC
a
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ba
b
a
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a
b
a
b
a
b
a
b
ab
Fig. 5. Observed (open bars) and expected (closed bars) values of immobilization and release of six nutrients with biphasic dynamics in 3-species mixtures (see Fig. 2 for legend) ofMediterranean maquis litters decomposing in situ.
G. Maisto et al. / Soil Biology & Biochemistry 43 (2011) 520e530528
nutrient to microorganisms, allowing ligninolysis (Virzo De Santoet al., 2009). Lignin decomposition has been found to be posi-tively correlated to litter Mn concentration (Berg et al., 2007; Daveyet al., 2007; Virzo De Santo et al., 2009). Thus, it seems reasonablethat Mn availability may control lignin degradation also in the fourinvestigated Mediterranean litter species. At the individual litterlevel, litter mixing significantly increases Mn release from Q. ilexlitter in two out of four mixtures, i.e. EQ and UPh; moreover, inmixture, Q. ilex degrades more lignin than in isolation (Fig. 3). It isinteresting that Ph. angustifolia and P. lentiscus in mixture increaseMn immobilization compared to monospecific litters (Fig. 3) butthey do not degrade lignin either in mixture or in isolation (Fig. 3)likely because a threshold value for microorganisms demand hasnot yet been reached. In contrast, Cistus in mixture accumulates Mnamounts greater than in isolation; nevertheless lignin degradationin mixture is inhibited (Fig. 3); this is consistent with the antago-nistic effects of litter mixing detected for mass loss (Fig. 4) likelydue to allelopathic substances produced by one (Magiatis et al.,1999) or more of litters constituting the mixture. Net Mnexchange (Fig. 4) of Q. ilex mixtures was very low; however in theeven mixture (EQ) observed Mn immobilization (Fig. 5) wassignificantly higher (P < 0.001) than expected suggesting a syner-gistic effect. Mn exchanges of Cistus mixtures were higher than Mnexchanges of Q. ilex mixtures but the effects of mixing seem to bemainly additive. The effects of litter mixing, as in the case of N, arepositive as they contribute to Mn conservation in the litter system,increasing the availability of this important nutrient to the litterspoorer in Mn (Figs. 4 and 5).
In the mixtures with Q. ilex, Fe and Cu exhibited higher immo-bilization, and Zn both higher immobilization and release, than itwas expected.
We hypothesize that non-additive effects of litter mixing onmovements of N, Fe, Cu and Zn, towards and/or from the litterbags,are due to more efficient processes performed by microbialcommunities that may share a pool of integrated resources offered
by the mixture as a whole thus counteracting limitations for singlelitters. This hypothesis is supported by the higher than expectedmass loss of the mixtures with Q. ilex, that contain litters of thesame functional group (three sclerophylls). In contrast themixtureswith Cistus that contain litters of two different functional groups(two sclerophylls and a mesophyll) have lower than expected massloss, i.e. non-additive antagonistic effects occur, but nutrient fluxesare just additive. A parallel study performed on the same littersshowed that fungal diversity was higher on mixed litters than onmonospecific litters, both for Quercus and Cistusmixtures (Lunghiniet al., 2010). Chapman and Newman (2010) report that bothmicrobial abundance and diversity increase on litters in mixture;however decomposition is stimulated and produce synergisms onlywhen mixed litters are functionally similar. They observed that themicrobial community on functionally different litters were distinctand suggested that these distinct communities have high fidelity tocertain substrate types that their respective sets of enzymes areable to process most efficiently; thus synergisms did not occur foraspen litter in mixture with conifer litters due to a lack of a partnercommunity. Further research is needed to fully understand themechanisms behind the effects of litter diversity on microbialcommunity composition and the feedback on decomposition ratesand nutrient dynamics. Nevertheless Hoorens et al. (2003), Wardleet al. (2006), Chapman and Koch (2007), and Bonanomi et al. (2010)report non-additive effect for functionally uniform litter mixturesand additive effects for contrasting quality mixtures.
In a study with litterbags containing mixtures with differentrelative abundance (evenness) of peatland species, Ward et al.(2010) found that higher levels of species evenness increasedrates of decomposition and that the identity of the dominantspecies influenced rates of decomposition and was responsible fornon-additive effects. In this study, the relative abundance of thespecies contained in the mixture seems to play no relevant role andnon-additive effects occur only when species of the same func-tional group are mixed. This gives further support to our hypothesis
G. Maisto et al. / Soil Biology & Biochemistry 43 (2011) 520e530 529
that microbial communities of litters belonging to the same func-tional group (Q. ilex mixtures) may more easily interact to promotenutrient retention in the system. On the contrary in Cistusmixtures,the presence of a species belonging to a different functional group,with different morpho-functional characteristics, generally richerin nutrients and with a more rapid decomposition, favours higherfluxes of most nutrients towards and from the mixture. Accordingto Ball et al. (2008), effects of litter diversity on the decompositionprocess are mediated by species composition rather than speciesrichness. Moreover Ball et al. (2009), in a study on nutrient releasefrom mixed litters of a deciduous hardwood forest, found that thepresence of nutrient-rich species in the mixture facilitated N and Prelease whereas the presence of nutrient-poor species facilitatednutrient retention. After Swan et al. (2009), species richness andevenness alone do not explain variation in decomposition rate, butan interaction between the two does.
In this study we considered two types of three species mixturesthat reflect litter composition in two distinct types of patch i.e. theedge maquis/gaps and the inner maquis. Soil nutrient content andmicrobial activity in the two types of patches are very different andlargely depend on the different plant cover (Rutigliano et al., 2004);moreover the turnover of soil organicmatter is higher in the gaps ascompared to the neighbouring low maquis (De Marco et al., 2008).The pattern of mass loss and nutrient changes of the two types ofmixtures (three species of the same functional group; three speciesof two different functional groups) is consistent with the chemicaland microbiological characteristics of low maquis’ soil and of gap’ssoil. Thus although the species diversity of the maquis communityis very high and the species assemblage varies across the landscape,they are all sclerophyllous shrubs and belong to the same functionalgroup. At the edge maquis/gaps a different functional groupadjoins, that of the mesophyllous shrub Cistus that produces litterof different quality, able to affect interactions among decomposinglitters. The important role of plant functional groups on decom-position has been reviewed by Cornwell et al. (2008). The investi-gation of two key types of mixtures, with attention to the twomainfunctional plant groups in the research area, gives informationabout the effects of mixing on nutrient dynamics that can be usefulwhen scaling-up nutrient fluxes at the maquis ecosystem level.
5. Conclusions
The study demonstrates that mass loss is enhanced (synergisticeffect) in leaf litter mixtures of three sclerophyllous shrubs, andretarded (antagonistic effect) in leaf litter mixtures of two scle-rophyllous with a mesophyllous shrub. The two types of mixtures,with different proportion of the component species, reflect littercompositionwithin two different types of patches, inner maquis andthe edge maquis/gaps, of the spatially heterogeneous maquis plantcover. The findings demonstrate that the interactions among littersdo not affect in the sameway litter nutrient dynamics and litter massloss. Synergistic effects on N accumulation have been observed in allmixtures. As the accumulation phase occurs during the rainy season,it is suggested that interactions among litters in the mixturesimprove N conservation in the system that is poor in nitrogen.
In Quercus mixtures, net Mn exchanges (import/export) of thelitterbags were very small; however Mn release from the nutrient-rich litter of Q. ilex was accompanied by the increase of Mn in thenutrient-poor litters Ph. angustifolia and P. lentiscus; this againsuggests that the mixtures, compared to single litters, are a moreconservative system avoiding nutrient losses into the surroundingsoil. Huge amount of Mn were accumulated in Cistus litter duringthe early decomposition phase; however this did not promotea similar increase in Mn amount in the two nutrient-poorer littersPh. angustifolia and P. lentiscus component the mixture. Thus Cistus
litter in mixture appears to be a sink for Mn; moreover, consistentlywith the antagonistic effect observed for litter mass loss in Cistusmixtures, despite Mn increase, lignin degradation was inhibited inCistus litter when in mixture.
Synergistic effects for Fe, Cu and Zn dynamics have beenobserved in all mixtures.
Consistently with other researches, our findings indicate that atthe ecosystem level litter decomposition and nutrient dynamics arenot predictable from those of component species. The mechanismsbehind the interactions among litters deserve more attention,particularly the effects of litter diversity on microbial communitycomposition and the feedback on decomposition rates and nutrientdynamics.
Acknowledgments
We are grateful to the Forest Service of the Castel VolturnoNature Reserve for logistic support and Dr. N. Di Fusco for allowingus to use the field site. We thank two anonymous referees for theirconstructive comments on the earlier version of the manuscript.This study was supported by MIUR e PRIN 2005.
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