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Biol Fertil Soils (2006) 43: 30–38
DOI 10.1007/s00374-005-0058-1

 ORIGINA L PA PER



F. Caravaca . G. Tortosa . L. Carrasco .
J. Cegarra . A. Roldán

Interaction between AM fungi and a liquid organic amendment
with respect to enhancement of the performance
of the leguminous shrub Retama sphaerocarpa
Received: 6 June 2005 / Revised: 14 October 2005 / Accepted: 18 October 2005 / Published online: 14 December 2005
# Springer-Verlag 2005


Abstract This study examined the interactions between            Keywords Aggregate stability . Arbuscular mycorrhizal
the inoculation with three arbuscular mycorrhizal fungi,         fungi . Dry olive residue . Microbial biomass C .
namely, Glomus intraradices, Glomus deserticola and Glo-         Semi-arid environments . Soil enzyme activities
mus mosseae, and the addition of a liquid organic amend-
ment at different rates (0, 50, 100 or 300 mg C of liquid
amendment per kilogram soil) obtained by alkaline extrac-        Introduction
tion of composted dry olive residue with respect to their
effects on growth of Retama sphaerocarpa seedlings and           Legumes are among the most effective species in reveg-
on some microbiological and physical properties of soil.         etation programmes because of their ability to form sym-
One year after planting, both mycorrhizal inoculation            biotic associations with both nitrogen-fixing bacteria and
treatments and the addition of amendment had increased           arbuscular mycorrhizal (AM) fungi. They have been con-
plant growth and dehydrogenase, urease and benzoyl               sidered useful for revegetation of dry Mediterranean hab-
argininamide hydrolysing activities. The inoculation with        itats that have low availability of nitrogen, phosphorus and
G. mosseae increased plant growth to a greater extent than       other nutrients (Moro et al. 1997). A leguminous species
the addition of the amendment (about 35% greater than            common in semi-arid environments of south-east Spain is
plants grown in the amended soil and about 79% greater           Retama sphaerocarpa (L.) Boissier, which has a deep root
than control plants) and both treatments produced similar        system, whose functionality is maintained at depths of
increases in soil aggregate stability (about 31% higher than     more than 25 m (Haase et al. 1996) that allows the plant
control soil). The organic amendment produced a very sig-        access to deep water sources; in addition, this shrub is
nificant decrease in the levels of microbial biomass C and a     capable of resisting the frequent droughts of arid and semi-
strong increase in soil dehydrogenase and urease activities,     arid zones. Also, R. sphaerocarpa and its conspicuous
which were proportional to the amendment rate. Only the          understorey vegetation of annual and perennial species
combined treatment involving the addition of a medium            constitute “fertility islands” (Moro et al. 1997), which are
dose of amendment (100 mg C kg−1 soil) and the mycor-            points of high biological activity scattered in a heteroge-
rhizal inoculation with G. intraradices or G. deserticola        neous landscape. Several studies have demonstrated the
produced an additive effect on the plant growth with respect     benefits of AM inoculation of these shrubs in semi-arid
to the treatments applied individually (about 77% greater        soils (Caravaca et al. 2003a). The selection of efficient AM
than plants grown in the amended soil and about 63%              fungi is a major topic in inoculation programmes, espe-
greater than inoculated plants).                                 cially in disturbed soils where the indigenous inoculum
                                                                 levels of AM fungi are considered as being low, which may
                                                                 limit the successful establishment of plants (Palenzuela et
                                                                 al. 2002; Azcón-Aguilar et al. 2003).
                                                                    The addition of organic materials can increase fertility
                                                                 and improve the physical and biological properties of de-
F. Caravaca (*) . G. Tortosa .
L. Carrasco . J. Cegarra . A. Roldán                             graded soils (Roldán et al. 1996). Among the organic
Department of Soil and Water Conservation,                       amendments, the agronomic use of dry olive residue (DOR)
CSIC-Centro de Edafología y Biología Aplicada del Segura,        or “alperujo” has increased steadily in recent years due to its
P.O. Box 164, Campus de Espinardo,                               high C and mineral nutrient content (Nogales et al. 1999).
30100 Murcia, Spain
e-mail: fcb@cebas.csic.es                                        However, these residues contain phenolic compounds that
Tel.: +34-968-396337                                             may have a negative effect on microbial activity, inhibit the
Fax: +34-968-396213                                              establishment of AM symbioses and decrease the plant
31
Table 1 Chemical, biochemical, microbiological and physical      Materials and methods
characteristics of the soil
pH (H2O)                                    8.5±0.0a             Materials
EC (1:5, μs cm−1)                           225±2
Texture                                     Loam                 The soil was a Typic Haplocalcid (Soil Survey Staff 1999)
Total organic C (g kg−1)                    10.3±0.3             with a texture loam developed from Quaternary sediments
Total carbohydrates (μg g−1)                552±20               (Table 1). It was collected from Los Cuadros in the
Water-soluble C (μg g−1)                    100±1                province of Murcia, south-east Spain (coordinates 1°05'W
Water-soluble carbohydrates (μg g−1)        8±0                  and 38°10'N). The climate is semi-arid Mediterranean with
Total N (g kg−1)                            0.95±0.02            an average annual rainfall of 300 mm and a mean annual
Available P (μg g−1)                        7±0                  temperature of 19.2°C; the potential evapotranspiration
Extractable K (μg g−1)                      222±4                reaches 1,000 mm year−1.
Microbial biomass C (μg g−1)                396±11                  The amendment used was the organic fraction extracted
Dehydrogenase (μg INTF g−1)                 51±1                 with KOH from a composted DOR (Alburquerque et al.
Urease (μmol NH3 g−1 h−1)                   0.31±0.03
                                                                 2005) collected from an olive mill in Granada, Spain. The
Protease-BAA (μmol NH3 g−1 h−1)             0.60±0.04
                                                                 extract was obtained by mechanically shaking the com-
                                                                 posted DOR with 0.1 M KOH (1:20, w/v) for 24 h (12 h at
Phosphatase (μmol PNP g−1 h−1)              0.28±0.02
                                                                 25°C and 12 h at 70°). The suspension was centrifuged at
β-Glucosidase (μmol PNP g−1 h−1)            0.46±0.01
                                                                 14,644×g for 20 min. After centrifugation the particulate
Aggregate stability (%)                     11.5±0.4
                                                                 matter was eliminated of supernatant. The analytical char-
a
    Mean±standard error (N=6)                                    acteristics of the amendment are shown in Table 2.
                                                                    The plant used for the reafforestation experiment was R.
                                                                 sphaerocarpa, a low-growing shrub reaching a height of
                                                                 1.3–2.5 m and widely distributed in the Mediterranean area.
                                                                 It is also well adapted to drought and, therefore, frequently
growth (Martín et al. 2002; Linares et al. 2003). Studies        used in the reafforestation of semi-arid disturbed lands.
have shown that the effect of phenolic compounds con-
tained in DOR on AM root colonization can vary with the
type of fungi and the time of inoculation (Martín et al.         Mycorrhizal inoculation of seedlings
2002). DOR composting could minimise its antimicrobial
effect, but the composted DOR may contain phytotoxic             The mycorrhizal fungi used in the experiment, Glomus
compounds (Linares et al. 2003). On the other hand, the          intraradices Schenck & Smith, Glomus deserticola (Trappe,
organic fraction extracted with alkaline solutions from          Bloss & Menge) and Glomus mosseae (Nicol & Gerd.) Gerd.
organic materials has been used for improving plant growth       & Trappe, were obtained from the collection of the exper-
and nutrient uptake (Ayuso et al. 1996). This fraction may       imental field station of Zaidín, Granada.
have a positive effect on plant growth directly and/or
through the improvement in soil structure, cation exchange
capacity, microbiological activity and for complexing cer-       Table 2 Chemical characteristics of the KOH-soluble extract of dry
tain soil ions. However, there are no data on the effects of     olive residue
this organic fraction extracted from DOR on colonization of      Ash (%)                                          30.4
roots by AM fungi or on soil properties in revegetation          pH                                                9.83
programmes. Our hypothesis was that the combined actions         EC (mS cm−1)                                      9.78
of this liquid organic amendment and mycorrhiza on the           Organic matter (%)                               69.6
growth of Mediterranean shrub species could be higher than       Extractable C (g l−1)                             8.6
the sum of individual effects.                                   Fulvic acid C (g l−1)                             2.1
   The objectives of this study were (1) to assess the inter-    Humic acid C (g l−1)                              6.5
actions between the inoculation with three AM fungi and          Water-soluble carbohydrates (g l−1)               1.03
the addition of a liquid organic amendment obtained by           Phenols (g l−1)                                   1.58
alkaline extraction of composted DOR, with respect to their      Total N (mg l−1)                                320
effects on the growth of R. sphaerocarpa seedlings in a          Na (mg l−1)                                     186
degraded semi-arid Mediterranean soil, and (2) to establish      K (mg l−1)                                    1,776
the optimum levels of amendment addition, thereby avoid-         P (mg l−1)                                       62
ing possible negative effects on plant growth, AM coloni-        Ca (mg l−1)                                     136
zation and soil properties considered to be indicators of soil   Mg (mg l−1)                                      28.9
quality such as labile C fractions (microbial biomass C and
                                                                 Fe (mg l−1)                                       3.4
water-soluble C), enzyme activities (dehydrogenase, ure-
                                                                 Cu (mg l−1)                                       0.2
ase, protease-BAA, and β-glucosidase) and soil aggregate
                                                                 Mn (mg l−1)                                       0.3
stability.
                                                                 Zn (mg l−1)                                       1.2
32




                                                                                                                                                                                                                                                                                                                                                                                            14.0bcd 17.2defg 16.9cdefg 17.7efg
   The AM fungal inoculum consisted of a mixture of rhi-




                                                                                                                                                                                                                                                                                                                                                                                   310abcd 300abcd 324abcde 322abcde 354cde

                                                                                                                                                                                                                                                                                                                                                                                                                      248cde
                                                                                                                                                                                                                                                                                                                                                                                                                      8.47ab
zosphere soil from trap cultures (Sorghum sp.) containing




                                                                      Table 3 Soil physical–chemical properties of R. sphaerocarpa after 1 year of growth in response to mycorrhizal inoculation treatments and KOH extract of DOR addition (n=4)
spores, hyphae and mycorrhizal root fragments. Once




                                                                                                                                                                                                                                                                      3
germinated, seedlings were transplanted into the growth
substrate consisting of peat and cocopeat (1:1, v/v). The




                                                                                                                                                                                                                                                                                                                                                                                                            254cde
                                                                                                                                                                                                                                                                                                                                                                                                            8.43ab
corresponding AM inoculum was applied at a rate of 5%
(v/v). The same amount of an autoclaved mixture of the




                                                                                                                                                                                                                                                                      2
inocula was added to control plants, supplemented with
a filtrate (Whatman No. 1 paper) of the pot culture of all




                                                                                                                                                                                                                                                                                                                                                                                                   8.40ab


                                                                                                                                                                                                                                                                                                                                                                                                   283e
three AM fungi to provide the microbial populations




                                                                                                                                                                                                                                                                      1
accompanying the mycorrhizal fungi. Inoculated and non-




                                                                                                                                                                                                                                                    G. mosseae
inoculated seedlings were grown for 8 months under nurs-




                                                                                                                                                                                                                                                                                                                                                                                   209bcd 270de
ery conditions without any chemical fertiliser treatment.




                                                                                                                                                                                                                                                                                                                                                                                           8.39a
                                                                                                                                                                                                                                                                      0




                                                                                                                                                                                                                                                                                                                                                                   18.5fg 17.0cdefg 19.2g
Experimental design and layout




                                                                                                                                                                                                                                                                                                                                                                                   8.34a
                                                                                                                                                                                                                                                                      3
The experiment was a mesocosm assay, conducted as a
completely randomized factorial design with two factors.




                                                                                                                                                                                                                                                                                                                                                          200bc 225cde 249cde
                                                                                                                                                                                                                                                                                                                                                          347bcde 357de 290ab
The first factor had four levels: without and with the




                                                                                                                                                                                                                                                                                                                                                          8.47ab 8.46ab 8.34a
addition of low, medium or high doses of the liquid




                                                                                                                                                                                                                                                                      2
amendment to the soil. The second factor had four levels:
non-inoculation and inoculation of R. sphaerocarpa plants
                                                                                                                                                                                                                                                    G. deserticola
with one of three AM fungi (G. intraradices, G. deserticola
                                                                                                                                                                                                                                                                      1
or G. mosseae) in the nursery. Four replicates per treatment




                                                                                                                                                                                                                                                                                                                                13.7bcd 14.6bcde 15.0bcdef 11.0a
were carried out, making a total of 64 pots.
   Two kilograms of substrate, consisting of soil and ver-




                                                                                                                                                                                                                                                                                                                                                                                                                                   0, 1, 2 or 3 indicates 0, 5.8, 11.7 or 35.1 ml amendment kg−1 soil/vermiculite mixture, respectively
                                                                                                                                                                                                                                                                      0

miculite at a ratio of 3:1 (v/v), were placed in 3.6-l pots. In
March 2003, R. sphaerocarpa seedlings (inoculated and
                                                                                                                                                                                                                                                                                                                                                 240cde
                                                                                                                                                                                                                                                                                                                                                 8.48ab


non-inoculated) were transplanted to the pots (one per pot).
                                                                                                                                                                                                                                                                                                                       303abcd 315abcde 320abcde 374e


Two weeks after planting, the amendment was applied to
                                                                                                                                                                                                                                                                      3




the pots at a rate of 0, 5.8, 11.7 or 35.1 ml kg−1 soil/vermiculite


                                                                                                                                                                                                                                                                                                                                                                                                                                 Values in rows followed by the same letter are not significantly different (LSD, p<0.05)
mixture, which corresponds to the addition of 0, 50, 100 or
                                                                                                                                                                                                                                                                                                                                        8.44ab




300 mg C liquid amendment kg−1 soil. The experiment was
                                                                                                                                                                                                                                                                                                                       213bcd 228cde 184a




carried out in the nursery of the University of Murcia (Murcia,
                                                                                                                                                                                                                                                                      2




Spain) without the addition of chemical fertiliser. The plants
were well watered and kept outdoors under ambient irradi-
                                                                                                                                                                                                                                                    G. intraradices


                                                                                                                                                                                                                                                                                                                               8.31a




ance, temperature and air humidity. One year after planting,
                                                                                                                                                                                                                                                                      1




the plants were harvested and rhizosphere soil samples of the
pots were taken. Rhizosphere soil samples, air-dried to 20%
                                                                                                                                                                                                                                                                                                  13.5bc 13.1b 14.8bcde 10.8a
                                                                                                                                                                                                                                                                                                                       8.34a




moisture content and sieved to less than 2 mm, were divided
                                                                                                                                                                                                                                                                      0




into two subsamples. One subsample was stored at 2°C for
microbiological analysis, and another subsample was allowed
to dry at room temperature for physical–chemical analysis.
                                                                                                                                                                                                                                                                                                        8.58b 8.60b
                                                                                                                                                                                                                                                                                         310abcd 287ab 294abc 278a

                                                                                                                                                                                                                                                                                                 208bcd 188ab 174a
                                                                                                                                                                                                                                                                      3




Plant analyses
                                                                                                                                                                                                                                                                      2




Basal stem diameters and heights of plants were measured
                                                                                                                                                                                                                                                                                                 8.58b




with callipers and rulers. Fresh and dry (105°C, 5 h) masses
                                                                                                                                                                                                                                                    No mycorrhiza




of shoots and roots were recorded. Plant tissues were
                                                                                                                                                                                                                                                                      1




ground before chemical analysis. Plant P was determined
                                                                                                                                                                                                                                                                                                                                                                                                                                 DOR Dry olive residue
                                                                                                                                                                                                                                                                                          10.6a




colorimetrically according to Murphy and Riley (1962)
                                                                                                                                                                                                                                                                                         8.56b


                                                                                                                                                                                                                                                                          Water-soluble 183a




after digestion in nitric–perchloric acid (5:3) for 6 h at
                                                                                                                                                                                                                                                                      a
                                                                                                                                                                                                                                                                      0




210°C. Plant N was determined by combustion at 1,020°C
                                                                                                                                                                                                                                                                           stability (%)
                                                                                                                                                                                                                                                                           C (μg g−1)




in a carbon and nitrogen analyser and reduction, separation
                                                                                                                                                                                                                                                                          Aggregate
                                                                                                                                                                                                                                                                          pH (H2O)

                                                                                                                                                                                                                                                                           μs cm−1)
                                                                                                                                                                                                                                                                          EC (1:5,




of N2 in a chromatographic column and measurement in a
thermic conductivity detector. Plant K was estimated by
flame photometry (Schollemberger and Simon 1954).
                                                                                                                                                                                                                                                                                                                                                                                                                                 a
33

   The percentage of root length colonized by AM fungi was       passed through the same 0.250-mm sieve with the assis-
calculated by the gridline intersect method (Giovannetti and     tance of a small stick to break the remaining aggregates.
Mosse 1980) after staining with trypan blue (Phillips and        The residue remaining on the sieve, which was made up of
Hayman 1970).                                                    plant debris and sand particles, was dried at 105°C and
                                                                 weighed (P2). The percentage of stable aggregates with
                                                                 regard to the total aggregates was calculated by the
Soil analyses                                                    following relationship (P1−P2)×100/(4−P2+T).

Soil pH and electrical conductivity were measured in a 1:5
(w/v) aqueous solution. In soil aqueous extracts (1:5),          Statistical analysis
water-soluble C was determined with an automatic carbon
analyser for liquid samples (Shimadzu TOC-5050A).                Data were log-transformed to achieve for normality.
   Microbial biomass C was determined by the fumigation–         Amendment addition, mycorrhizal inoculation and their
extraction method (Vance et al. 1987). Ten grams of soil at      interaction effects on measured variables were tested by a
60% of field capacity was fumigated in a 125-ml Erlenmeyer       two-way analysis of variance, and comparisons among
flask with purified CHCl3 for 24 h. After removal of             means were made using the least significant difference
residual CHCl3, 40 ml of 0.5 M K2SO4 solution was added          (LSD) test calculated at p<0.05. Statistical procedures were
and the sample was shaken for 1 h before filtration of the       carried out with the software package SPSS 10.0 for
mixture. The K2SO4-extracted C was measured as indi-             Windows.
cated for water-soluble C. Microbial biomass C was cal-
culated as the difference between the C of fumigated and
non-fumigated samples divided by the calibration factor          Results
KEC=0.38.
   Dehydrogenase activity was determined according to            Soil parameters
Trevors et al. (1982). For this, 1 g of soil at 60% of field
capacity was exposed to 0.2 ml of 0.4% 2-p-iodophenyl-3-p-       Only the mycorrhizal treatments with G. intraradices and
nitrophenyl-5-phenyltetrazolium chloride (INT) in distilled      G. mosseae significantly decreased soil pH (Tables 3 and
water for 20 h at 22°C in the dark. The iodonitrotetrazolium     4). However, neither amendment addition nor the interac-
formazan (INTF) formed was extracted with 10 ml of               tion of amendment × mycorrhizal inoculation had any sig-
methanol by shaking vigorously for 1 min and filtering           nificant effect on soil pH and electrical conductivity
through Whatman No. 5 filter paper. INTF was measured            (Table 4).
spectrophotometrically at 490 nm.
   Urease and N-α-benzoyl-L-argininamide (BAA) hydro-
lysing activities were determined in 0.1 M phosphate buffer
at pH 7; 1 M urea (Tabatabai and Bremner 1972) and               Table 4 Two-factor ANOVA (mycorrhizal inoculation treatments
0.03 M BAA (Ladd and Butler 1972) were used as                   and amendment addition) for all parameters studied in the
substrates, respectively. Two millilitres of buffer and 0.5 ml   rhizosphere soil of R. sphaerocarpa seedlings 1 year after planting
of substrate were added to 0.5 g of sample, which was            (P significance values)
incubated at 30°C (for urease) or 39°C (for protease) for                                Amendment      Mycorrhiza     Interaction
                                                        þ
90 min. Both activities were determined as the NH4 re-                                   (A)            (M)            (A×M)
leased in the hydrolysis reaction.
   β-Glucosidase was determined using p-nitrophenyl-β-D-         pH                        0.700         <0.001         0.814
glucopyranoside (PNG, 0.05 M) as substrate. This assay is        Electrical                0.669          0.079         0.169
based on the release and detection of p-nitrophenol (PNP).        conductivity
Two millilitres of 0.1 M maleate buffer (pH 6.5) and 0.5 ml      Water-soluble C          0.615           0.003         0.987
of substrate were added to 0.5 g of sample and incubated at      Aggregate stability     <0.001           0.014         0.362
37°C for 90 min. The reaction was stopped with tris(hydro        Microbial biomass C     <0.001           0.587         0.806
xymethyl)aminomethane (THAM) according to Tabatabai              Dehydrogenase            0.002           0.026         0.685
(1982). The amount of PNP was determined by spec-                Urease                  <0.001          <0.001         0.001
trophotometry at 398 nm (Tabatabai and Bremner 1969).            Protease                 0.643          <0.001         0.807
   The percentage of stable aggregates was determined by         β-Glucosidase            0.818           0.293         0.384
the method described by Lax et al. (1994). Sieved (0.2–          Shoot                    0.037           0.001         0.211
4 mm) soil (4 g) was placed on a small, 0.250-mm sieve           Root                     0.604           0.353         0.163
and wetted by spray. After 15 min the soil was subjected to
                                                                 N foliar                 0.006          <0.001         0.018
an artificial rainfall of 150 ml with energy of 270 J m−2.
                                                                 P foliar                 0.002          <0.001         0.003
The remaining soil on the sieve was placed in a previously
                                                                 K foliar                 0.319           0.001         0.028
weighed capsule (T), dried at 105°C and weighed (P1).
                                                                 Colonization             0.861          <0.001         0.547
Then the soil was soaked in distilled water and, after 2 h,
34
Table 5 Soil microbial biomass C and enzyme activities of R. sphaerocarpa after 1 year of growth in response to mycorrhizal inoculation treatments and KOH extract of DOR addition (n=4)
                                                                                                                                                                                                                                                                                                                                                                          Water-soluble C concentrations were increased only




                                                                                                                                                                                                                                                    0.27abc
                                                                                                                                                                                                                                           1.15ef
                                                                                                                                                                                                                                  0.61d
                                                                                                                                                                                                                                                                                                                                                                       with the mycorrhizal inoculation treatments (Tables 3 and




                                                                                                                                                                                                                         53.4f
                                                                                                                                                                                                                  42ab
                                                                                                                                                                                                             3                                                                                                                                                         4), the greatest increases being observed in the inoculation
                                                                                                                                                                                                                                                                                                                                                                       treatment with G. mosseae (on average, about 40% greater


                                                                                                                                                                                                                         42.4de




                                                                                                                                                                                                                                           1.15ef
                                                                                                                                                                                                                                  0.69d




                                                                                                                                                                                                                                                    0.32c
                                                                                                                                                                                                                  46ab                                                                                                                                                 than in the soil of non-inoculated plants).
                                                                                                                                                                                                                                                                                                                                                                          Both amendment addition and inoculation with G. mos
                                                                                                                                                                                                             2



                                                                                                                                                                                                                                                                                                                                                                       seae significantly increased soil aggregate stability, reach-




                                                                                                                                                                                                                                                    0.29abc
                                                                                                                                                                                                                         30.2ab

                                                                                                                                                                                                                                  0.19ab
                                                                                                                                                                                                                                                                                                                                                                       ing similar values at the end of the growth period (Tables 3


                                                                                                                                                                                                                                           1.50g
                                                                                                                                                                                                                  73bc




                                                                                                                                                                                                                                                                                                                                                                       and 4). In the amended soils, the percentage of stable
                                                                                                                                                                                                             1
                                                                                                                                                                                           G. mosseae




                                                                                                                                                                                                                                                                                                                                                                       aggregates did not vary with the dose of the amendment


                                                                                                                                                                                                                                                    0.28abc
                                                                                                                                                                                                                                                                                                                                                                       added. The highest aggregate stability was found in the
                                                                                                                                                                                                                         34.8bc

                                                                                                                                                                                                                                  0.19ab

                                                                                                                                                                                                                                           1.29fg
                                                                                                                                                                                                                  301e




                                                                                                                                                                                                                                                                                                                                                                       amended soil of plants inoculated with G. deserticola or G.
                                                                                                                                                                                                             0




                                                                                                                                                                                                                                                                                                                                                                       mosseae.
                                                                                                                                                                                                                                                                                                                                                                          The addition of the amendment decreased soil microbial
                                                                                                                                                                                                                                                    0.26abc
                                                                                                                                                                                                                         43.8de

                                                                                                                                                                                                                                  0.56cd

                                                                                                                                                                                                                                           0.57b



                                                                                                                                                                                                                                                                                                                                                                       biomass C for both non-inoculated and inoculated plants,
                                                                                                                                                                                                                  81c




                                                                                                                                                                                                                                                                                                                                                                       particularly for the plants inoculated with G. mosseae or
                                                                                                                                                                                                             3




                                                                                                                                                                                                                                                                                                                                                                       G. intraradices (Table 5). In general, microbial biomass C
                                                                                                                                                                                                                         46.0de




                                                                                                                                                                                                                                           0.69bc




                                                                                                                                                                                                                                                                                                                                                                       decreased as the dose of amendment increased. Microbial
                                                                                                                                                                                                                                  0.83e




                                                                                                                                                                                                                                                    0.31c
                                                                                                                                                                                                                  180d




                                                                                                                                                                                                                                                                                                                                                                       biomass C was not affected by the mycorrhizal inocula-
                                                                                                                                                                                                             2




                                                                                                                                                                                                                                                                                                                                                                       tion treatments (Table 4). With the exception of G. desert
                                                                                                                                                                                                                                                    0.27abc




                                                                                                                                                                                                                                                                                                                                                                       icola, the mycorrhizal inoculation alone produced sig-
                                                                                                                                                                                                                         31.3ab




                                                                                                                                                                                                                                           0.75bc
                                                                                                                                                                                                                                  0.24b
                                                                                                                                                                                                                  149d
                                                                                                                                                                                           G. deserticola




                                                                                                                                                                                                                                                                                                                                                                       nificantly higher dehydrogenase and benzoyl arginina-
                                                                                                                                                                                                             1




                                                                                                                                                                                                                                                                                                                                                                       mide hydrolysing activities than the control soil (Table 5).
                                                                                                                                                                                                                                                                                                                                                                       In general, neither amendment addition nor mycorrhizal
                                                                                                                                                                                                                                                    0.25abc
                                                                                                                                                                                                                         29.8ab

                                                                                                                                                                                                                                  0.14ab

                                                                                                                                                                                                                                           0.46a




                                                                                                                                                                                                                                                                                                                                                                       inoculation modified β-glucosidase activity. The medium
                                                                                                                                                                                                                  288e




                                                                                                                                                                                                                                                                                                                                                                       and high dose of amendment significantly increased dehy-
                                                                                                                                                                                                             0




                                                                                                                                                                                                                                                                                                                                                                       drogenase and urease activities. Only urease activity
                                                                                                                                                                                                                                           0.84cd

                                                                                                                                                                                                                                                    0.22ab




                                                                                                                                                                                                                                                                0, 1, 2 or 3 indicates 0, 5.8, 11.7 or 35.1 ml amendment kg−1 soil/vermiculite mixture, respectively
                                                                                                                                                                                                                                  0.66d
                                                                                                                                                                                                                         47.5e




                                                                                                                                                                                                                                                                                                                                                                       increased proportionally with the increase in the amend-
                                                                                                                                                                                                                  35a




                                                                                                                                                                                                                                                                                                                                                                       ment dose. The interaction amendment × mycorrhizal
                                                                                                                                                                                                             3




                                                                                                                                                                                                                                                                                                                                                                       inoculation had no significant effect on the biochemical
                                                                                                                                                                                                                         40.9cd

                                                                                                                                                                                                                                  0.56cd

                                                                                                                                                                                                                                           0.68bc

                                                                                                                                                                                                                                                    0.29bc




                                                                                                                                                                                                                                                                                                                                                                       properties (Table 4).
                                                                                                                                                                                                                                                              Values in rows followed by the same letter are not significantly different (LSD, p<0.05)
                                                                                                                                                                                                                  86c
                                                                                                                                                                                                             2



                                                                                                                                                                                                                         30.0ab

                                                                                                                                                                                                                                  0.16ab

                                                                                                                                                                                                                                           0.96de

                                                                                                                                                                                                                                                    0.21a
                                                                                                                                                                                                                  167d
                                                                                                                                                                                           G. intraradices
                                                                                                                                                                                                             1




                                                                                                                                                                                                                                                                                                                                                                       Table 6 Growth parameters, foliar nutrient content and root
                                                                                                                                                                                                                                                    0.25abc
                                                                                                                                                                                                                         34.8bc

                                                                                                                                                                                                                                  0.14ab

                                                                                                                                                                                                                                           0.95de




                                                                                                                                                                                                                                                                                                                                                                       infection of R. sphaerocarpa in response to mycorrhizal inoculation
                                                                                                                                                                                                                  296e




                                                                                                                                                                                                                                                                                                                                                                       treatments and KOH extract of DOR addition previous to planting
                                                                                                                                                                                                                                                                                                                                                                       (n=4)
                                                                                                                                                                                                             0




                                                                                                                                                                                                                                                    0.25abc




                                                                                                                                                                                                                                                                                                                                                                                          No         G.           G.          G.
                                                                                                                                                                                                                         40.7cd

                                                                                                                                                                                                                                  0.56cd

                                                                                                                                                                                                                                           0.53ab




                                                                                                                                                                                                                                                                                                                                                                                          mycorrhiza intraradices deserticola mosseae
                                                                                                                                                                                                                  23a
                                                                                                                                                                                                             3




                                                                                                                                                                                                                                                                                                                                                                       Shoot              0.5a           0.7a          0.7a         0.5a
                                                                                                                                                                                                                         40.6cd




                                                                                                                                                                                                                                           0.48ab

                                                                                                                                                                                                                                                    0.23ab
                                                                                                                                                                                                                                  0.43c
                                                                                                                                                                                                                  70bc




                                                                                                                                                                                                                                                                                                                                                                        (g dry wt.
                                                                                                                                                                                                                                                                                                                                                                        plant−1)
                                                                                                                                                                                                             2




                                                                                                                                                                                                                                                                                                                                                                       Root               0.6ab          0.8b          0.7ab        0.5a
                                                                                                                                                                                                                                                    0.24abc
                                                                                                                                                                                                                                  0.19ab

                                                                                                                                                                                                                                           0.54ab




                                                                                                                                                                                                                                                                                                                                                                        (g dry wt.
                                                                                                                                                                                                                         26.0a
                                                                                                                                                                                                                  177d
                                                                                                                                                                                           No mycorrhiza




                                                                                                                                                                                                                                                                                                                                                                        plant−1)
                                                                                                                                                                                                             1




                                                                                                                                                                                                                                                                                                                                                                       Nitrogen           8a           13b           10ab           9a
                                                                                                                                                                                                                                                    0.26abc




                                                                                                                                                                                                                                                                                                                                                                        (mg plant−1)
                                                                                                                                                                                                                         26.1a

                                                                                                                                                                                                                                  0.05a

                                                                                                                                                                                                                                           0.44a
                                                                                                                                                                                                                  281e




                                                                                                                                                                                                                                                                                                                                                                       Phosphorus         0.6a           0.8ab         1.2b         1.0ab
                                                                                                                                                                                                             0a




                                                                                                                                                                                                                                                                                                                                                                        (mg plant−1)
                                                                                                                                                                                                                                                              DOR Dry olive residue
                                                                                                                                                                                                                   (μmol PNP g−1 h−1)
                                                                                                                                                                                                                   (μmol NH3 g−1 h−1)




                                                                                                                                                                                                                                                                                                                                                                       Potassium          7a            9a             9a           8a
                                                                                                                                                                                                                   (μg INTF g−1 soil)




                                                                                                                                                                                                                                                                                                                                                                        (mg plant−1)
                                                                                                                                                                                                                  Microbial biomass

                                                                                                                                                                                                                  Dehydrogenase




                                                                                                                                                                                                                  β-Glucosidase




                                                                                                                                                                                                                                                                                                                                                                       Colonization (%)   0.4a         61.9b         67.7b        51.8b
                                                                                                                                                                                                                  Protease-BAA
                                                                                                                                                                                                                   NH3 g−1 h−1)
                                                                                                                                                                                                                  Urease (μmol
                                                                                                                                                                                                                   C (μg g−1)




                                                                                                                                                                                                                                                                                                                                                                       Values in rows followed by the same letter are not significantly
                                                                                                                                                                                                                                                                                                                                                                        different (LSD, p<0.05)
                                                                                                                                                                                                                                                                                                                                                                       a
                                                                                                                                                                                                                                                                                                                                                                         0, 1, 2 or 3 indicates 0, 5.8, 11.7 or 35.1 ml amendment kg−1 soil/
                                                                                                                                                                                                                                                                                                                                                                        vermiculite mixture, respectively
                                                                                                                                                                                                                                                              a
2006 Caravaca et al liquid organic amendments and retama
2006 Caravaca et al liquid organic amendments and retama
2006 Caravaca et al liquid organic amendments and retama
2006 Caravaca et al liquid organic amendments and retama

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2006 Caravaca et al liquid organic amendments and retama

  • 1. Biol Fertil Soils (2006) 43: 30–38 DOI 10.1007/s00374-005-0058-1 ORIGINA L PA PER F. Caravaca . G. Tortosa . L. Carrasco . J. Cegarra . A. Roldán Interaction between AM fungi and a liquid organic amendment with respect to enhancement of the performance of the leguminous shrub Retama sphaerocarpa Received: 6 June 2005 / Revised: 14 October 2005 / Accepted: 18 October 2005 / Published online: 14 December 2005 # Springer-Verlag 2005 Abstract This study examined the interactions between Keywords Aggregate stability . Arbuscular mycorrhizal the inoculation with three arbuscular mycorrhizal fungi, fungi . Dry olive residue . Microbial biomass C . namely, Glomus intraradices, Glomus deserticola and Glo- Semi-arid environments . Soil enzyme activities mus mosseae, and the addition of a liquid organic amend- ment at different rates (0, 50, 100 or 300 mg C of liquid amendment per kilogram soil) obtained by alkaline extrac- Introduction tion of composted dry olive residue with respect to their effects on growth of Retama sphaerocarpa seedlings and Legumes are among the most effective species in reveg- on some microbiological and physical properties of soil. etation programmes because of their ability to form sym- One year after planting, both mycorrhizal inoculation biotic associations with both nitrogen-fixing bacteria and treatments and the addition of amendment had increased arbuscular mycorrhizal (AM) fungi. They have been con- plant growth and dehydrogenase, urease and benzoyl sidered useful for revegetation of dry Mediterranean hab- argininamide hydrolysing activities. The inoculation with itats that have low availability of nitrogen, phosphorus and G. mosseae increased plant growth to a greater extent than other nutrients (Moro et al. 1997). A leguminous species the addition of the amendment (about 35% greater than common in semi-arid environments of south-east Spain is plants grown in the amended soil and about 79% greater Retama sphaerocarpa (L.) Boissier, which has a deep root than control plants) and both treatments produced similar system, whose functionality is maintained at depths of increases in soil aggregate stability (about 31% higher than more than 25 m (Haase et al. 1996) that allows the plant control soil). The organic amendment produced a very sig- access to deep water sources; in addition, this shrub is nificant decrease in the levels of microbial biomass C and a capable of resisting the frequent droughts of arid and semi- strong increase in soil dehydrogenase and urease activities, arid zones. Also, R. sphaerocarpa and its conspicuous which were proportional to the amendment rate. Only the understorey vegetation of annual and perennial species combined treatment involving the addition of a medium constitute “fertility islands” (Moro et al. 1997), which are dose of amendment (100 mg C kg−1 soil) and the mycor- points of high biological activity scattered in a heteroge- rhizal inoculation with G. intraradices or G. deserticola neous landscape. Several studies have demonstrated the produced an additive effect on the plant growth with respect benefits of AM inoculation of these shrubs in semi-arid to the treatments applied individually (about 77% greater soils (Caravaca et al. 2003a). The selection of efficient AM than plants grown in the amended soil and about 63% fungi is a major topic in inoculation programmes, espe- greater than inoculated plants). cially in disturbed soils where the indigenous inoculum levels of AM fungi are considered as being low, which may limit the successful establishment of plants (Palenzuela et al. 2002; Azcón-Aguilar et al. 2003). The addition of organic materials can increase fertility and improve the physical and biological properties of de- F. Caravaca (*) . G. Tortosa . L. Carrasco . J. Cegarra . A. Roldán graded soils (Roldán et al. 1996). Among the organic Department of Soil and Water Conservation, amendments, the agronomic use of dry olive residue (DOR) CSIC-Centro de Edafología y Biología Aplicada del Segura, or “alperujo” has increased steadily in recent years due to its P.O. Box 164, Campus de Espinardo, high C and mineral nutrient content (Nogales et al. 1999). 30100 Murcia, Spain e-mail: fcb@cebas.csic.es However, these residues contain phenolic compounds that Tel.: +34-968-396337 may have a negative effect on microbial activity, inhibit the Fax: +34-968-396213 establishment of AM symbioses and decrease the plant
  • 2. 31 Table 1 Chemical, biochemical, microbiological and physical Materials and methods characteristics of the soil pH (H2O) 8.5±0.0a Materials EC (1:5, μs cm−1) 225±2 Texture Loam The soil was a Typic Haplocalcid (Soil Survey Staff 1999) Total organic C (g kg−1) 10.3±0.3 with a texture loam developed from Quaternary sediments Total carbohydrates (μg g−1) 552±20 (Table 1). It was collected from Los Cuadros in the Water-soluble C (μg g−1) 100±1 province of Murcia, south-east Spain (coordinates 1°05'W Water-soluble carbohydrates (μg g−1) 8±0 and 38°10'N). The climate is semi-arid Mediterranean with Total N (g kg−1) 0.95±0.02 an average annual rainfall of 300 mm and a mean annual Available P (μg g−1) 7±0 temperature of 19.2°C; the potential evapotranspiration Extractable K (μg g−1) 222±4 reaches 1,000 mm year−1. Microbial biomass C (μg g−1) 396±11 The amendment used was the organic fraction extracted Dehydrogenase (μg INTF g−1) 51±1 with KOH from a composted DOR (Alburquerque et al. Urease (μmol NH3 g−1 h−1) 0.31±0.03 2005) collected from an olive mill in Granada, Spain. The Protease-BAA (μmol NH3 g−1 h−1) 0.60±0.04 extract was obtained by mechanically shaking the com- posted DOR with 0.1 M KOH (1:20, w/v) for 24 h (12 h at Phosphatase (μmol PNP g−1 h−1) 0.28±0.02 25°C and 12 h at 70°). The suspension was centrifuged at β-Glucosidase (μmol PNP g−1 h−1) 0.46±0.01 14,644×g for 20 min. After centrifugation the particulate Aggregate stability (%) 11.5±0.4 matter was eliminated of supernatant. The analytical char- a Mean±standard error (N=6) acteristics of the amendment are shown in Table 2. The plant used for the reafforestation experiment was R. sphaerocarpa, a low-growing shrub reaching a height of 1.3–2.5 m and widely distributed in the Mediterranean area. It is also well adapted to drought and, therefore, frequently growth (Martín et al. 2002; Linares et al. 2003). Studies used in the reafforestation of semi-arid disturbed lands. have shown that the effect of phenolic compounds con- tained in DOR on AM root colonization can vary with the type of fungi and the time of inoculation (Martín et al. Mycorrhizal inoculation of seedlings 2002). DOR composting could minimise its antimicrobial effect, but the composted DOR may contain phytotoxic The mycorrhizal fungi used in the experiment, Glomus compounds (Linares et al. 2003). On the other hand, the intraradices Schenck & Smith, Glomus deserticola (Trappe, organic fraction extracted with alkaline solutions from Bloss & Menge) and Glomus mosseae (Nicol & Gerd.) Gerd. organic materials has been used for improving plant growth & Trappe, were obtained from the collection of the exper- and nutrient uptake (Ayuso et al. 1996). This fraction may imental field station of Zaidín, Granada. have a positive effect on plant growth directly and/or through the improvement in soil structure, cation exchange capacity, microbiological activity and for complexing cer- Table 2 Chemical characteristics of the KOH-soluble extract of dry tain soil ions. However, there are no data on the effects of olive residue this organic fraction extracted from DOR on colonization of Ash (%) 30.4 roots by AM fungi or on soil properties in revegetation pH 9.83 programmes. Our hypothesis was that the combined actions EC (mS cm−1) 9.78 of this liquid organic amendment and mycorrhiza on the Organic matter (%) 69.6 growth of Mediterranean shrub species could be higher than Extractable C (g l−1) 8.6 the sum of individual effects. Fulvic acid C (g l−1) 2.1 The objectives of this study were (1) to assess the inter- Humic acid C (g l−1) 6.5 actions between the inoculation with three AM fungi and Water-soluble carbohydrates (g l−1) 1.03 the addition of a liquid organic amendment obtained by Phenols (g l−1) 1.58 alkaline extraction of composted DOR, with respect to their Total N (mg l−1) 320 effects on the growth of R. sphaerocarpa seedlings in a Na (mg l−1) 186 degraded semi-arid Mediterranean soil, and (2) to establish K (mg l−1) 1,776 the optimum levels of amendment addition, thereby avoid- P (mg l−1) 62 ing possible negative effects on plant growth, AM coloni- Ca (mg l−1) 136 zation and soil properties considered to be indicators of soil Mg (mg l−1) 28.9 quality such as labile C fractions (microbial biomass C and Fe (mg l−1) 3.4 water-soluble C), enzyme activities (dehydrogenase, ure- Cu (mg l−1) 0.2 ase, protease-BAA, and β-glucosidase) and soil aggregate Mn (mg l−1) 0.3 stability. Zn (mg l−1) 1.2
  • 3. 32 14.0bcd 17.2defg 16.9cdefg 17.7efg The AM fungal inoculum consisted of a mixture of rhi- 310abcd 300abcd 324abcde 322abcde 354cde 248cde 8.47ab zosphere soil from trap cultures (Sorghum sp.) containing Table 3 Soil physical–chemical properties of R. sphaerocarpa after 1 year of growth in response to mycorrhizal inoculation treatments and KOH extract of DOR addition (n=4) spores, hyphae and mycorrhizal root fragments. Once 3 germinated, seedlings were transplanted into the growth substrate consisting of peat and cocopeat (1:1, v/v). The 254cde 8.43ab corresponding AM inoculum was applied at a rate of 5% (v/v). The same amount of an autoclaved mixture of the 2 inocula was added to control plants, supplemented with a filtrate (Whatman No. 1 paper) of the pot culture of all 8.40ab 283e three AM fungi to provide the microbial populations 1 accompanying the mycorrhizal fungi. Inoculated and non- G. mosseae inoculated seedlings were grown for 8 months under nurs- 209bcd 270de ery conditions without any chemical fertiliser treatment. 8.39a 0 18.5fg 17.0cdefg 19.2g Experimental design and layout 8.34a 3 The experiment was a mesocosm assay, conducted as a completely randomized factorial design with two factors. 200bc 225cde 249cde 347bcde 357de 290ab The first factor had four levels: without and with the 8.47ab 8.46ab 8.34a addition of low, medium or high doses of the liquid 2 amendment to the soil. The second factor had four levels: non-inoculation and inoculation of R. sphaerocarpa plants G. deserticola with one of three AM fungi (G. intraradices, G. deserticola 1 or G. mosseae) in the nursery. Four replicates per treatment 13.7bcd 14.6bcde 15.0bcdef 11.0a were carried out, making a total of 64 pots. Two kilograms of substrate, consisting of soil and ver- 0, 1, 2 or 3 indicates 0, 5.8, 11.7 or 35.1 ml amendment kg−1 soil/vermiculite mixture, respectively 0 miculite at a ratio of 3:1 (v/v), were placed in 3.6-l pots. In March 2003, R. sphaerocarpa seedlings (inoculated and 240cde 8.48ab non-inoculated) were transplanted to the pots (one per pot). 303abcd 315abcde 320abcde 374e Two weeks after planting, the amendment was applied to 3 the pots at a rate of 0, 5.8, 11.7 or 35.1 ml kg−1 soil/vermiculite Values in rows followed by the same letter are not significantly different (LSD, p<0.05) mixture, which corresponds to the addition of 0, 50, 100 or 8.44ab 300 mg C liquid amendment kg−1 soil. The experiment was 213bcd 228cde 184a carried out in the nursery of the University of Murcia (Murcia, 2 Spain) without the addition of chemical fertiliser. The plants were well watered and kept outdoors under ambient irradi- G. intraradices 8.31a ance, temperature and air humidity. One year after planting, 1 the plants were harvested and rhizosphere soil samples of the pots were taken. Rhizosphere soil samples, air-dried to 20% 13.5bc 13.1b 14.8bcde 10.8a 8.34a moisture content and sieved to less than 2 mm, were divided 0 into two subsamples. One subsample was stored at 2°C for microbiological analysis, and another subsample was allowed to dry at room temperature for physical–chemical analysis. 8.58b 8.60b 310abcd 287ab 294abc 278a 208bcd 188ab 174a 3 Plant analyses 2 Basal stem diameters and heights of plants were measured 8.58b with callipers and rulers. Fresh and dry (105°C, 5 h) masses No mycorrhiza of shoots and roots were recorded. Plant tissues were 1 ground before chemical analysis. Plant P was determined DOR Dry olive residue 10.6a colorimetrically according to Murphy and Riley (1962) 8.56b Water-soluble 183a after digestion in nitric–perchloric acid (5:3) for 6 h at a 0 210°C. Plant N was determined by combustion at 1,020°C stability (%) C (μg g−1) in a carbon and nitrogen analyser and reduction, separation Aggregate pH (H2O) μs cm−1) EC (1:5, of N2 in a chromatographic column and measurement in a thermic conductivity detector. Plant K was estimated by flame photometry (Schollemberger and Simon 1954). a
  • 4. 33 The percentage of root length colonized by AM fungi was passed through the same 0.250-mm sieve with the assis- calculated by the gridline intersect method (Giovannetti and tance of a small stick to break the remaining aggregates. Mosse 1980) after staining with trypan blue (Phillips and The residue remaining on the sieve, which was made up of Hayman 1970). plant debris and sand particles, was dried at 105°C and weighed (P2). The percentage of stable aggregates with regard to the total aggregates was calculated by the Soil analyses following relationship (P1−P2)×100/(4−P2+T). Soil pH and electrical conductivity were measured in a 1:5 (w/v) aqueous solution. In soil aqueous extracts (1:5), Statistical analysis water-soluble C was determined with an automatic carbon analyser for liquid samples (Shimadzu TOC-5050A). Data were log-transformed to achieve for normality. Microbial biomass C was determined by the fumigation– Amendment addition, mycorrhizal inoculation and their extraction method (Vance et al. 1987). Ten grams of soil at interaction effects on measured variables were tested by a 60% of field capacity was fumigated in a 125-ml Erlenmeyer two-way analysis of variance, and comparisons among flask with purified CHCl3 for 24 h. After removal of means were made using the least significant difference residual CHCl3, 40 ml of 0.5 M K2SO4 solution was added (LSD) test calculated at p<0.05. Statistical procedures were and the sample was shaken for 1 h before filtration of the carried out with the software package SPSS 10.0 for mixture. The K2SO4-extracted C was measured as indi- Windows. cated for water-soluble C. Microbial biomass C was cal- culated as the difference between the C of fumigated and non-fumigated samples divided by the calibration factor Results KEC=0.38. Dehydrogenase activity was determined according to Soil parameters Trevors et al. (1982). For this, 1 g of soil at 60% of field capacity was exposed to 0.2 ml of 0.4% 2-p-iodophenyl-3-p- Only the mycorrhizal treatments with G. intraradices and nitrophenyl-5-phenyltetrazolium chloride (INT) in distilled G. mosseae significantly decreased soil pH (Tables 3 and water for 20 h at 22°C in the dark. The iodonitrotetrazolium 4). However, neither amendment addition nor the interac- formazan (INTF) formed was extracted with 10 ml of tion of amendment × mycorrhizal inoculation had any sig- methanol by shaking vigorously for 1 min and filtering nificant effect on soil pH and electrical conductivity through Whatman No. 5 filter paper. INTF was measured (Table 4). spectrophotometrically at 490 nm. Urease and N-α-benzoyl-L-argininamide (BAA) hydro- lysing activities were determined in 0.1 M phosphate buffer at pH 7; 1 M urea (Tabatabai and Bremner 1972) and Table 4 Two-factor ANOVA (mycorrhizal inoculation treatments 0.03 M BAA (Ladd and Butler 1972) were used as and amendment addition) for all parameters studied in the substrates, respectively. Two millilitres of buffer and 0.5 ml rhizosphere soil of R. sphaerocarpa seedlings 1 year after planting of substrate were added to 0.5 g of sample, which was (P significance values) incubated at 30°C (for urease) or 39°C (for protease) for Amendment Mycorrhiza Interaction þ 90 min. Both activities were determined as the NH4 re- (A) (M) (A×M) leased in the hydrolysis reaction. β-Glucosidase was determined using p-nitrophenyl-β-D- pH 0.700 <0.001 0.814 glucopyranoside (PNG, 0.05 M) as substrate. This assay is Electrical 0.669 0.079 0.169 based on the release and detection of p-nitrophenol (PNP). conductivity Two millilitres of 0.1 M maleate buffer (pH 6.5) and 0.5 ml Water-soluble C 0.615 0.003 0.987 of substrate were added to 0.5 g of sample and incubated at Aggregate stability <0.001 0.014 0.362 37°C for 90 min. The reaction was stopped with tris(hydro Microbial biomass C <0.001 0.587 0.806 xymethyl)aminomethane (THAM) according to Tabatabai Dehydrogenase 0.002 0.026 0.685 (1982). The amount of PNP was determined by spec- Urease <0.001 <0.001 0.001 trophotometry at 398 nm (Tabatabai and Bremner 1969). Protease 0.643 <0.001 0.807 The percentage of stable aggregates was determined by β-Glucosidase 0.818 0.293 0.384 the method described by Lax et al. (1994). Sieved (0.2– Shoot 0.037 0.001 0.211 4 mm) soil (4 g) was placed on a small, 0.250-mm sieve Root 0.604 0.353 0.163 and wetted by spray. After 15 min the soil was subjected to N foliar 0.006 <0.001 0.018 an artificial rainfall of 150 ml with energy of 270 J m−2. P foliar 0.002 <0.001 0.003 The remaining soil on the sieve was placed in a previously K foliar 0.319 0.001 0.028 weighed capsule (T), dried at 105°C and weighed (P1). Colonization 0.861 <0.001 0.547 Then the soil was soaked in distilled water and, after 2 h,
  • 5. 34 Table 5 Soil microbial biomass C and enzyme activities of R. sphaerocarpa after 1 year of growth in response to mycorrhizal inoculation treatments and KOH extract of DOR addition (n=4) Water-soluble C concentrations were increased only 0.27abc 1.15ef 0.61d with the mycorrhizal inoculation treatments (Tables 3 and 53.4f 42ab 3 4), the greatest increases being observed in the inoculation treatment with G. mosseae (on average, about 40% greater 42.4de 1.15ef 0.69d 0.32c 46ab than in the soil of non-inoculated plants). Both amendment addition and inoculation with G. mos 2 seae significantly increased soil aggregate stability, reach- 0.29abc 30.2ab 0.19ab ing similar values at the end of the growth period (Tables 3 1.50g 73bc and 4). In the amended soils, the percentage of stable 1 G. mosseae aggregates did not vary with the dose of the amendment 0.28abc added. The highest aggregate stability was found in the 34.8bc 0.19ab 1.29fg 301e amended soil of plants inoculated with G. deserticola or G. 0 mosseae. The addition of the amendment decreased soil microbial 0.26abc 43.8de 0.56cd 0.57b biomass C for both non-inoculated and inoculated plants, 81c particularly for the plants inoculated with G. mosseae or 3 G. intraradices (Table 5). In general, microbial biomass C 46.0de 0.69bc decreased as the dose of amendment increased. Microbial 0.83e 0.31c 180d biomass C was not affected by the mycorrhizal inocula- 2 tion treatments (Table 4). With the exception of G. desert 0.27abc icola, the mycorrhizal inoculation alone produced sig- 31.3ab 0.75bc 0.24b 149d G. deserticola nificantly higher dehydrogenase and benzoyl arginina- 1 mide hydrolysing activities than the control soil (Table 5). In general, neither amendment addition nor mycorrhizal 0.25abc 29.8ab 0.14ab 0.46a inoculation modified β-glucosidase activity. The medium 288e and high dose of amendment significantly increased dehy- 0 drogenase and urease activities. Only urease activity 0.84cd 0.22ab 0, 1, 2 or 3 indicates 0, 5.8, 11.7 or 35.1 ml amendment kg−1 soil/vermiculite mixture, respectively 0.66d 47.5e increased proportionally with the increase in the amend- 35a ment dose. The interaction amendment × mycorrhizal 3 inoculation had no significant effect on the biochemical 40.9cd 0.56cd 0.68bc 0.29bc properties (Table 4). Values in rows followed by the same letter are not significantly different (LSD, p<0.05) 86c 2 30.0ab 0.16ab 0.96de 0.21a 167d G. intraradices 1 Table 6 Growth parameters, foliar nutrient content and root 0.25abc 34.8bc 0.14ab 0.95de infection of R. sphaerocarpa in response to mycorrhizal inoculation 296e treatments and KOH extract of DOR addition previous to planting (n=4) 0 0.25abc No G. G. G. 40.7cd 0.56cd 0.53ab mycorrhiza intraradices deserticola mosseae 23a 3 Shoot 0.5a 0.7a 0.7a 0.5a 40.6cd 0.48ab 0.23ab 0.43c 70bc (g dry wt. plant−1) 2 Root 0.6ab 0.8b 0.7ab 0.5a 0.24abc 0.19ab 0.54ab (g dry wt. 26.0a 177d No mycorrhiza plant−1) 1 Nitrogen 8a 13b 10ab 9a 0.26abc (mg plant−1) 26.1a 0.05a 0.44a 281e Phosphorus 0.6a 0.8ab 1.2b 1.0ab 0a (mg plant−1) DOR Dry olive residue (μmol PNP g−1 h−1) (μmol NH3 g−1 h−1) Potassium 7a 9a 9a 8a (μg INTF g−1 soil) (mg plant−1) Microbial biomass Dehydrogenase β-Glucosidase Colonization (%) 0.4a 61.9b 67.7b 51.8b Protease-BAA NH3 g−1 h−1) Urease (μmol C (μg g−1) Values in rows followed by the same letter are not significantly different (LSD, p<0.05) a 0, 1, 2 or 3 indicates 0, 5.8, 11.7 or 35.1 ml amendment kg−1 soil/ vermiculite mixture, respectively a