Mycorrhizal inoculum potential of soils from alley cropping plots in Sénégal

Forest Ecology and Management 146 (2001) 35±43

Mycorrhizal inoculum potential of soils from alley cropping plots in SeÂneÂgal O. Diagnea,*, K. Inglebyb,1, J.D. Deansb1, D.K. Lindleyc, I. DiaiteÂd, M. Neyrae a Institut SeÂneÂgalais de Recherches Agricoles, B.P. 2312, Dakar, SeÂneÂgal Institute of Terrestrial Ecology, Bush Estate, Penicuik, Midlothian, EH26 0QB, UK c Institute of Terrestrial Ecology, Merlewood Research Station, Grange-over-Sands, Cumbria, LA11 6JU, UK d Institut SeÂneÂgalais de Recherches Agricoles, B.P. 53, Bambey, SeÂneÂgal e Laboratoire de Microbiologie des Sols Tropicaux, IRD, B.P. 1386, Dakar, SeÂneÂgal b

Received 13 September 1999; received in revised form 22 March 2000; accepted 24 March 2000

Abstract Intact soil cores were sampled from around three leguminous tree species (Acacia nilotica, Acacia tortilis and Prosopis juli¯ora) in 10-year-old alley-cropping plots at ThieÂnaba, SeÂneÂgal. Cores were removed from two depths (0±25 and 25±50 cm) and at two distances from the trunk (1 and 5 m). Duplicate soil cores were taken for assessment of root concentration (cm/ 100 cm3 soil), mycorrhizal infection (% of infected root length) and spore concentration in the soils. In order to determine the mycorrhizal inoculum potential (MIP) of the soils, a mycorrhizal bioassay of the soil cores was conducted in the greenhouse using millet seedlings. For all plots, seedlings grown in soils from the surface layer (0±25 cm) were larger and formed higher levels of infection than those grown in soils from 25 to 50 cm depth. Mycorrhizal infection of the seedlings was greatest in soil from the A. tortilis plots and, unlike the other tree species, also the greatest in soil collected near the tree. Positive relationships were found between the growth and infection of the bioassay seedlings and the root and spore concentrations in the ®eld soils. Seedling growth and infection may also have been related to higher levels of carbon in the ®eld soils. The results indicated that root and spore concentrations in the ®eld soils were good indicators of MIP, but that levels of root infection were not. The results also indicated the potential bene®t to crop yield of maintaining high levels of mycorrhizal propagules in alley-cropping soils and a possible role of the trees in maintaining these sources of inoculum. # 2001 Elsevier Science B.V. All rights reserved. Keywords: Mycorrhizal bioassay; Alley cropping; Agroforestry; Acacia nilotica; A. tortilis; Prosopis juli¯ora

1. Introduction

*

Corresponding author. Tel.: ‡221-832-32-19/832-16-38; fax: ‡221-832-96-17. E-mail address: [email protected] (O. Diagne). 1 Institute of Terrestrial Ecology, Bush Estate, Penicuik, is a component of The Edinburgh Centre for Tropical Forests.

In many semi-arid areas of Africa, like the Sahel, expanding agricultural activities and intensive cropping are leading to over exploitation of soil nutrients, increasing soil erosion and a decline in overall land productivity (Van Keulen and Breman, 1990). In these areas, fast-growing multipurpose tree species

0378-1127/01/$ ± see front matter # 2001 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 0 0 ) 0 0 4 4 4 - 8

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O. Diagne et al. / Forest Ecology and Management 146 (2001) 35±43

especially leguminous species are widely recommended for use in agroforestry systems in conjunction with agricultural crops. The trees stabilize and ameliorate soils while providing fuelwood, poles and other timber products of direct bene®t to rural populations (Kang and Wilson, 1987). Most of these plant species require symbiotic associations with arbuscular mycorrhizal (AM) fungi for the ef®cient uptake of nutrients and water from the soil and the maintenance of growth (Le Tacon et al., 1987). AM fungi predominate in dry tropical soils, associate with a wide range of host species and can confer substantial growth bene®ts to both tree species (Wilson et al., 1991; Michelson, 1993) and crop species (Howeler et al., 1987; Sieverding, 1991). In agroforestry systems, tree root mycorrhizas may therefore be of additional bene®t by maintaining active mycorrhizal propagules in the soil which can rapidly colonize developing crop root systems. However, little is known of the dynamics of AM fungal populations in agroforestry systems or the relative importance of the different fungal propagules in the soil (Haselwandter and Bowen, 1996). Propagules of AM fungi in the soil normally take the form of spores, root fragments or hyphal networks. The capacity of these fungal propagules to form mycorrhizal associations is known as the mycorrhizal inoculum potential (MIP) of that soil (Brundrett and Abbott, 1995). Currently, the best method of determining the MIP of different soils is by growing nonmycorrhizal bioassay plants in intact soil cores and comparing levels of infection after a short period of growth (Brundrett, 1991). The objective of this study was to examine the effect of different tree species on the numbers of active mycorrhizal propagules present in alley-cropping soils. To do this, root, mycorrhizal and spore distributions occurring in alley-cropping plots of three fastgrowing, multipurpose tree species A. nilotica, A. tortilis and P. juli¯ora, were determined and then related to differences in the MIP of the soils as determined by a bioassay experiment. Because the bioassay plant species selected was a crop species widely used in local agroforestry, the study also directly examined the potential for improving crop yields through early mycorrhizal infection. This work formed part of a wider study of the above- and belowground growth and nutrient/water use ef®ciencies of

such species, in order to identify which were most appropriate for use in the Sahel. 2. Materials and methods 2.1. Site The study site was at the Institut SeÂneÂgalais de Recherches Agricoles (ISRA) experimental research station at ThieÂnaba, SeÂneÂgal (148480 N, 168500 W). Individual plots of ®ve tree species were planted in 1985, with each plot replicated within four blocks. Each plot consisted of 36 trees arranged in three rows with 2.5-m spacing within rows and 10 m between rows. In 1994, the plots had been cropped with peanut (Arachis hypogaea L.) but had remained fallow until sampling in December 1995. The climate at ThieÂnaba is typical of semi-arid regions of West Africa with mean monthly temperatures ranging between 26±308C and an annual precipitation of 600±700 mm, which occurs mostly during a single rainy season (June±October). In recent years, annual precipitation has been less than average (400±500 mm). In the year of planting the total rainfall was 385 mm. On a global scale, the soil is sandy (>90% of soil) and representative of a Dior-type tropical ferruginous soil (Al®sol) which is very common in the Northern Peanut Basin of SeÂneÂgal. 2.2. Tree species Tree species and provenances examined were: Acacia nilotica ssp. adstringens (Schum.), ISRA 84/1146 ex. SeÂneÂgal; Acacia tortilis (Forsk.) Hayne, ssp. raddiana (Savi) Brenan ISRA 84/1073 ex. SeÂneÂgal; and Prosopis juli¯ora (Swartz) D.C., ISRA 84/1147 ex.SeÂneÂgal. 2.3. Soil sampling and set-up of bioassay test Samples were taken in December 1995, during the dry season and 10 years after establishment of the plots. Plots of each tree species were selected from three of the four blocks on the basis of uniformity of site topography, aboveground growth and optimal survival. Trees with a DBH measurement similar to the mean for that plot were selected for sampling

O. Diagne et al. / Forest Ecology and Management 146 (2001) 35±43

from the central row, avoiding trees at the ends of the row. In each plot, two transects were established on opposite sides of the same tree. Sampling points were located on the transects at 1 and 5 m (midpoint between the rows) from the tree. Intact soil cores (150 cm3 in volume) were then carefully removed at 0±25 and 25±50 cm depths using a 5-cm diameter corer with a removable inner tube. A second core was taken at each sample point for determination of root concentration, mycorrhizal infection and spore concentration. The cores were immediately transferred to tightly ®tting polythene bags and sealed to protect their structural integrity and prevent drying out. For transportation, the cores were packed into boxes to prevent further disturbance and stored under cool, shaded conditions at all times. The following day the cores were placed in 250-cm3 plant pots, packed with sterilized grit to provide further support and laid out in randomized blocks in the greenhouse. The randomized block design used in the ®eld was also used for the bioassay experiment, with each treatment randomized within three blocks and the two transects randomized in a split plot design within each block. Each core was sown with ®ve millet (Pennisetum americanum (L.) Leeke) seeds and covered with a layer of sterilized grit to prevent transfer of soil between pots during watering. Watering was done daily with 20 ml of distilled water in each pot. After one week, germinating seedlings were thinned to leave one seedling (of similar size) in each pot. 2.4. Assessments Assessments of root concentration (cm root length per 100 cm3 soil), mycorrhizal infection (% of infected root length) and spore concentration (number per 100 g dry wt. of soil) in the ®eld soils were made closely following methods detailed in a previous, related study (Ingleby et al., 1997). Logistical problems resulted in the ®eld samples being stored for a period of 2±3 months before assessment, after which time deterioration of the roots made it dif®cult to distinguish tree roots from those of non-woody species. Assessments were, therefore, made of total (tree and fallow) root length in the samples using the gridline intersect method (Tennant, 1975). Fine roots

37

(<2 mm) were stained for mycorrhizal assessment according to Koske and Gemma (1989). After staining, roots were cut into 1 cm fragments and 20 fragments were removed at random from each sample and observed under a compound microscope. Mycorrhizal infection was assessed according to the methods of Allen and Allen (1980) and McGonigle et al. (1990). AM spores were extracted from 100 g samples following the methods of Walker et al. (1982). Chemical analysis was conducted on one replicate set (Block 3) of soils from the 12 treatments (3 tree species2 distances2 depths). Total carbon (K2Cr2O7 in H2SO4), nitrogen (Kjeldahl), potassium and phosphorus (HNO3‡HCl) were determined. Bioassay seedlings were harvested 40 days after sowing and measurements were made of shoot dry weight, root fresh weight and mycorrhizal infection. Mycorrhizal infection was determined on the whole of the ®ne roots which meant that only measurement of root fresh weight, and not root dry weight, was possible. Root staining and mycorrhizal assessment followed the same methods used for the ®eld samples. 2.5. Statistical analysis Data were examined by analysis of variance (ANOVA) using tree species, distance and depth as treatment factors and block/transect number as block structures. Before analysis, arcsine and log (n‡1) transformations were performed on mycorrhizal infection percentages and spore numbers, respectively, and the Bartlett test (Sokal and Rohlf, 1995) was used to ensure that sample variances were homogenous. Means were compared using Fisher's LSD test when the F-test from ANOVA was signi®cant at p<0.05. Correlation coef®cients were determined to examine relationships between parameters. 3. Results 3.1. Field samples Root concentrations were less in the P. juli¯ora plots than in the A. tortilis and A. nilotica plots (Table 1a). Levels of mycorrhizal infection also differed between tree species with roots in the P. juli¯ora plots having higher levels than those in the A. tortilis

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O. Diagne et al. / Forest Ecology and Management 146 (2001) 35±43

Table 1 Effect of tree species on (a) root concentration, mycorrhizal infection and spore concentration found in alley-cropping soils at ThieÂnaba, SeÂneÂgal, and (b) growth and mycorrhizal infection of millet seedlings grown in similar soils Tree species A. nilotica

A. tortilis

P. juliflora

P value

(a) Field samples Root concentration (cm/100 cm3) Root infection (%) Spore concentration (No./100 g soil)

181 aa 42.2 b 164

184 a 45.9 b 167

142 b 66.2 a 187

<0.018 <0.001 0.786

(b) Bioassay plants Shoot dry wt. (mg) Root fresh wt. (mg) Root infection (%)

36.1 442 12.6 b

39.0 478 17.9 a

34.9 388 11.0 b

0.719 0.334 <0.001

a

Letters indicate significant differences within each row at p<0.05 as determined by ANOVA and Fisher's LSD test.

and A. nilotica plots. Spore concentrations did not differ between tree species plots. Root and spore concentrations decreased with depth in all plots (Table 2a), but not with distance from the tree. Levels of mycorrhizal infection were not affected by soil depth or by distance from the tree. Differences in soil nutrients were associated with tree species and soil depth, not distance from the tree (Table 3). Amounts of nitrogen and potassium were greatest in the A. nilotica plot and least in the P. juli¯ora plot, with the trend being reversed for phosphorus which was greatest in the P. juli¯ora plot. Amounts of phosphorus and carbon tended to decrease with depth, whereas nitrogen and potassium concentrations were unaffected by depth. Positive correlations (p<0.001) were found between spore concentration and root concentration for all

three tree species, but neither root nor spore concentration were related to root infection. None of the soil nutrients were signi®cantly correlated with root concentration, spore concentration or root infection. 3.2. Bioassay experiment Millet growth did not differ signi®cantly between sample plots unlike the root infection. However, differences were observed in seedling growth in relation to depth and distance. Seedlings grown in cores from the surface layer (0±25 cm depth) had larger shoot dry weight, root fresh weight and higher levels of mycorrhizal infection than those grown in cores from the 25±50 cm depth (Table 2b). Overall levels of mycorrhizal infection were signi®cantly higher on seedlings grown in cores from the A. tortilis plots than the other

Table 2 Effect of soil depth on (a) root concentration, mycorrhizal infection and spore concentration found in alley-cropping soils at ThieÂnaba, SeÂneÂgal, and (b) growth and mycorrhizal infection of millet seedlings grown in similar soils Soil depth 0±25 cm

25±50 cm

P value

(a) Field samples Root concentration (cm/100 cm3) Root infection (%) Spore concentration (No./100 g soil)

236 aa 50.0 279 a

102 b 52.4 66 b

<0.001 0.598 <0.001

(b) Bioassay plants Shoot dry wt. (mg) Root fresh wt. (mg) Root infection (%)

48.2 a 561 a 17.6 a

25.1 b 311 b 10.1 b

<0.001 <0.001 <0.001

a

Letters indicate significant differences within each row at p<0.05 as determined by ANOVA and Fisher's LSD test.

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Table 3 Chemical analysis of soils sampled under three tree species and at two depths in alley-cropping plots at ThieÂnaba, SeÂneÂgal A. nilotica

Carbon (g/kg) Potassium (mg/kg) Nitrogen (g/kg) Phosphorus (mg/kg)

A. tortilis

P. juliflora

0±25 cm

25±50 cm

0±25 cm

25±50 cm

0±25 cm

25±50 cm

1.08 156 0.15 34.0

0.79 171 0.15 22.0

1.14 161 0.14 35.5

0.81 117 0.12 28.5

1.00 102 0.10 42.5

1.02 97.5 0.11 29.5

tree species (Table 1b). Levels of infection also differed according to distance from the tree. Although an overall effect of distance on seedling infection was found, a tree speciesdistance interaction (p<0.001) indicated that this was due entirely to high levels of infection on seedlings grown in cores from nearest the tree in the A. tortilis plots (Fig. 1). Although levels of infection on the seedlings were generally low (5±32%), overall positive correlations were found between mycorrhizal infection and both shoot dry weight (p<0.001) and root fresh weight (p<0.001). When the tree species were considered separately, these relationships were present in the A. tortilis (shoot dry wt., p<0.05; root fresh wt., p<0.05)

and A. nilotica plots (root fresh wt., p<0.05), but absent in the P. juli¯ora plot. 3.3. Relationships between field and bioassay parameters Better growth and infection of the bioassay plants was positively correlated with root and spore concentrations in the ®eld soils, but not to root infection (Table 4). When the tree species were considered separately, these relationships were present in the A. tortilis (root concentration, p<0.05; spore concentration, p<0.05) and A. nilotica plots (root concentration, p<0.05) but absent in the P. juli¯ora plot. Levels of

Fig. 1. Mycorrhizal infection of millet seedlings grown in soil cores collected under three tree species, at two soil depths and two distances from the tree in alley-cropping plots at ThieÂnaba, SeÂneÂgal (Bars indicate ‡S.E.).

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O. Diagne et al. / Forest Ecology and Management 146 (2001) 35±43

Table 4 Correlations (r) between root concentration, mycorrhizal infection, AM spore concentration and soil nutrients found in soils from ThieÂnaba, SeÂneÂgal and the growth and infection of bioassay seedlings grown in similar soils (for root concentration, mycorrhizal infection and spore concentration, nˆ72; for soil nutrients, nˆ12) Bioassay seedlings Shoot dry wt. (mg) Root concentration (cm/100 cm3) Mycorrhizal infection (%) Spore concentration (no/100 g soil) Carbon (g/kg) Potassium (mg/kg) Nitrogen (g/kg) Phosphorus (mg/kg) *

0.488*** 0.116 0.328** 0.748** 0.120 0.247 0.606*

Root fresh wt. (mg) 0.514*** 0.156 0.316** 0.857*** 0.276 0.097 0.479

Infection (%) 0.342** 0.043 0.299* 0.603* 0.080 0.087 0.195

Significant at *, p<0.05; **, p<0.01 and *** p<0.001, respectively.

carbon in the soils were also positively correlated with the growth and infection of the bioassay plants and phosphorus was correlated with shoot dry weight (Table 4). 4. Discussion The effect of tree root distribution on the MIP of the soils cannot be directly assessed from this study and the probable distribution of tree roots in these plots can only be inferred from other studies on similar-aged plots which indicate that tree root concentration decreases with depth and with distance from the tree (Rao and Roger, 1990; Ruhigwa et al., 1992; Hauser, 1993). However, it can be noted that fewer roots were found in the P. juli¯ora plots which tends to support the results of Cazet (1989) who studied tree root distributions on the same plots when the trees were 30 months old. It is also interesting to note that Ingleby et al. (1997) reported lower root concentrations and higher levels of infection on roots of P. juli¯ora than for A. tortilis and A. nilotica in plots at Bandia, SeÂneÂgal, and that a similar result was obtained here even though `mixed' root samples were assessed. Overall levels of mycorrhizal infection in the ®eld samples were high and similar to those found on roots of the same tree species at Bandia, SeÂneÂgal (Ingleby et al., 1997). Although soils at ThieÂnaba were sandier than soils at Bandia and subject to erosion and to cropping activities, the results indicated that the soil conditions and cropping practices did not affect the

level of mycorrhizal infection as found by Abbott and Robson (1991a,b). Because no differences in mycorrhizal infection were found with distance from the tree and the proportion of tree to fallow roots would be expected to decrease considerably with distance from the tree, it appears that tree and fallow roots had similar levels of infection. Mycorrhizal infection did not vary with soil depth, but differences might have been detected had depths greater than 50 cm been examined, as mycorrhizal infection is thought to decrease with depth (Abbott and Robson, 1991a,b). In contrast to results on mycorrhizal infection, spore concentrations were very different (at least 5 times greater) from those found at Bandia (Ingleby et al., 1997). The effect of previous crops and the present fallows probably contributed to the increased spore numbers at ThieÂnaba. However, numbers of AM spores recovered from the ®eld soils were low compared to other studies of spore populations in alleycropping soils (Sieverding, 1991). Sieverding (1991) also reported a 10-fold reduction in spore numbers after a one-year grass fallow. Most spores were found in the surface layer (0±25 cm), which supports the widely held view that spore production is concentrated near the soil surface (Abbott and Robson, 1991a,b; Ingleby et al., 1997). As spore concentrations did not vary with distance from the tree it could be assumed that both tree and fallow mycorrhizas were responsible for similar inputs of spores. The main objective of the bioassay experiment was to compare the numbers of propagules initially present in the soils by measuring primary mycorrhizal

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infection on the millet seedlings. This required a short growing period and, as a result, overall levels of infection on the millet seedlings were low compared to other ®ndings (Plenchette et al., 1989). In addition, the experiment was undertaken in December±January when low temperatures (16±208C) may have slowed the growth and root infection of the millet seedlings. The importance of hyphal networks for rapid AM colonisation is well recognized (Read, 1992), and the severance of roots and hyphal networks during removal of the soil cores may also have reduced levels of infection, although great care was taken to minimize soil disturbance after removal of soil cores. Even though levels of infection were low, growth bene®ts of mycorrhizal infection were recorded and indicated the potential bene®t to crop yield of maintaining high numbers of mycorrhizal propagules in alley-cropping soils to ensure rapid infection. The importance to crop yield of maintaining AM spore populations in agricultural soils is widely recognized (Bethlenfalvay, 1992); indeed, Thompson et al. (1990) found that reductions in AM spore numbers were the cause of long-fallow disorder, which could be alleviated by the introduction of mycorrhizal-dependent crops to restore spore populations. Studies by Veenendaal et al. (1992) and Brundrett et al. (1996) have demonstrated that active fungal propagules (as determined by a plant bioassay) are concentrated in the surface horizon and this study supports those results. Only depths to 50 cm were examined, as potential mycorrhizal bene®ts in alleycropping soils are likely to depend on the early infection of crop roots, which are concentrated near the soil surface. Brundrett et al. (1996) also found that prolonged dry soil conditions did not affect MIP of soils from tropical regions of Australia, so it is not surprising that the drier soil conditions found at ThieÂnaba and under trees in alley-cropping plots (ICRAF, 1993) were not detrimental to MIP. Unlike root concentration and root infection, spore concentration was not different between Acacia and Prosopis species. This shows that spore concentration is not related to tree genera or tree species, but more likely to annual crops since all the plots studied had been planted with the same crops. In a previous study, Ingleby et al. (1997) attributed differences on spore concentration between tree species to differences on ground vegetation under these trees. The spore con-

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centrations found in this study are low compared to some results found in Savanna (Cuenca and Lovera, 1992), but are more than the average of spore number found in Poland under 20 plants species (Blaszkowski, 1994). The high MIP of soils from the A. tortilis plots cannot be explained by the root concentration, percentage of root infection or spore concentration. We hypothesize, therefore, that the AM fungi present in ThieÂnaba were more effective on A. tortilis than on the other tree species. However, further in-depth studies are needed to examine the species composition of AM fungi in these soils and to compare the effectiveness of different fungi isolated from these soils in promoting plant growth. Although both root and spore concentrations were correlated with growth and mycorrhizal infection of the bioassay plants, the high root concentration and low infection of bioassay plants in soil from the A. nilotica plots suggests that spore concentration provides the most reliable (and rapid) indication of MIP when the soil in question is subject to periodic disturbance through cultivation. Levels of mycorrhizal infection showed little promise as indicators of MIP under these circumstances. In other ecosystems where soil disturbance is minimal, infection via mycorrhizal roots and hyphal networks is likely to be more signi®cant (Jasper et al., 1989). MIP was also positively related to soil carbon content and Brundrett et al. (1996) found a positive relation between organic carbon and MIP in bioassays of soil from tropical regions of Australia. Mycorrhizas are traditionally seen as an aid to establishment and survival of nursery plants following outplanting, and applied studies frequently focus on selection, nursery inoculation and plant/fungus performance. This study indicates the potential bene®t to crop yield of maintaining high levels of mycorrhizal propagules in alley-cropping soils and a possible role of the trees in maintaining these sources of inoculum. Thus, in the rehabilitation programmes of degraded lands, it is worth introducing plants that are able to associate rapidly with AM fungi and help restore the equilibrium within the soil/plant ecosystem. Belowground processes are an important, yet frequently undervalued, factor in the success of agroforestry systems and the adoption of management practices which improve or sustain tree mycorrhizas and the levels of propagules in the soil should be encouraged.

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O. Diagne et al. / Forest Ecology and Management 146 (2001) 35±43

Acknowledgements We wish to thank B. Ngom, I. Camara and A. Sarr for technical support and Mr R. Smith for statistical advice. This work was partly funded under CEE contract No. TSH-CT93-0232. Soil and root material were imported to the UK under DAFS licence number IMP/SCE/REA/27/1994 issued under the Plant Health (Great Britain) Order 1993.

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