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Dipartimento di Biologia Vegetale, Università "La Sapienza", Piazzale Aldo Moro 5, 00185 Roma, Italy
Miguel A. Casado
Francisco D. Pineda
Departamento Interuniversitario de Ecología, Facultad de Biología, Universidad Complutense de Madrid, 28040 Madrid, Spain
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ABSTRACT |
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The fungal communities of grassland soils in Spain from four sites at different elevations were studied. Each site contained grazed and fenced ungrazed plots. These plots were situated in two slope positions (upper and lower zones). The ungrazed plots, fenced off 6 y before the sampling, were part of a study of global change that simulates conditions of rural abandonment, which is widespread in Iberian countries, since Spain joined the European Union. We analyzed the structure of the soil fungi communities and its relationship with herbaceous vegetation. The distribution of 207 taxa of fungi revealed that the elevation was the main factor of fungal variability; the effect of grazing and slope position were associated with less variability. Although a halt in grazing resulted in the accumulation of standing plants and plant litter in these ecosystems, it had relatively little effect on soil microfungi and appeared to be related mainly to growing conditions affected by that accumulation.
Key words: Elevation, fungal communities, herbivory, soil fungi, Spain
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Huenneke and Mooney 1989, Godron 1989, Mc Neill 1992). These ecosystems are subjected to the stresses of winter cold and summer drought, with peaks of primary production in fall and spring.
In many areas of the Mediterranean basin, especially in Iberian countries since their entry into the European Union (Valladares 1993, Varela et al 1996), traditional livestock farming on these grasslands has been abandoned. Abandonment has been considered to be one of the causes of a decline in biological diversity (Ruíz and Groome 1986, Baldock 1988, Bernáldez 1991, Beaufoy 1996, Liang et al 2001).
Fungi, which play an important role in nutrient cycling, can decompose 90% of biomass (Kjøller and Struwe 1982). Although the microfungi of other temperate grasslands have been studied for some time (England and Rice 1957, Orpurt and Curtis 1957, Luppi Mosca 1960, Ruscoe 1973, Wicklow 1973, Paul et al 1979, Christensen 1981, Clarke and Christensen 1981, Grayston et al 2001), little is known of Mediterranean grassland microflora. Allen et al (1995) found 50–300 m of living hyphae per gram of soil in coastal sage and chaparral sites, which represents 2–20 mg of fungal biomass per gram of soil. There is little information on fungal species that contribute to this biomass or on species occurrence in response to different environmental patterns and grassland management conditions.
Our study analyzed soil microfungal variation in response to elevation, slope position (upper and lower zones) and herbivory (grazing or excluded from grazing). The first of these factors is related to climatic variations, which have been studied in detail for both soil fungal communities (Bisset and Parkinson 1979a, b; Widden 1987; Rodríguez et al 1990) and plant communities (Montalvo et al 1991, Rahbek 1995, among others). The influence of slope position and grazing on soil microfungi has attracted much less attention, except in the case of mycorrhizae (see for example Eom et al 2001). Slope habitats create heterogeneous environments that can affect the structure and function of the plant and fungal communities. Moreover the absence of livestock has led to increased living and dead plant matter that can influence the occurrence of fungal species.
The objective of this study was to characterize the fungal community structure of Mediterranean grasslands in an environment that varies with elevation and slope position. In this framework we analyzed the impact on the fungal community of the cessation of traditional livestock farming. This cessation is known to affect the structure and function of the grassland, and we considered it important to determine the effects on fungi therein because they are the main recyclers of nutrients.
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MATERIAL AND METHODS |
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). The soils are sandy and oligotrophic; granular structure changes little with elevation (TABLE I).
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). Along this gradient there is a noteworthy change in herbaceous species composition, with highly diverse communities dominated by annual species at lower elevations and less diverse communities, with a greater presence of perennial herbaceous species at higher elevation (FIG. 1a). A detailed description of these grasslands can be found in Montalvo et al (1991, 1993).
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) with standing plants and plant litter (FIG. 1b).
To compare the effects of grazing, in 1986 we fenced off 5 x 8 m plots in areas that traditionally were grazed by cattle and sheep. At each site, on both upper and lower zones, we fenced off a plot and adjacent to each plot we established a grazed plot with an identical surface area. The increase of standing plant and especially plant litter values became evident after fencing off the plots (FIG. 1b).
The study design included: elevation (4) x slope position (2) x grazed vs ungrazed plots (2) = 16 total plots. Throughout this paper, "grazing effects" refer to pairwise comparison between enclosed ungrazed plots and adjacent grazed plots.
Sampling.— –
In Sep 1992, 6 y after exclosure of herbivores, soils were sampled. We randomly collected from each plot five soil samples with a 5 cm diam soil corer in the first 5 cm of the mineral horizon, excluding litter. Each of the 80 samples was sieved through a 2 mm mesh sieve. We analyzed 1 g of soil with the dilution plate method (soil/water ratio of 1 : 1000), according to Johnson and Curl (1972) and Maggi and Persiani (1983). This method reveals the groups of fungal species in the soil (Keller and Bidochka 1998). From each suspension, 0.5 mL were plated in five Petri dishes (0.1 mL/dish). The culture medium was soil extract agar, prepared on each occasion from the soil from each plot (Christensen 1969, Persiani and Maggi 1981). In a parallel assay, 0.2 mL (0.1 mL/dish) from each suspension was plated to isolate selectively xerophilic fungi using MY50G (Pitt and Hocking 1985).
Before soil extraction we measured the percentage of surface covered by the herbaceous plants in each soil sample in a 20 x 20 cm quadrant at the center of each core. Other variables associated with the vegetation, such as standing plants and roots, plant litter and percentage of perennial plants, were taken from previous studies (Montalvo 1992, B. Acosta data unpublished).
Data analysis.— –
The number of times each fungal taxon grew in culture was counted from five samples from each plot. For each taxon we analyzed the effects of elevation (four sites), slope position (upper and lower zones) and grazing effect (ungrazed and grazed) with one-way ANOVA (data transformed as log (x + 1)). An LSD test of multiple and simultaneous comparison of means (Day and Quin 1989) was used to identify which species were significantly associated with these factors.
We have done a Multivariate Ordination Analysis to characterize the fungal communities. For each taxon we calculated the frequency of appearance in the five samples of each plot. Only the taxa that appeared in more than two plots were considered. The resulting matrix of data (94 taxa x 16 plots) was analyzed with a detrended correspondence analysis (DCA, Hill 1979) over a dissimilarity matrix obtained with the Bray-Curtis index (Bray and Curtis 1957). We used the PATN statistical package (Belbin 1992).
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RESULTS |
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).
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). When considering only the most frequent taxa (the 68 species appearing in at least 25% of the plots), these differences were greater: elevation (81%), slope position (41%) and the exclusion of the herbivores (38%).
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The position of the 16 plots according to their scores of the first two axes of DCA is provided (FIG. 2). The plots clearly are distributed along axis 1 according to a fungal compositional gradient related to sites: lower scores for the low elevation plots and higher scores for the high elevation plots. Within each site, the lower slope zone tends to have lower scores on axis 1 than the upper one, which likens them in fungal composition to the sites at greater elevations. The same pattern of displacement along this axis is true for the ungrazed plot within each site and slope zone in comparison with its grazed plot. The changes caused by slope position and enclosure tend to be attenuated with elevation (more similar scores in higher elevations).
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). The variation in fungal composition had a significant negative correlation with the herbaceous plants cover (R2 = 0.54, P = 0.0013; FIG. 3e), roots (R2 = 0.585, P = 0.0006; FIG. 3b) and percentage of perennial plants (R2 = 0.83, P < 0.0001; FIG. 3d). It showed no relationship with standing plants and plant litter. However, analyzing separately the higher (sites 3 and 4) and lower (sites 1 and 2) elevations, the relationship found between axis 1 and standing plant was significant (R2 = 0.738, P = 0.0063 and R2 = 0.623, P = 0.0199, respectively; FIG. 3a).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and FIG. 1). Slope position affects availability of water and nutrients, which allows more (in lower slope zones) or less (in upper zones) plant growth and litter accumulation (Casado et al 1985, Montalvo 1992). The effect of slope position is attenuated with elevation. At the same time consumption by livestock determines the amount of standing plants and plant litter in the plot. A halt in grazing eliminates this factor. Although standing plants and litter tend to present higher values with elevation, these value show great variability related to grazing effects and water availability.
Microfungi communities are related to the three factors studied. Higher elevation causes changes in fungal community in the same way that lower slope zones do when compared to upper ones, and ungrazed plots compared to grazed ones. However, some factors are more important than others. Mycoflora communities primarily depend on climatic variation with elevation; the microclimatic and edaphic conditions determined by slope position are less important than elevation. Last, the grazing effect acts in the framework of the slope zone at each site (FIG. 2, TABLE II).
Fungal community is affected mainly by elevation. Fungi also can extend their niche to other elevations where climatic conditions are similar. For example, we found Absidia glauca in all four plots of the site with the most rainfall. In site 3, it appeared only in the two plots of the humid lower slope zone, in site 2 only in the ungrazed lower slope zone, and in site 1 it did not appear at all. On the other end Aspergillus ustus was represented at all site 1 plots. In site 2 it appeared only in the grazed upper slope plot. The predominance of species with patterns similar to these two examples is responsible for only one variation trend, simultaneously related to elevation, slope zone and grazing (FIG. 2).
Bisset and Parkinson (1979a) and Widden (1987) have investigated the influence of elevation on fungal communities. Temperature, humidity, vegetation and some edaphic characteristics were identified as determining factors of fungal community structure (Gochenaur 1978, Bisset and Parkinson 1979c, Widden and Abitol 1980, Widden 1986, Christensen 1989, among others). Mortierella isabellina, for example, is considered to be associated with humid areas (Nilsson et al 1992). In our study it can be seen to dominate the two sites with the highest rainfall. Something similar occurred with Penicillium brevicompactum (Domsch et al 1980, Widden 1986), which in our study appears only in the site with the greatest rainfall. Similar responses to temperature have been described. Widden (1987) associates Penicillium canescens and P. simplicissimum with cold conditions. We found both species at all four elevations, although at greater abundance at the two sites with lower temperatures. Furthermore P. simplicissimum has been associated with the wettest places (Bisset and Parkinson 1979c), which possibly reflects the difficulty involved in separating the effects of temperature and rainfall along an elevation gradient. Although both species of Penicillium appear at the four sites, they are restricted to the lower slope plots, which are more humid.
In addition to elevation, slope position also affects fungi. In our study species such as Penicillium canescens and P. janthinellum, associated by some authors with humid areas, characterized the lower slope plots, whereas Aspergillus fumigatus var. fumigatus, a thermotolerant fungus with a worldwide distribution (Domsch et al 1980) and a marginal xerophile (Ayerst 1969), characterized the two sites at lower elevation and especially upper slope plots with hotter and drier conditions.
In many of the species abundance varies primarily with elevation and secondarily with slope position and presence or absence of herbivores. Grazing effect could be due both to the quantity of litter in the soil and to conditions caused by plants and litter on the surface (Bettucci et al 1993); the ungrazed surface becomes more insulated and retains moisture.
Some characteristics of the plant community are related to variation in fungal composition (FIG. 3). Standing plants and herbaceous cover can affect conditions at the surface, which also might be affected by the percentage of perennial plant species because an increase in that ratio would lessen the influence of summer drought (Schaeffer 1973, Higashida and Takao 1985). Even roots indicate a greater soil moisture content and greater protection from heat.
Plant litter is the only variable that shows no relationship with fungal community composition (FIG. 3c). Standing plants affect fungal communities, but their effect depends on elevation. The same amount of standing plants can have different consequences for fungi depending on elevation (partial correlations in FIG. 3a). Plant materials that are used by fungi undoubtedly constitute an important and decisive resource for the life of the different species (Bisset and Parkinson 1979a, Frankenberger and Dick 1983, Christensen 1989, Schmitz et al 1989), but absolute quantities may be relatively insignificant.
Our hypothesis that fungal composition is affected by environmental factors appears to be supported with respect to elevation along with slope position and herbivory (FIG. 2). In drier conditions at lower elevations the changes induced in the fungi, both due to grazing effect and to slope position, are evident (high dispersion of these plots in FIG. 2). Humid conditions at greater elevation conversely mitigate the effects of slope position, with fewer differences occurring in standing plants and roots and in the proportion of perennial plants between upper and lower slope zones (FIG. 1). On the mountainside the ungrazed plot can accumulate a large amount of litter without any notable modification in its fungal composition, unlike the adjacent grazed plot (FIG. 2).
Experimentally simulated abandonment leads to structural and functional changes in plant communities. It results in an increase in plants and plant litter and a decline in plant species richness (Montalvo 1992, Montalvo et al 1993), although the effect on fungi is relatively unimportant. Change in fungal community seems to be more closely related to temperature and humidity than to the increase in substrate for fungi (Bettucci et al 1993). A halt in grazing does not seem to affect fungi in a major way; the species simply adjust to conditions that may be new to the site but comparable to those already existing in the whole of the territory studied. We must take into account that this study does not consider fungi isolated from litter, which very well might be influenced by plants not consumed by livestock. In summary, similar conditions on ungrazed plots, lower slope plots and plots at higher elevations favor fungi that thrive in wet, cooler, more fertile soil over fungi that prefer drier and hotter conditions.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: oriana.maggi{at}uniroma1.it
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LITERATURE CITED |
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