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Native arbuscular mycorrhizal fungi (AMF) from mountain grassland (Córdoba, Argentina) I. Seasonal variation of fungal spore diversity

     Herbario UNSL, Facultad de Química, Bioquímica y Farmacia, Ejército de los Andes 950, 5700 San Luis, Argentina, Email: lugo{at}unsl.edu.ar

Marta N. Cabello

     Instituto Spegazzini, Facultad de Ciencias Naturales y Museo, Calle 53 N° 477, 1900 La Plata, Argentina

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

Arbuscular mycorrhizal fungi (AMF) were studied in the rhizosphere of 3 Poaceae with metabolic pathway C₃ (Briza subaristata Lam., Deyeuxia hieronymi (Hack.) Türpe and Poa stuckertii (Hack.) Parodi), 2 Poaceae with C₄ metabolic type (Eragrostis lugens Nees and Sorghastrum pellitum (Hack.) Parodi.), and a Rosaceae (Alchemilla pinnata Ruíz & Pav.) from a natural mountain grassland in Central Argentina (South America). Host species, their metabolic type, seasonal changes, and grazing effects over AM fungal diversity were analyzed. Seventeen mycorrhizal fungi taxa were found, widespread in all families of Glomales. Density of endomycorrhizal fungi was found to be strongly influenced with seasons and host metabolic pathway, although biodiversity (H), richness (S) and evenness (E) did not change. In most cases grazing did not affect these variables.

Key words: C₃, C₄, endomycorrhizal fungi richness, fungal spore biodiversity, glomalean density, Glomales, highland grass

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Arbuscular mycorrhizal fungi (AMF) are colonizing the majority of herbaceous plant roots in natural ecosystems all over the world (Trappe 1987, Allen et al 1995). In Poaceae this association is widespread and occurs, with few exceptions, in both annual and perennial species. AM colonization is common in infertile habitats (Newsham and Watkinson 1998) and typical grassland soils with low phosphorus level (McNaughton and Oesterheld 1990). In grass hosts, AMF colonization is influenced by the host metabolic type. Thus, cold-season grasses (C₃ metabolic type) are facultative mycotrophs, while warm-season grasses (C₄ metabolic type) are the obligate ones (Hetrick et al 1990, Bentivenga and Hetrick 1992). Likewise, fungal species showed different responses regarding growth and colonization intensity, which depend on host species. Thus, some host-fungus combinations would be more favored than others (Sanders and Fitter 1992a).

Seasonal fungal patterns are closely related to host phenology and climate variations (Bentivenga and Hetrick 1992, Rosendahl and Rosendahl 1992, Sanders and Fitter 1992b, De Mars and Boerner 1995, Allen 1996). Seasonal changes in diversity of AMF were studied mainly in sand dune systems (e.g., Koske 1975, Giovannetti and Mosse 1985, Sylvia 1986, Gemma and Koske 1988, Gemma et al 1989, Blaszkowski 1994, Stümer and Beller 1994, Sigüenza et al 1996, Blaszkowski et al 1998). However, few studies were carried out in other habitats (Johnson et al 1991, Cuenca and Lovera 1992, Clapp et al 1995, Vestberg 1995, Guadarrama and Álvarez-Sánchez 1999).

Grazing effects over AM fungal colonization are controversial (Reece and Bohman 1978, Bethlenfalvay and Dakessian 1984, Bethlenfalvay et al 1985, Wallace 1987, Allen et al 1989, Gange et al 1993, Gehring and Whitman 1994), and their influence on fungal diversity has been poorly reported.

Despite our knowledge about how seasonal changes, grazing effects, and the host metabolic type influence AMF colonization, there are few field experiments to date that take all these factors into consideration. The aim of this work, then, was to study AM fungal diversity (density and richness) in mountain grassland, its relationship with host species and host metabolic types, gazing, and seasonality.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Site of study – This research was carried out in Pampa de Achala, a granite plateau at 2250 m above sea level, in Sierras de Córdoba, Argentina (31°20'S, 64°45'W). The climate is temperate with cold dry winters (average temperature 5 C) and short cool summers (average temperatures 11, 4 C). The average rainfall is 850 mm, from October to April. Frost may occur at almost any time, occasionally snow may fall in winter and spring (Díaz et al 1994, Pucheta and Cabido 1992). The vegetation is a climatically determined grassland traditionally subjected to pastoral use (cattle, sheep, and horse). Climatic and floristic features are described in detail by Cabido (1985).

Soils have light acid pH and high degradation velocity. The texture varies from loam to clay-loam. It is related to the "Deyeuxia grassland" classified as Humic Cambisol/Cumulic Haplumbrept, Haplic Phaeozem/Entic Hapludoll, and Haplic Phaeozem/Fluventic Hapludoll (Cabido et al 1987).

Host species – The rhizospheres of three Poaceae with C₃ metabolic type (Briza subaristata Lam., Deyeuxia hieronymi (Hack.) Türpe, Poa stuckertii (Hack.) Parodi), two Poaceae with C₄ metabolic type (Eragrostis lugens Nees and Sorghastrum pellitum (Hack.) Parodi), and that of a C₃ Rosaceae (Alchemilla pinnata Ruíz et Pav.), were studied. All hosts were perennial species.

Experimental design – To examine the effect of grazing on AMF spore production we considered two situations: an area protected by fences from large herbivores for at least 20 yr (NG: ungrazed) and a nearby area under continuous intense grazing by cattle and horses (G: grazed) with moderate to high stocking rate: ca 0.25 horses and 0.5 cows per hectare (Pucheta et al 1998). Six sampling sites of 1 hectare each, separated by 3 km, were selected. Three corresponded to grazed lands and the others to the ungrazed. They represented the three replicates for each situation, and they were named site 1, 2, and 3.

In each site studied, samples were collected during iterated seasons: autumn (21-V-96), autumn (2-3-VI-97), winter (8-IX-96), winter (6-8-VIII-97), spring (8-XII-96), spring (11-12-XI-97), and summer (20-II-97). Eight whole (stem and root) individuals per host species and their rhizospheric soil were collected from each site and from the 2 different situations (G or NG). Samples were kept in plastic bags at 4 C for around a week until processed.

Methodology – The rhizospheric soil from the 8 host individuals for each species, under grazing and non-grazing conditions, was mixed. For the spore and sporocarps extraction, 100 mL were treated by the wet sieving and decanting method (Gerdemann and Nicolson 1963). The resulting material was centrifuged with 80% sacarose (Walker et al 1982). Quantification was carried out in 9-cm-diameter Petri dishes with gridline of 1 cm per side under a stereoscopic microscope at 50 X. In the major fractions (500 and 250 µm sieves) the total divisions were counted, while only 10 divisions were counted in the minor one (45 µm). These 10 divisions were related to the total number of spores, using the method modified by McKenney and Lindsey (1987). Sporocarps were counted as one spore. For the taxonomic identification, fungal spores and sporocarps were mounted onto slides using PVA (Omar et al 1979) with and without Melzer reagent (Morton 1988). Vouchers were deposited in the Herbarium at the Botanic Museum of Córdoba (CORD), Argentina.

The total fungal density was considered as total spore number per 100 mL of soil, and spore density of each fungal species as the spore number of a specific fungal species per 100 mL of soil.

The fungal specific spore density was used to calculate the biodiversity index Shannon-Weaver, H; species richness, S; and evenness, E. Species richness, S, is simply the number of different species found in all samples. Species diversity, H, that encompasses both S and E, may be quantified according to Magurran (1988):

where Pi is the probability of finding each species i in one sample.

Species evenness, E, that measures the equity of the presence of each species in all samples, is given by:

From eq. 2 it can be deduced that

in which the Shannon-Weaver index appears as the product of the two main components of diversity: evenness and the number of species. Thus, an increased diversity implies not only an augmentation in the number of species but also in the evenness of their distribution (Frontier and Pichod-Viale 1995).

The Shannon-Weaver index was used since an equal probability of capture/encounter of species was assumed due to the high number of host individuals sampled, the large sample sites, and the seasonal collection of samples.

Identification of AM fungal species was specified by Lugo and Cabello (1999) and Lugo et al (1999). Monospecific cultures were placed in "AMF living culture collection" at Spegazzini Institute, La Plata, Argentina. Current, non identified specimens were maintained in culture and were named with the genera followed by a discriminated number.

Data analysis – In agreement with other authors (St. John and Koske 1988, Bever et al 1996), spore density (total and specific) was not normally distributed, data were compared by Kruskal-Wallis one way analysis by ranks when the factors had more than two levels (season and host species), and Mann-Whitney U-test when factors had only two levels (host metabolic type, grazing conditions) using SPSS (Systat Co.). All factors were analyzed at = 0,05 and P 0,005 significance.

AM diversity (H), fungal richness (S) and evenness (E) differences between grazing conditions for all the host species analyzed in this study were determined by paired t-test at P 0.05.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
When field spores were quantified, the acknowledged entities were named at generic level with a numerical subscript. After isolation and trap culture, these entities were identified at specific level, resulting 17 species. Fungal entities were identified as the following genera and species: A. mellea Spain & Schenck (C-6, C-6.1 LPS); complex namely as Acaulospora₂ was identified as A. bireticulata Rothwell & Trappe (C-14 LPS) and A. spinosa Walker & Trappe; the complex Acaulospora₃ as A. excavata Ingleby & Walker (C-11 LPS), A. gerdemannii Schenk & Nicolson (C-19 LPS), and A. scrobiculata Trappe (C-24 LPS); Entrophospora infrequens (Hall) Ames & Schneider (C-25 LPS); A. laevis Gerd. & Trappe; sporarpic complex Glomus spp.; Sclerocystis rubiformis Gerd. & Trappe; G. intraradices Schenck & Smith; G. fuegianum (Speg.) Trappe & Gerd.; Glomus sp.₃; G. dimorphicum Boyetchko & Tewari (C-21 LPS); Glomus sp₇.; Scutellospora biornata Spain, Sieverding & Toro and Scutellospora sp.

Fungal spore density – Total number of spore ranged between 8 to 4083 spores/100 soil mL (data not shown cf Lugo 1999). A significant variation was observed according to the seasons (K: 59.9849; P = 0.000, Kruskal-Wallis one way analysis by ranks). In general, higher values were found in autumn which decreased in summer (Fig. 1). Most of the host species showed similar patterns, and the metabolic types and grazing did not affect the spore total number.

View larger version (39K): [in this window] [in a new window]    FIG. 1. Seasonality of spore total density/100 mL of soil in different grazing conditions. Data are mean of three replicates (sites 1, 2, 3). Error bars = SE. The same letter above bars indicates that the values do not differ significantly as determined by Kruskal-Wallis no-parametric test (P 0.05). Abbreviations: AP, A. pinnata; BS, B. subaristata; DH, D. hieronymi; PS, P. stuckertii; EL, E. lugens; SP, S. pellitum; G, grazed, NG ungrazed

View larger version (23K): [in this window] [in a new window]    FIG. 2. Seasonality of spore specific density/100 ml of soil in different grazing conditions. Data are mean of three replicates (sites 1, 2, 3). Abbreviations: C3, host metabolic type C3; C4, host metabolic type C4; A, complex Glomus spp.; B, Glomus sp3; C, G. dimorphicum; D, G. fuegianum; E, G. intraradices; F, Sclerocystis rubiformis; G, Acaulospora laevis; H, A. mellea; I, complex Acaulospora sp3; J, complex Acaulospora sp2; K, Entophospora infrequens; L, Scutellospora sp; M, S. biornata; N, Glomus sp7.

Fungal biodiversity – In general, the highest value of biodiversity index (H) was found in wet seasons as spring and summer. Significant differences in the H index were only found in the rhizosphere of E. lugens in winter and of A. pinnata in autumn between ungrazed/grazed situations. The same pattern was observed with the species richness (S) and evenness (E) (data not shown).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Seasonal variation relative to spore density and its relationship with host phenology and water availability are well known (Ebbers et al 1987, Gemma et al 1989, Allen 1991, Bentivenga and Hetrick 1992, Rosendahl and Rosendahl 1992, Sanders and Fitter 1992b, Blaszkowski 1994, De Mars and Boerner 1995, Sigüenza et al 1996, Wilson and Hartnett 1997) and they agree with our results. The highest spore density was found in the dry seasons (autumn and winter) coincident with the lack of flowering and fruting, and the end of the growth season. The opposite occurrence was found in wet seasons (spring and summer).

Changes in seasonal spore density would define three sporulation patterns in these arbuscular mycorrhizal fungi: (i) in the first group fungi sporulation appeared in autumn (sporocarpic complex Glomus spp and Sclerocystis rubiformis); (ii) in the second group in spring (A. mellea, A. excavata + A. gerdemanni + A. scrobiculata, G. dimorphicum and Scutellospora biornata), and (iii) in the third one the sporulation occured throughout the year (the remaining species). This phenomenon of AM fungal species substitution or succession was reported by some authors (Walker et al 1982, Gemma et al 1989, Allen and Allen 1992, Koske and Gemma 1997). Likewise, root colonization in this mountain grassland reflected this fact (Lugo 1999).

The spore total density records were higher than those found by others authors (Walker et al 1982, Anderson et al 1983, McGraw and Hendrix 1984, Dalpé et al 1986, Ebbers et al 1987, Gemma and Koske 1988, Gemma et al 1989, Blaszkowski 1994, Stürmer and Beller 1994, Vestberg 1995, Bever et al 1996, Koske and Gemma 1997, Blaszkowski et al 1998). It is reasonable to assume that these differences are mainly due to the different ecosystems studied.

Preferential density variation in Glomus sp₃ associated to P. stuckertii, G. fuegianum to all C₃ hosts and Scutellospora sp to the C₄ ones is in agreement with AMF low physiological specificity or differential association hypothesis (Hetrick et al 1990, Sanders and Fitter 1992a, Hartnett et al 1993, Read 1998, van der Heijden et al 1998). Also, root colonization was higher in C₄ hosts (Lugo 1999) because they are obligatory mycotroph plants (Hetrick et al 1988, 1990, Bentivenga and Hetrick 1992, Wilson and Hartnett 1997). Further, when we analyzed total spore density in each season we found that Gigasporaceae members were preferentially associated to C₄ host as seen in the colonization morphology (Lugo 1999). Thus, our current results evidence that the host-dependence of fungi affects their population growth rates. In addition, it must be emphasized the host influence over the AMF species diversity (Bever et al 1996).

The 17 AM fungi taxa found in Pampa de Achala plateau showed that the AMF richness was low resembling the one present in temperate grasslands (Allen et al 1995, Morton et al 1995). However, Bethlenfalvay and Dakessian (1984) reported that richness and density decrease when the host is grazed, this fact was only observed in Scutellospora sp whereas the opposite was found in A. mellea, A. laevis and sporocarpic complex Glomus spp. The fact that spore density was higher under grazing than under no grazing conditions in dry seasons, could be due to the low water content in soil, and/or to grazing derived effects e.g., trampling, which could be considered as inhibitory or triggering factors in AM fungi spore production. This analysis is supported by the hypothesis that certain fungal species may be tolerant or not to grazing (Gehring and Whitham 1994).

Eom et al (2001) reported the influence of grazing over specific spore density, however our result showed that it was not modified. The fungal biodiversity was significantly higher only in ungrazed A. pinnata and E. lugens hosts in autumn and winter, respectively. This finding agreed with the result found in tallgrass prairie above cited.

It must be taken into account that the lack of variation in the total spore density and in fungal richness could be the consequence of the hosts selected since all of them were dominant species within the studied community. A further analysis, including rhizospheric soil from dominant and less important plants could paint a complete picture of the AMF richness in the grassland studied.

View larger version (37K): [in this window] [in a new window]    FIG. 3. Mean Shannon-Weaver species diversity of AM fungal spore communities. Data are mean of three replicates (sites 1, 2, 3). Error bars = SE. Asterisks denote significant differences between ungrazed and grazed (P0.05) as determined by t-test. Abbreviations: S, summer; A, autumn; W, winter; SP, spring; Ap, A. pinnata; Bs, B. subaristata; Dh, D. hieronymi; El, E. lugens; Ps, P. stuckertii; Sp, S. pellitum; G, grazed; NG, ungrazed

	ACKNOWLEDGMENTS

	FOOTNOTES

 
¹ Corresponding author, Email: lugo{at}unsl.edu.ar

Accepted for publication November 27, 2001.

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