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Herbario UNSL, Facultad de Química, Bioquímica y Farmacia, Ejército de los Andes 950, 5700 San Luis, Argentina
Marta N. Cabello 2
Instituto Spegazzini, Facultad de Ciencias Naturales y Museo, Ave. 53 No. 477, 1900 La Plata, Argentina
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ABSTRACT |
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The relationships among seasons, host metabolic type, grazing and arbuscular mycorrhizal colonization were analyzed in a high South American native grassland. This study investigated seasonal changes and grazing effects on the symbiotic endomycorrhizal interaction in 5 Poaceae [C3 metabolic pathway: Briza subaristata Lam., Deyeuxia hieronymi (Hack.) Türpe and Poa stuckertii (Hack.) Parodi; with C4 metabolic pathway: Eragrostis lugens Nees and Sorghastrum pellitum (Hack.) Parodi; and a Rosaceae (Alchemilla pinnata Ruíz & Pav.)]. All hosts were dominant species in the mountain grassland in central Argentina. It was found that the seasons markedly influenced endomycorrhizal colonization, whereas grazing did not affect this interaction. C4 grasses presented the highest root colonization. Hosts Briza subaristata (C3 metabolic pathway) and Sorghastrum pellitum (C4 metabolic pathway) showed Arum- and Paris-type colonization and intermediate forms.
Key words: AMF, endomycorrhiza, grasses, grazing, mountain grassland, plant metabolic pathway, seasonality
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Haystead et al 1988, Sanders and Fitter 1992c). AM association aids plant growth and biomass enlargement, increasing plant resistance to herbivores and pathogens (Clay 1992, Gehring and Whitman 1994). Fungi also benefit from this association because they obtain carbon compounds, necessary for fungal growth, from plant photosynthetic activity. Moreover, the extraradical mycelium may translocate nutrients from one host to another (Haystead et al 1988, Martins 1992, McNaughton and Oesterheld 1990). AM fungi likely are important wherever soils have little organic matter (Allen et al 1995).
It is known that AM fungi root colonization has seasonal dynamics (Allen 1996, DeMars and Boerner 1995, Rosendahl and Rosendahl 1992, Sanders and Fitter 1992b). Hetrick et al (1990) observed a close relationship between the degree of association with AM fungi and the metabolic pathway of the Poaceae host; thus, C3 hosts are considered to be facultatively mycotrophic and C4 obligately mycotrophic. In addition, the fungal symbiont will influence different developmental stages of grasses depending on host type, favoring seedlings in C3 and flowering stages in C4 hosts (Hartnett et al 1993, Wilson and Hartnett 1997). Finally, host growth and colonization by AM fungi are a function of plant/fungus combinations (Sanders and Fitter 1992a).
Bethlenfalvay and Dakessian (1984) and Bethlenfalvay et al (1985) support the idea that colonization and diversity of plant species decline with grazing, while other authors (Gange et al 1993, Gehring and Whitman 1994) have corroborated the opposite. At the same time, Wallace (1987), Reece and Bonham (1978), and Allen et al (1989) found no effects.
Even though the degree of association of Gramineae and mycorrhizal fungi varies with the seasons (DeMars and Boerner 1995, Rosendahl and Rosendahl 1992, Sanders and Fitter 1992b), intensity and the type of disturbance (Gange et al 1993, Gehring and Whitman 1994, Grime et al 1987, Sanders and Fitter 1992a, c), and host metabolic pathway (Hetrick et al 1988, 1990), no field experimental studies in natural ecosystems simultaneously take into account all these factors. Furthermore, only a few field studies have dealt with the morphology of AM colonization (Merryweather and Fitter 1998). Thus, the aim of this research was to study the AM root colonization of C3 and C4 grass hosts in different grazing situations, to analyze their morphological variation in fungi, and to observe seasonal changes and the interactions among them in a native mountain grassland.
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MATERIALS AND METHODS |
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The average winter temperature is 5 C and average summer temperature is 11.4 C. Rain averages 850 mm per year; frost may occur at almost any time, with occasional snowfall (Díaz et al 1994, Pucheta and Cabido 1992). The vegetation is a climatically determined grassland traditionally subjected to pastoral use (cattle, sheep and horses).
Experimental design –
To examine the effect of grazing on AM fungal colonization, we examined sites in two conditions: an area protected by fences from large herbivores for at least 20 years (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 of them corresponded to grazed lands and the others to ungrazed ones. They represented the three replicates for each situation, and they were designated as Grazed (1, 2, 3) or Not Grazed (1, 2, 3).
Plant species studied –
The Poaceae studied were perennial: Briza subaristata Lam., Deyeuxia hieronymi (Hack.) Türpe, and Poa stuckertii (Hack.) Parodi (with C3 metabolism); and Eragrostis lugens Nees and Sorghastrum pellitum (Hack.) Parodi (with C4 metabolism). Alchemilla pinnata Ruiz & Pav. (Rosaceae with C3 metabolism), frequently present, also were included in this study. All of them are palatable (Pucheta and Cabido 1992).
Methodology – At each site, samples were collected in autumn (May 21, 1996), autumn (June 2–3, 1997), winter (Sept. 8, 1996), winter (Aug. 6–8, 1997), spring (Dec. 8, 1996), spring (Nov. 11–12, 1997), and summer (Feb. 20, 1997). Eight whole (stem and root) individuals per host species and their rhizospheric soil were collected from each site. Samples were kept in plastic bags, at 4 C; roots were separated from rhizospheric soil, washed and fixed in FAA solution.
Roots –
Washed and stored in FAA for later clarification and staining, following Phillips and Hayman (1970) and Grace and Stribley (1991) methodology, respectively. Five subsamples of 100 root segments (1 cm long each) for host species were analyzed for each season, in each site and grazing situation. Frequency of colonization (F) and percentage of root length colonized (% RL) were quantified according to the grid-line intercept method (Biermann and Linderman 1981). From Briza subaristata and Sorghastrum pellitum 10 colonized root fragments from each of the five subsamples (n = 50) were placed on slides, and the number of fungal intraradical structures, such as arbuscules, vesicles, coils and entry points, were estimated, according to Ocampo et al (1980). These host species were chosen because they are the most palatable grasses in this ecosystem and they represent both C3 and C4 metabolic types.
Statistical analysis –
The data distribution was not normal (Kolmorov-Smirnov and Shapiro-Wilkins normality tests), and variances were not homogeneously distributed throughout the treatment (Levene Test). Thus data transformation was not suitable for application of parametric analysis. The variables (percentage of root colonized, frequency of colonization, frequency/cm of root arbuscules, vesicles, coils and entry points) 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) and the Wilcoxon test using SPSS (Systat Co., http://www.spss.com). The various host species, their metabolic pathways (C3 or C4), grazing conditions (grazed or not grazed) and seasons (summer, autumn, winter and spring) were considered factors. All were analyzed at 
= 0.05 and P 
0.05 significance. When Kruskall Wallis showed significant differences, data were analyzed by an a posteriori test, using the Infostat statistic program (Infostat Beta Version, Department of Statistics and Biometry, Faculty of Agronomic Sciences, National University of Córdoba, Córdoba, Argentina). Correlation analysis using the Spearman coefficient with = 0.05 for frequency/root cm of intraradical structures was performed.
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RESULTS |
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When each season was analyzed separately, both F and % RL showed significant differences among host species (Table II). Thus, F and % RL were found to be influenced by host in summer, autumn, winter and spring. In summer, S. pellitum showed the significantly highest colonization followed by B. subaristata, E. lugens and P. stuckertii (without significant differences among them). The lowest F values were observed in D. hieronymi and A. pinnata. In autumn and winter, B. subaristata and S. pellitum showed the highest F value; the lowest F value was found in E. lugens, P. stuckertii and D. hieronymi (without significant differences among them) in autumn and in E. lugens and D. hieronymi in winter. In spring, B. subaristata had the significantly highest F value, followed by S. pellitum, P. stuckertiii and E. lugens without significant differences among them, followed by D. hieronymi and A. pinnata with the lowest colonization. The % RL showed similar F patterns but with lower values.
When each host was analyzed separately, both F and % RL showed significant differences among host species (Table II). Based on F and % RL, two groups of grasses could be determined: one of them formed by S. pellitum, E. lugens, P. stuckertii and D. hieronymi with the highest colonization in summer; the other with highest values in autumn comprising B. subaristata and A. pinnata.
Taking into account the seasons, in summer F and % RL colonization were significantly different between C3 and C4 host species (Table III). In autumn, F was significantly different between metabolic types with the highest colonization in C4 plants, and % RL did not differ; % RL was significantly higher in hosts with C3 metabolic pathway in winter and spring, whereas F did not change in winter and in spring. Grazing did not influence root colonization (F and % RL, respectively) either in summer, autumn, winter or spring.
Intraradical fungal structures in B. subaristata (C3) and S. pellitum (C4) – Number of intraradical fungal structures by root cm differed significantly with seasons, being higher in summer and lower in winter, autumn and spring. The percentage of vesicles showed the highest value in summer, followed by autumn, winter and spring. The percentage of arbuscles and coils was higher in the period between summer and winter than in the period between autumn and spring, whereas % entry points were highest between summer and winter, falling in autumn and spring. Although % arbuscles showed significant differences between autumn–spring and summer–winter periods, these values were zero or nearly zero. Similar results were found in % entry points between autumn and spring (Table IV). Frequency of structures had no significant differences, related to grazing (Table IV).
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DISCUSSION |
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, Douds 1994, McNaughton and Oesterheld 1990, Miller and Jastrow 1994, Newsham and Watkinson 1998).
Some authors (Gange et al 1993, Grime et al 1987, Wilson and Hartnett 1997, McNaughton and Oesterheld 1990, Sanders and Fitter 1992b) hypothesized that, in environments with little phosphorus in the soil, dominant species are those that associate with AM fungi. Pampa de Achala soils have little phosphorus (Lugo 1999). Moreover, the plant species that we analyzed were among the dominant species in these communities (Cabido 1985) and were associated with endomycorrhizae, in agreement with this hypothesis. Root colonization values were found to be similar to those in other grassland communities studied (Dickman et al 1984, Hetrick and Bloom 1983, Wallace 1987).
Seasonality –
It is known that fungus colonization is influenced by soil moisture. In the grassland studied, summer is the wet season, while autumn and winter are dry, with occasional rain in spring (Cabido et al 1987). Root colonization, number of arbuscles, and vesicles reached their maximum values in summer. These values might be due to the high metabolic activity of plants and soil moisture. The peaks of colonization observed during spring could be due to the sporadic rains that can activate fungus colonization. Our observations of seasonal changes and their relationship to root colonization, soil moisture and host phenology were similar to the results of other authors (Bentivenga and Hetrick 1992, DeMars and Boerner 1995, Ebbers et al 1987, Rosendahl and Rosendahl 1992, Sanders and Fitter 1992b, Sigüenza et al 1996, Wilson and Hartnett 1997). In the system studied total live root biomass followed a seasonal pattern (Pucheta pers com) and was reflected in F and % RL colonization.
Based on the seasonality of radical colonization, the host species could be separated into two groups: i) greater colonization in autumn-winter (A. pinnata and B. subaristata) and ii) greater colonization in summer-autumn (D. hieronymi, P. stuckertii, E. lugens and S. pellitum). In addition, these patterns among hosts could correlate with seasonal changes in fungal communities in rhizospheric soil (Lugo and Cabello 2002). Thus, in the Pampa de Achala, high root colonization by AM fungi is associated with a low number of spores in soil and vice versa. This fungal behavior and host seasonal patterns would explain the seasonal changes in spore diversity and the little host specificity found in this grassland (Lugo and Cabello 2002).
Grazing effects –
Controversial opinions about grazing effects on root colonization abound. Some authors (Bethlenfalvay and Dakessian 1984, Bethlenfalvay et al 1985) have reported that colonization declines with great ungulate herbivory; others supported the idea that herbivory favors colonization (Reece and Bonham 1978); while still others (Allen et al 1989, Wallace 1987) have stated that herbivory does not modify colonization. In this study, results showed that radical colonization was not modified by grazing. This could be due to three factors. First, AMF colonization is related to host phenology (Allen 1991a) and in the Pampa de Achala ecosystem, grazing did not influence host phenology (Díaz et al 1994). Thus, the absence of grazing influence on host phenology could be reflected in root colonization. Second, in soils poor in phosphorus, such as the grassland studied, the extraradical mycelium is more developed and it behaves as a system stabilizer (McNaughton and Oesterheld 1990), interconnecting hosts and diminishing grazed and ungrazed differences. Third, McNaughton (1983) suggested that grazing increases photosynthesis and growth as the plant compensates. Mycorrhiza increase photosynthesis and require carbon from the host (Allen 1991b). Thus, the failure of grazing to affect fungal colonization in the Pampa de Achala is the result of a compensatory response of these grasses. Thus, one might speculate that plants overcome the loss of photosynthetic cells by increasing photosynthesis and nutrition with the help of symbiotic fungi.
In this mountain grassland, B. subaristata (C3 host) and S. pellitum (C4 host) are perennial, long-life cycle, and largely consumed by livestock. Moreover, the ecosystem of Pampa de Achala has a lengthy grazing history (Díaz et al 1994). The failure of grazing to affect B. subaristata and S. pellitum colonization could be an adaptation to its long grazing history.
Host metabolic pathways – Significantly higher values of root colonization in the summer–autumn period in C4 hosts could be due to their capacity to obtain higher profits and root growth at higher temperatures and with abundant rainfall. The opposite was valid for C3 hosts, which showed significant colonization in winter and spring, when temperatures are low and rain is scarce. It is possible that the mycorrhizae provide water to its host, improving survival during dry seasons.
Fungal intraradical structures –
In B. subaristata (C3) and in S. pellitum (C4), the fungal structure quantification showed a marked seasonality. This could be related to nutrient exchanges. In both hosts, fungal structures (arbuscules, coils, vesicles and entry points) were more abundant in summer, the season with high moisture, temperature as well as solar radiation. In a previous study (Smith and Read 1997), the abundance of intraradical structure was closely related to host growth, flowering and fruit production. Solar radiation declined in autumn and winter, resulting in a decline in the amount of mycorrhizal structures (Smith and Read 1997). This might explain the few exchange structures found. Considering the amount of these structures, both hosts presented a similar seasonal behavior. In spring and autumn, Briza subaristata showed a large number of coils and arbuscles, due to high radical colonization. On the other hand, Sorghastrum pellitum exchange structures did not change seasonally, suggesting that this host has the same metabolic activity throughout the year.
Colonization morphology –
The endomycorrhiza types that colonize B. subaristata and S. pellitum were characterized by their colonization morphology; both hosts showed multiple colonizations. Characteristics of Acaulosporaceae and Glomaceae were recognized in B. subaristata. Thick walls of intercellular hyphae with projections and H connections, as well as intercellular vesicles determining the Arum-type, were abundant. On the other hand, Paris-type colonization was determined by intracellular coils and arbuscules that partially occupy the host cell. In S. pellitum, structures of Acaulosporaceae, Glomaceae and Gigasporaceae were recognized, with coils and intracellular hyphae being the most common. These structures, together with intercellular hyphae and terminal arbuscules, indicate the coexistence of Arum- and Paris-types in the same plant (Barker et al 1998, Smith and Smith 1997). The positive correlation among arbuscules, coils, entry points and vesicles could be related to colonization by several fungi. Then, it was found that in some host species AM fungi might form vesicles. The correlation between entry points-vesicles and entry points-arbuscules suggests AM fungi families Glomaceae and Acaulosporaceae, which form these root colonization structures, while the entry points-coils relationship suggests Gigasporaceae because the vesicles are absent in host roots. The correlation between vesicles-arbuscles and vesicles-coils might be an expression of the symbionts' physiological condition. In fact, the presence of arbuscles and coils, which are considered the exchange structures between symbionts, along with the presence of vesicles, which are storage structures, might be due to the intense exchange activity between the symbionts. The positive correlation between coils-arbuscules could explain multiple colonization because arbuscles are the common structure among all AM fungi and coils are more frequently formed by Gigasporaceae.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 M.N. Cabello is researcher of the CIC, Bs. As. Prov., Argentina
Accepted for publication December 6, 2002.
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