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a Division of Biology, 232 Ackert Hall, Kansas State University, Manhattan, Kansas 66506-5502
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: cool-season grass • forb • mycorrhizae • mycorrhizal responsiveness • phenology • tallgrass prairie • warm-season grass
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In tallgrass prairie, host-plant mycorrhizal dependence, phenology, and root morphology differ significantly between C3 and C4 grasses. The cool-season C3 grasses achieve maximum growth in spring and fall when temperatures are relatively low. They have highly fibrous root systems and are weakly or nondependent on mycorrhizal symbiosis, despite the low available phosphorus levels in native prairie soils. In contrast, warm-season C4 grasses grow best in midsummer when temperatures are high, have coarser root systems, and are obligate mycotrophs, i.e., warm-season grasses cannot grow to maturity in native prairie soil without mycorrhizal symbiosis or additional phosphorus fertilization (Hetrick, Kitt, and Wilson, 1988; Hetrick, Wilson, and Todd, 1990). Tallgrass prairie forbs can similarly be separated into distinct groups that reach vegetative maturity and flower in late spring (cool-season) or by early fall (warm-season). However, unlike the grasses, dicots (including the tallgrass prairie forbs) use the C3 photosynthetic pathway (Salisbury and Ross, 1985) regardless of phenology. Root fibrousness of prairie forbs also varies among species or genera groups, and previous research has indicated that mycorrhizal dependence of prairie forbs is strongly related to root fibrousness and, to a lesser extent, flowering phenology (Hetrick, Wilson, and Todd, 1992).
The determination of plant growth responses under controlled conditions is a valuable first step in evaluating the importance of the symbiosis in nature and understanding ecosystem dynamics and interactions. Previous studies have assessed the mycorrhizal dependencies of selected tallgrass prairie grasses and forbs, however these data have been presented only for designated groups of species, with no information provided for individual plant species (Hetrick, Wilson, and Todd, 1990, 1992). While the responses of physiological groups of plants within an ecosystem are important, an understanding of the variation in responses among individual species is also important. Much current work on the role of mycorrhizal symbiosis in native plant communities indicates that interspecific variation in host-plant benefits from mycorrhizal colonization may be a key factor explaining patterns of species interactions and community structure (Gange, Brown, and Sinclair, 1993; Hartnett et al., 1993; Newsham et al., 1995). In addition, variation in mycorrhizal dependency among species has potentially important applications for prairie conservation, restoration, and management. The purpose of this study was to assess patterns of interspecific variation in host-plant benefit (i.e., growth response) from the symbiosis among a wide range of tallgrass prairie grasses and forbs and to examine patterns of responses of various taxonomic, life history, and phenological host-plant guilds. Specifically, we examined differences in the importance of mycorrhizal symbiosis among warm- and cool-season grasses and forbs, between annual and perennial species, and between legumes and nonlegumes. The latter comparison was of particular interest because of evidence suggesting an important role of mycorrhizal symbiosis in enhancing N-fixation in legumes.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Plant preparation
Seeds of 36 grass species and 59 forb species were obtained locally from the Soil Conservation Service Plant Materials Center, or from commercial seed sources: F&J Seed Service, Woodstock, Illinois 60098; Prairie Moon Nursery, Winona, Minnesota 55987; Prairie Ridge Nursery, Mt. Horeb, Wisconsin 53572; Sharp Brothers Seed Company of Missouri, Inc., Clinton, Missouri 64735; or Valley Seed Service, Fresno California 93791. Nomenclature of listed species follows Flora of the Great Plains (Great Plains Flora Association, 1986). Seed was pretreated as suggested by Prairie Moon Nursery or the Prairie Propagation Handbook (Rock, 1977). Seeds of each species were germinated in vermiculite. Six to 24 days (second-leaf stage) after emergence 14 seedlings were individually transplanted into pots containing steam-pasteurized soil, and seven seedlings were transplanted into pots containing nonsterile soil. Plastic pots (6 x 25 cm) were filled with 470 g (dry mass) of steamed or nonsterile soil. Legumes were inoculated with species-specific Rhizobium inoculum supplied by Prairie Ridge Nursery (Mt. Horeb, Wisconsin).
Mycorrhizal fungus inoculum preparation
Spores of G. etunicatum and G. mosseae were collected from Trifolium pratense L. pot cultures by wet-sieving, decanting, and sucrose density centrifugation (20-40-60% sucrose; Daniels and Skipper, 1982). Spores were originally isolated from Konza Prairie Research Natural Area and subsequently maintained in pot cultures in a 20°–25°C greenhouse. For each plant species, seven of the pots containing steam-pasteurized soil were inoculated with 200 G. etunicatum and 200 G. mosseae spores by pipetting them onto roots of each seedling at transplant. The seven pots containing nonsterile soil were not inoculated because the soil contained indigenous mycorrhizal fungi. The remaining seven pots containing steam-pasteurized soil were left noninoculated to provide a nonmycorrhizal control. Thus, there were three soil treatments (steamed soil inoculated with mycorrhizal fungus, steamed soil without inoculum, and nonsterile soil), with seven pots for each soil treatment for each plant species.
Experimental design and maintenance
Pots were blocked by plant species, and plants within a species were arranged in a completely randomized design with seven replicates per treatment. The plants were maintained in a 18°–22°C greenhouse for 16 wk. This temperature was selected because it is suitable for growth of both warm- and cool-season plant species and does not differentially inhibit the growth of plants in either group (Hetrick, Kitt, and Wilson, 1988). Plants were watered daily and fertilized every other week with 35 µg/g N and 35 µg/g K, applied as Peter's No-Phos Special Fertilizer solution (25:0:25, Robert B. Peter's Co., Inc., Allentown, Pennsylvania). After 16 wk, plants were harvested and roots were washed free of soil. Plants were oven-dried for 72 h at 70°C; then shoot, root, and total dry masses were recorded. Subsamples of dried roots were stained in trypan blue (Phillips and Hayman, 1970) and examined microscopically to assess percentage root colonization using a Petri dish scored in 1-cm squares (Daniels, McCool, and Menge, 1981).
Statistical analysis
Data were tested for homogeneity of variance prior to analysis. Variances were determined to be homogeneous according to Levine's test for homogeneity of variance (Milliken and Johnson, 1984). Shoot and root dry masses were highly correlated with total dry mass for all plant species. Thus, only total dry masses were used for mycorrhizal responsiveness calculations.
In this experiment, plant growth in nonsterile soil and in steam-pasteurized soil inoculated with G. etunicatum and G. mosseae spores were highly correlated (P = 0.0001; r = 0.894). Therefore, the data were analyzed with these mycorrhizal treatments combined (N = 14), and were considered a "mycorrhizal" treatment and compared to the "nonmycorrhizal" treatment of the noninoculated steam-pasteurized soil. All mycorrhizal responsiveness calculations were conducted using these combined values. Had only steamed soil amended with mycorrhizal spores been used, the observed results could have been attributed, at least in part, to varied host affinities for these Glomus species. In nonsterile soil, however, the diversity of fungi present should ensure that the observed responses reflect the mycorrhizal responsiveness of the plants tested.
Mycorrhizal responsiveness was calculated for each plant species as follows. Percentage mycorrhizal responsiveness = [(dry mass mycorrhizal plant - dry mass nonmycorrhizal plant)/dry mass mycorrhizal plant] x 100 (Hetrick, Wilson, and Todd, 1996). Differences between mycorrhizal and nonmycorrhizal plants of the same species were determined using the two-sample t test. Mycorrhizal responsiveness was considered to be significant when the total dry masses of the mycorrhizal and nonmycorrhizal plants were assessed as significantly different as determined by t test. To determine whether mycorrhizal responsiveness of warm-season and cool-season grasses and forbs differed, a two-way analysis of variance (ANOVA, P 
0.05) using Proc GLM (SAS statistical package; SAS, 1988) was performed on treatment means of each plant group (warm- or cool-season grasses, or forbs, and annual vs. perennials) rather than individual species.
Grass and forb species were ranked by peak biomass and flowering time as follows: 1 = early season (April–May); 2 = mid-season (June–July); 3 = late season (August–September). For plant species with flowering periods that extend beyond one portion of the season, the predominant flowering period was designated in the ranking. Relationships between mycorrhizal responsiveness and root colonization or phenology were examined using correlation analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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0.001) responsiveness values (86.5–99.4%) indicate that without the mycorrhizal symbiosis, these grasses failed to grow and often died. Biomass production of warm-season perennial grasses with responsiveness values ranging from 67.9 to 81.7% (P 0.05) was significantly increased by mycorrhizae, however some growth was attained in the absence of the symbiosis. Conversely, biomass production of perennial cool-season C3 grasses was generally not affected by mycorrhizal colonization (Tables 1, 3). In only two of the 14 observed species was the dry mass of the mycorrhizal grasses significantly (P 0.05) improved as compared to the nonmycorrhizal controls, and all of the cool-season grasses tested were able to grow normally in the absence of the symbiosis. One species, Bromus inermus, produced significantly more biomass without, than with, mycorrhizal fungi. As a group, the cool-season grasses showed the greatest interspecific variation in mycorrhizal dependency, compared to warm-season grasses or forbs (Table 3). Annual grasses, both cool- and warm-season, exhibited low responsiveness to mycorrhizal colonization, i.e., there was no significant difference between dry mass production of mycorrhizal and nonmycorrhizal plants (Tables 1, 3).
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0.05). In contrast, the annual or biennial forbs tended to be nonresponsive, with dry mass of only two of 12 species significantly improved by mycorrhizal fungal colonization (Table 2).
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Host plant guilds
When the plant species were assessed as taxonomic, phenologic or physiologic guilds, as opposed to individual species, warm-season grasses and forbs had significantly higher mycorrhizal responsiveness (P 0.0001) and percentage root colonization (P 0.01), as compared to the cool-season grasses. Annual grasses and forbs were significantly less responsive (P < 0.0001) and were less colonized (P < 0.01) than were the perennial grasses and forbs (Table 3).
Mycorrhizal root colonization
All inoculated plants, and plants grown in nonsterile soil, were colonized by mycorrhizal fungi (Tables 1, 2). Plant roots grown in steam-pasteurized soil without mycorrhizal inoculum were not colonized at experimental harvest. Colonization of plants from nonsterile soil treatments ranged from 4 to 29% and were generally lower and more variable than the corresponding values from the inoculated steam-pasteurized soil treatments. Mean responsiveness for the seven inoculated plants did not differ significantly from that of the 14 mycorrhizal (inoculated and nonsterile treatments) plants. Therefore, all reported values are from plants grown in steam-pasteurized soil.
The relationship between responsiveness and root colonization was generally positive. When all nonleguminous plants were analyzed together, root colonization was strongly positively correlated with mycorrhizal responsiveness (P = 0.0002; r = 0.408). When each group (cool- and warm-season grasses and forbs) was assessed individually, the correlation with the cool-season grasses was the strongest (P = 0.0146; r = 0.564) with much lower relationships observed for the forbs (P = 0.0492; r = 0.302) and the warm-season grasses (P = 0.0639; r = 0.433). In contrast, root colonization of perennial legumes showed a significant, but negative, relationship with mycorrhizal responsiveness (P = 0.0001; r = 0.821).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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It has been well documented that morphology of roots is an extremely important factor in determining mycorrhizal responsiveness. Plants with roots that are comparatively thick, with little branching and few or no root hairs tend to show greater positive growth responses to mycorrhizal colonization than plants with fine, highly branched roots and many root hairs (Baylis, 1975; Hetrick, Wilson, and Todd, 1990; Smith and Smith, 1996). The latter type of root system is generally more metabolically costly due to the production and turnover of finer roots and root hairs. Cool-season grasses generally have significantly more primary and secondary roots than warm-season grasses and the diameter of primary, secondary, and tertiary roots of cool-season grasses is significantly smaller than those of warm-season grasses (Hetrick, Wilson, and Leslie, 1991). Hetrick, Wilson, and Leslie (1991) hypothesized that the most important factor determining mycorrhizal responsiveness of cool- and warm-season grasses was, in fact, root morphology. These patterns indicate that carbon allocation to development of a finely branched root system with high root hair density and carbon allocation to mycorrhizal fungi are alternative absorption strategies for acquisition of soil resources.
The only perennial warm-season species in this study that did not show a significant increase in biomass in response to mycorrhizal colonization was Cynodon dactylon. This grass is an introduced species from Africa and is of different origin than that of the other warm-season grasses tested, which are of native tallgrass prairie (Great Plains Flora Association, 1986; Whitson et al., 1992). However, it is likely that the lack of response in C. dactylon is more closely related to the nature of the root system than to origin. C. dactylon is a stoloniferous species with relatively fine, highly branched roots, whereas the native perennial warm-season grasses are characterized by coarse, less highly branched root systems (The Herbarium of Kansas State University, HB.KSC; Whitson et al., 1992).
All annual grasses and annual and biennial forbs examined in this study showed low mycorrhizal responsiveness. This is not surprising, as it has been estimated that only 15% of all annual Monocotyledonae form a mycorrhizal association, as compared to 85% of perennials (Trappe, 1987). The annuals studied in this experiment are considered facultative mycotrophs, i.e., although these species were colonized by mycorrhizal fungi, biomass production was unaffected. These grasses and forbs are typically early invaders or species that thrive in continuously disturbed sites in the absence of strong competition. While extremely harsh or severely disturbed sites are often colonized by nonmycotrophic species, ruderal plant species that colonize frequently disturbed sites are often facultative mycotrophs (Miller, 1987; Francis and Read, 1994). The facultative mycorrhizal status of these annual species is possibly related to the type of disturbance regime to which these plants are exposed and may confer a competitive advantage to these species, as compared to nonmycotrophic species. Maintaining low levels of colonization may allow benefit during periods of nutritional stress or during certain life history stages such as seedling establishment or flowering. Previous field studies in tallgrass prairie have shown that, for several grass and forb hosts, benefit from mycorrhizal symbiosis varies significantly among life history stages within species (Hartnett et al., 1994). Perennials, in contrast, must develop long-term strategies for competition for limited nutrients if they are to survive over extended periods. Allocation of carbon to support mycorrhizal associations is presumably one such strategy for the warm-season grasses and perennial forbs.
In contrast to the perennial grasses, the relationship between phenology and mycorrhizal responsiveness of forbs was not highly significant (P = 0.1007). The majority of perennial forbs in this study increased significantly in biomass production when colonized by mycorrhizal fungi, regardless of flowering time. The forb species in this study that were responsive (P 0.05) were generally late-successional species that compose undisturbed, stable tallgrass prairie ecosystems. These species tend to disappear with disturbance. As observed in other ecosystems, mycorrhizal benefit is highest in plants in undisturbed, stable sites (Janos, 1980; Brundrett and Kendrick, 1988), while disturbance can limit mycorrhizal symbiosis and its contribution to plants (Miller, 1987; Evans and Miller, 1988). The forb species that were not significantly responsive in this study are generally less abundant in tallgrass prairie than those with high responsiveness or are characteristic of disturbed prairie sites. These plants are facultative mycotrophs, which presumably have an extensive enough root system such that, in the native prairie soil tested, nutrient demand was accomplished without the mycorrhizal symbiosis.
Fourteen of the 15 perennial legumes were highly responsive to mycorrhizal inoculation. This high mycorrhizal dependency of legumes probably reflects the relatively high P demand of the N2-fixation process (Azcon-Aguilar and Barea, 1992). In addition, nutrients other than P, such as Zn, Cu, Mo, and Ca can affect the infectivity or symbiotic effectiveness of Rhizobium, and the enhanced uptake of these elements by the mycorrhizae may also be important (Munns and Mosse, 1980; Hayman, 1986; O'Hara, Boonkerd, and Dilworth, 1988). The negative relationship between root colonization and mycorrhizal dependence (or plant responsiveness) in the legumes was unexpected, due to the well-established importance of AM fungi for nodule formation by Rhizobium and nitrogen fixation (Hayman and Mosse, 1979; Robson, O'Hara, and Abbott, 1981; Barea and Azcon-Aguilar, 1983; see Azcon-Aguilar and Barea, 1992). However, it has previously been observed in Pisum sativum L. that mycorrhizal colonization level did not reflect benefit (Estaun, Calvet, and Hayman, 1987) or was negatively correlated with mycorrhizal dependencies of several varieties (Martensson and Rydberg, 1994). The negative correlation observed in this study is generally a reflection of low levels of colonization in highly dependent species. Therefore, it is possible that those species that depend on the symbiosis have very efficient phosphorus uptake, involving enzymes with a high affinity for phosphorus, and thus, require a lower level of fungal colonization (Jakobsen, 1991). The reasons for species-specific responses to AM fungal colonization and plant benefit are probably mediated by a complex combination of plant and fungal signals based on genetically controlled substances (Gianinazzi-Pearson et al., 1991).
The significant correlation between root colonization levels and mycorrhizal dependence of the nonleguminous species may indicate that plants that do not rely on the symbiosis regulate mycorrhizal colonization in some way and, thus, control carbon expenditure on the fungus. As was observed in this study, cool-season grasses were significantly less responsive to the symbiosis than were the warm-season grasses or forbs and were also less colonized by the fungi. Based on the premise that plants optimize carbon expenditure to avoid limiting any one resource (e.g., nitrogen, carbon, or phosphorus) more than another (Bloom, Chapin, and Mooney, 1985), it is logical that species of low mycorrhizal dependencies would limit carbon expenditure for mycorrhizal colonization more than species highly dependent on the symbiosis. Fitter and Merryweather (1992) suggest that the level of mycorrhizal colonization within roots is an evolved character that plants may regulate in relation to the benefit they receive. However, since AM fungi form an association with 80% of all vascular plants (Harley and Harley, 1987) and even plants of low mycorrhizal dependencies have apparently not evolved any resistance to AM fungi, it may be argued that there must be some alternative benefit conferred by the association with these species.
Historically, the benefit of the symbiosis for the plant has been considered to be improved nutrient supply, in particular improved uptake of phosphorus by mycorrhizal roots as compared to nonmycorrhizal roots, especially in nutrient-poor soils. However, recent studies suggest that in natural ecosystems these fungi may have other beneficial effects on plants beyond improved plant phosphorus nutrition (see Newsham, Fitter, and Watkinson, 1995a). For example, plant hormone levels as well as plant architecture may be altered (Allen, 1985). AM fungi may affect phenotypic characteristics of grasses such as stolon branching and stolon length (Streitwolf-Engle et al., 1997), increase drought tolerance or improve water uptake (Allen and Allen, 1986; Lapointe and Molard, 1997), improve defense against herbivores (Gange and West, 1994), and increase resistance to root pathogenic fungi (Newsham, Fitter, and Watkinson, 1995b). Clearly, the importance of this symbiosis cannot be inferred solely on assessment of biomass increases of mycorrhizal plants, as compared to nonmycorrhizal plants. However, to elucidate the role played by mycorrhizal fungi in plant communities, we must first build sufficient information to allow for the formation of general theories. The present study elucidates the pattern of responses of tallgrass prairie grasses and forbs to mycorrhizal colonization in relation to life histories and morphological traits, onto which community-level experiments may build, in order to discern the significance of AM fungi in mediating ecological interactions.
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FOOTNOTES |
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