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2W. K. Kellogg Biological Station, Michigan State University, 3700 East Gull Lake Drive, Hickory Corners, Michigan 49060 USA; 3Department of Zoology and Program in Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, Michigan 48823 USA; and 4Department of Botany and Plant Pathology and Program in Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, Michigan 48823 USA
Received for publication March 9, 2000. Accepted for publication July 5, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Danthonia spicata • environmental variability • plant–fungal interactions • spatial heterogeneity • symbiosis
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Dobson and Crawley, 1997
; Thrall and Burdon, 1997
; Clay and Holah, 1999
). Many plant species, particularly grasses, commonly form symbiotic associations with epiphytic or endophytic fungi that have the potential to strongly alter a host plant's morphology, physiology, and response to environmental conditions (e.g., Bacon et al., 1986
; Read and Camp, 1986
; Belesky et al., 1987
; Carroll, 1988
; Marks and Clay, 1990
). These fungi can be beneficial to their host plant in some environments, but may be parasitic in others (Clay, 1990a
).
Nutrient requirements of active, sometimes toxin-producing, fungal biomass may outstrip nutrient availability when nutrients available to a host are very low, causing otherwise advantageous fungal infections to be disadvantageous (Bacon, 1993
). Soil fertility-dependent growth advantages of fungal infection have been demonstrated for endophyte-infected Lolium perenne and Festuca arundinacea (Cheplick, Clay, and Marks, 1989
; Marks and Clay, 1990
; Cheplick, 1997
). In both of these species, the growth advantage of infected plants was either small or negative at the lowest fertility levels and increased with fertility in the greenhouse.
In most plant species that have epiphytic or endophytic fungal associations, both infected and uninfected individuals occur within and among populations (Bradshaw, 1959
; Clay, 1990a
). In mixed populations, infected and uninfected plants may be patchily distributed, with some areas having predominantly infected and other areas predominantly uninfected plants. The distribution of infected plants may have substantial impacts on population and community composition and interactions (Dobson and Crawley, 1994
; Clay and Holah, 1999
).
Soil resources also can vary spatially within and among plant communities over a range of scales (Jackson and Caldwell, 1993
; Robertson and Gross, 1994
; Gross, Pregitzer, and Burton, 1995
). If infected and uninfected plants respond differently to soil conditions that are patchily distributed, then the spatial distribution of infected individuals in a population might correspond to patches of environmental conditions that are favorable to infected plants.
To determine whether patchy distributions of soil nitrogen and percentage water were related to observed spatial variation in a plant–fungal symbiosis, we examined the correlation between Atkinsonella hypoxylon infection and soil resource (nitrogen and moisture) in three populations of Danthonia spicata in southwestern Michigan. We conducted a parallel greenhouse experiment to test whether growth and survival of D. spicata plants infected by A. hypoxylon differed from that of uninfected plants under high and low levels of moisture and fertility. A common garden planting of infected and uninfected culms was used to determine how the growth and survival of infected and uninfected plants differed in the field.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Throughout much of its range, D. spicata is infected by the epiphytic fungus Atkinsonella hypoxylon (Balansiae), which is specific to the genus Danthonia (Clay, 1994
). Spread of A. hypoxylon in D. spicata populations occurs asexually through seedlings from infected plants and sexually through dissemination of ascospores, but infection of previously healthy plants is very rarely observed in the field (Kover, Thomas, and Clay, 1997
). Uninfected D. spicata produce two flower types. Potentially outcrossed, wind-pollinated chasmogamous flowers are produced at the tip of the reproductive stalk. Obligately self-fertilized cleistogamous flowers are produced in the axils of the leaf sheaths along the reproductive stalk. In infected plants, a fungal sclerotium, or "choke," is produced at the initiation of host plant flowering and causes abortion of all but a few infected cleistogamous seeds at the base of the much-reduced reproductive stalk. Plants infected by A. hypoxylon often have higher growth rates than uninfected plants and so this symbiosis is generally considered mutualistic (Diehl, 1950
; Clay, 1984, 1990a
). The proportion of plants infected by A. hypoxylon varies among populations in Michigan. Some populations have a high proportion of plants infected by A. hypoxylon (>75%; Leuchtmann and Clay, 1989
), but others are entirely free of infection (Scheiner, 1989
; McCormick, 1999
). The three populations of D. spicata we examined in this study were all partially infected by A. hypoxylon and growing in low-productivity old fields that had been abandoned at least 45 yr ago. Plant communities at these sites were dominated by herbaceous, perennial species, especially Andropogon virginicus, Schizachirium scoparium, and Carex spp. Two populations (L1 and L2) were located near the W. K. Kellogg Biological Station (KBS) of Michigan State University in Hickory Corners, Michigan, USA. The third population (R) was located in the Rose Lake Wildlife Research Area near East Lansing, Michigan, USA.
In each population, we measured plant density (number of D. spicata plants per square meter) and percentage infection along two randomly located belt transects (12 x 0.25 m). We also established a 4 x 6 m permanent plot where we quantified soil moisture and nitrogen supply. Seventy soil samples were taken from each plot, using a 10 cm deep, 2.5 cm diameter soil core, in a stratified, nested sampling design. At each location where a soil core was removed we inserted an ion exchange resin bag (Dowex MR-3, Sigma, St. Louis, Missouri, USA) and buried it under 5 cm of soil to measure the relative supply of ammonia–nitrogen in the soil. Soil moisture and relative supply of ammonia were chosen to characterize environmental quality because these resources often limit plant growth in the dry, nutrient-poor environments where D. spicata occurs. We also sampled nitrate-nitrogen in these locations, but nitrate levels were low and were not consistent among years in these sites (McCormick, 1999
). Because relative nitrate-nitrogen supply was not spatially or temporally consistent, we felt that it would not be a reliable determinant of microhabitat conditions related to infection distribution.
We measured soil moisture gravimetrically in all three populations in mid-May 1998, corresponding to the time of maximum growth by D. spicata. The relative ammonia supply rate was estimated in all three populations for 4 mo after sampling for infection (June 1997–October 1997). Soil moisture and ammonia supply were also measured at other times using identical methods (see McCormick, 1999
), but these other measurements were used only to assess temporal consistency in infected and uninfected quadrats. We used 1998 measures of soil moisture and 1997 measures of ammonia supply to characterize the spatial pattern of soil resources in each sites. These sampling periods were closest in time to when we measured the distribution of infected and uninfected plants in these populations.
To determine whether the pattern of infection in each population was correlated with soil moisture or ammonia supply, we surveyed the incidence of A. hypoxylon infection in each population after the plants had bolted in June 1997. Infected plants are easily distinguished from uninfected plants at this stage by the presence of a gray fungal sclerotium ("choke") on each aborted reproductive stalk. We randomly selected 75 quadrats (25 x 25 cm) from within each of our three permanent plots (4 x 6 m; 384 quadrats) to survey for incidence of infection. This small quadrat size was chosen to allow assessment of plant density without integrating across substantial variation in spatially heterogeneous environmental conditions. In each quadrat, we noted the number and location of infected and uninfected D. spicata plants. We used semivariance analysis and kriging interpolation (GS+ version 3.11.6. 1999, Gamma Design Software, Plainwell, Michigan, USA) to estimate percentage water and ammonia supply for the center of each quadrat that we sampled for infection incidence. Kriging interpolation uses the variance–distance relationship, summarized in a semivariogram, to assign weights to sample points as a function of their distance from a point for which an estimate is desired (Robertson and Gross, 1994
).
We used logistic regression (Systat 8.0 for Windows, Systat, 1998, Evanston, Illinois, USA) to analyze the distribution of infected quadrats over the range of soil moisture and ammonia conditions across the three populations. We designated a quadrat as infected if it contained at least one infected plant. Because of the possible confounding of current spatial structure of infection with point of infection introduction or other processes within a population, we can only draw conclusions about the association between environmental factors and infection incidence across all three populations. A significant population effect in the regression would indicate that patterns were not the same across the three populations.
We also examined whether there were indirect environmental effects on the distribution of infection acting through plant density. Favorable environments might promote higher plant densities and plant density could affect contagious spread of the fungus. To evaluate this effect, we estimated plant density across all quadrats and used a t test to compare the average plant density in infected and uninfected quadrats.
We conducted a 2 x 2 factorial greenhouse experiment in which watering regime and fertilizer were manipulated to determine whether variation in soil fertility and moisture levels could affect performance and thus influence the differential distribution of infected and uninfected plants in the field. We collected cleistogamous seeds from 21 infected and 28 uninfected individuals selected randomly from two D. spicata populations. We collected seeds from Population L1, where we had conducted the field pattern survey, and a second, unsurveyed, population located at the Lux Arbor Reserve of KBS. The herbaceous vegetation at this site was similar to L1 and L2, except for the presence of more woody species. Seedlings from these two populations had similar growth and survival in the greenhouse and thus were combined in all analyses.
We surface sterilized infected and uninfected seeds with bleach and ethanol according to the methods of Leuchtmann and Clay (1988)
and nicked each with a sterile razor blade to stimulate germination. Seeds were then placed in moist, sterile sand in a growth chamber with 14-h days at 29°C and 10-h nights at 24°C. Of the 21 infected and 28 uninfected plants from which we collected seeds, 12 infected and 17 uninfected plants had sufficient seed germination for experimental replication. Nine days after being sown in the sterile sand, we randomly assigned the 109 seedlings from infected and uninfected families to four treatment groups and planted them into random positions in 70-hole conetainers (each hole was 2.5 cm diameter x 15 cm deep) filled with sterile silica sand. Each infected family was represented by nine or ten seedlings, two in each treatment with the additional one or two seedlings randomly assigned to treatments. Each uninfected family was represented by six or seven seedlings, one per treatment with the other two or three randomly assigned to treatments. The plants were placed in the greenhouse under ambient light. After a 4-d stabilization period with daily watering to saturation, we established the four treatments (2 x 2 factorial) in which fertility and watering regime were varied. Seedlings from each infected and uninfected family were grown under all combinations of high and low fertilizer and high and low watering.
The moisture and fertility levels used in the experiment were chosen to represent the range of conditions observed in the field, without imposing extremely high mortality. Fertilizer levels consisted of 0.015 g/L (low fertility) or 0.500 g/L (high fertility) of Peter's Peat-lite Special Fertilizer (20-10-20) applied at a rate of 4.5 mL per planting location 2–3 times per week. The nitrogen levels in these fertility treatments corresponded to nitrogen mineralization rates in field incubations of 0.01 and 0.45 mg N·g dry soil-1·d-1, the approximate range of fertility found in field populations of D. spicata (McCormick, 1999
). Plants in high-moisture treatments were watered daily, while plants in the low-moisture treatments were watered every second or third day, when approximately half of the plants showed leaf rolling, symptomatic of water stress. Average greenhouse temperatures were 
30°C from June to September and 24°C from October to April with ambient light. The positions of the 70-hole conetainers on the greenhouse bench were randomly rotated each week to minimize location effects.
We monitored plants monthly over 9 mo for size and survival, using the number of living leaves as our measure of plant size. After 6 mo, plants in high-fertility treatments were sufficiently large that they began to shade plants in adjacent locations. Therefore, we transplanted plants in these treatments into staggered locations in 70-hole conetainers, with one empty cell on all sides to prevent shading.
Plant growth data were log transformed to minimize heterogeneous variances produced by substantial growth differences between high- and low-fertility treatments. Transformed data were analyzed using a repeated measures MANOVA (Systat 8.0 for Windows, Systat, 1998, Evanston, Illinois, USA). We also calculated performance by using the percentage survival as a weight on the size of each plant in each treatment (log number of leaves). We compared seedling performance among treatments over the experimental period using a repeated measures ANOVA.
To assess differences in growth of infected and uninfected plants under field conditions, we established a common garden adjacent to our permanent plot in Population L1. We collected nine uninfected and three infected adult D. spicata plants from field Populations L1 and L2 in April 1995. The plants were divided into culms and each culm was planted into a 10 x 10 cm pot filled with sterile sand in the greenhouse. Culms that produced vegetative shoots were again divided into individual culms and planted into new 10 x 10 cm pots in May 1995. The culms were grown in the greenhouse without fertilizer until June 1995, when we used them to establish the common garden experiment.
We established a common garden by tilling a 2 x 2 m area near Population L1. We planted individual culms of each genotype (individual parent) into four randomly selected locations on a 10 x 10 cm grid established in the central 1 x 1 m of the tilled area. Remaining planting locations in the grid were occupied by D. spicata culms from another experiment. We planted additional culms around the perimeter of the common garden to avoid edge effects on the study plants.
Culms were grown in the common garden for 2 yr (June 1995–1997) and then harvested for determination of aboveground biomass. At the time of harvest, plants were still separated by at least 5 cm of open ground. We measured final plant size by counting the number of tillers, leaves, and inflorescences produced. We also measured initial size, but its effect on final size was not significant (Pearson correlation, P > 0.3), so we only considered final size in these analyses. All harvested material was dried at 45°C for 48 h and then weighed to the nearest 0.01 g. We ground subsamples of leaf material from each culm to determine tissue nitrogen concentration. We also ground reproductive stalks, with seeds removed, from all infected culms and from three randomly selected uninfected culms from different parents. For each infected reproductive stalk we included the fungal sclerotium, which was intimately associated with the stalk, in tissue to be ground so we could assess the overall nitrogen content of the reproductive stalk. Percentage nitrogen content of this tissue was analyzed using an elemental analyzer (Nitrogen Analyser 1500 Series 2, 1990, Carlo-Erba Instruments, Milan, Italy).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Several studies that have addressed the role of fungal epi- and endophytic fungi in altering growth patterns and resource requirements of infected host plants have also found that the effect of fungal infection on a host plant varies with environmental conditions (e.g., Cheplick, Clay, and Marks, 1989
; Bacon, 1993
). Epi- and endophytic fungal symbionts are often advantageous to plant growth in high-nutrient environments where they may increase plant growth, but can become disadvantageous in low-nutrient environments where increased nutrient demands of infected plants preclude increased host growth rates (e.g., Bacon, 1993
; Latch, 1993
). While acknowledging the impact of environmental conditions on host plant performance, these studies have rarely assessed the importance of heterogeneous environmental conditions in structuring plant–fungal interactions (but see Thrall and Burdon, 1997
). The uniqueness of our study is that we linked growth differences in the greenhouse and common garden to the distribution of fungal infection in natural field populations.
Studies in Indiana and North Carolina have found that infected D. spicata plants consistently grew better than uninfected plants in both field plantings and in the greenhouse (Clay, 1984
; Kelley and Clay, 1987
; Leuchtmann and Clay, 1988
). In contrast, we found that although infected plants were common in areas of the field with high ammonia supply, areas with high soil moisture and low ammonia supply had very few infected plants. Across all three field sites, occurrence of A. hypoxylon was unrelated to D. spicata density, suggesting that the distribution of infection in these sites cannot be explained by increased potential for infectious spread in fertile areas as a result of higher plant density. In two of three field populations, areas where D. spicata was infected by A. hypoxylon had lower soil moisture and higher ammonia than areas with only uninfected plants. This result suggests that in these Michigan sites, soil resource heterogeneity may influence the distribution of A. hypoxylon infected D. spicata plants. It also implies that the impact of A. hypoxylon on D. spicata depends on environmental conditions at the microsite where the plant is located.
One possible explanation for differences between our results and those in Indiana and North Carolina is that all three field sites we surveyed have low-fertility soils and the substrate we used to grow plants in the greenhouse (silica sand) was extremely nutrient poor compared to the substrates used in other experiments (standard greenhouse soil; K. Clay, personal communication). It also suggests that the consistent performance advantage of infected over uninfected plants observed in previous studies (Clay, 1984
; Kelley and Clay, 1987
; Leuchtmann and Clay, 1988
) may, in part, be due to the higher fertility of the medium used in their greenhouse studies.
In our three field populations, D. spicata occurred primarily in areas of the field where soil moisture generally was 5–12% and was rarely found in sites where soil moisture was >20%. Moister areas of these fields were dominated by Polytricum sp., Rubus sp., and other grasses, especially Poa compressa and P. pratensis (McCormick, unpublished data), which may have excluded D. spicata (Kelley and Clay, 1987
). Soil moisture in our low-frequency watering treatments was maintained at 6%, while in the high frequency watering treatments soil moisture was 25%. Consequently, responses of D. spicata to our low-moisture greenhouse treatments are most relevant to distribution of infected and uninfected plants in our three field populations. In the low-moisture, low-fertility treatment we found that infected plants performed less well than uninfected plants, but in the low-moisture, high-fertility treatment infected and uninfected plants performed equally well.
A possible reason for the poor performance of infected plants in the low-fertility, low-moisture treatment is suggested by the differences in tissue nitrogen concentration we measured in infected and uninfected plants grown in the common garden experiment. Although infected reproductive stalks and vegetative parts both had higher nitrogen concentration than corresponding parts of uninfected plants, the nitrogen difference for reproductive stalks was substantially greater than for vegetative tissue. Infected reproductive stalks included fungal sclerotia, so they had a substantially higher proportion of fungal tissue relative to plant tissue than vegetative parts did. Hence, the higher tissue nitrogen in infected plants was most likely a result of high nitrogen concentrations in fungal tissue, rather than increased nitrogen in plant tissues. Higher nitrogen concentration in fungal biomass may put a high nitrogen acquisition demand on infected plants. An increased nitrogen demand by A. hypoxylon may have caused infected plants to grow less well than uninfected plants in the low-fertility, low-moisture treatment in our greenhouse experiment and could limit infected plants to field locations with higher relative ammonia supply. However, other studies have shown that D. spicata is a poor competitor for light with other grass species (Kelley and Clay, 1987
), suggesting that competition with plant species that are better light competitors might exclude D. spicata from more fertile areas of a field. Thus, light competition together with the high nitrogen demand of infection may limit infected D. spicata to high nitrogen, low-moisture patches in the field.
Infected D. spicata might also be especially sensitive to nitrogen availability if infected individuals are less infected by mycorrhizal fungi than uninfected plants, as has been shown for endophyte-infected fescue by Chu-chou et al. (1992)
. Danthonia spicata are considered to be obligately mycorrhizal (Darbyshire and Cayouette, 1989
) and decreased access to mycorrhizal nitrogen and other nutrients could also limit D. spicata infected by A. hypoxylon to higher fertility locations than occupied by uninfected plants. It is also possible that differences in root structure could allow infected plants greater access to soil nitrogen, as has been shown for some endophyte-infected grasses (e.g., Richardson et al., 1999
). However, this effect has not been shown for epiphyte-infected plants and preliminary studies indicate that neither mycorrhizal colonization nor root structure differs substantially between infected and uninfected D. spicata plants (McCormick, unpublished data).
Infected D. spicata plants are common and often dominate low-moisture, high-ammonia areas of fields in southern Michigan. However, in the greenhouse, infected plants did not have a clear performance advantage under these, or any, conditions. A high incidence of infection in some areas of the field, despite no indication of advantage in the greenhouse or common garden, suggests that other factors may be influencing the field distribution of A. hypoxylon-infected D. spicata in these sites. Competition (intra- and interspecific) and herbivory were not included in our greenhouse study, but could influence the distribution of infected plants in the field. Kelley and Clay (1987)
found that infected D. spicata were better interspecific competitors than uninfected D. spicata. Infected plants in our common garden study did not differ from uninfected plants in total biomass, but they did have greater vegetative biomass. Weeding and spacing of plants in the common garden precluded most competition, but greater allocation to vegetative components (albeit at the expense of seed production) could increase the competitive ability of infected plants in field environments where interaction with other plants is common. Further, such increased allocation to vegetative components may explain the increased competitive ability found by Kelley and Clay (1987)
.
Several studies have shown that infected plants are less susceptible to herbivory (e.g., Bacon et al., 1986
; Read and Camp, 1986
; Clay, Marks, and Cheplick, 1993
). We saw little evidence of herbivory in our common garden study even though herbivores (e.g., rabbits, deer, mice) were common in this field and were not excluded from the plots. Increased competitive ability or herbivory resistance could convey a performance advantage to infected plants in the field. Thus, biotic components of the field environment may convert the D. spicata–A. hypoxylon relationship from parasitic or mutualistic (as in our greenhouse study) to beneficial in some environments.
If a symbiotic relationship can change from parasitic to beneficial as a function of environmental conditions, as seems to be the case for the D. spicata–A. hypoxylon symbiosis and has been shown for many mycorrhizal associations (Johnson, Graham, and Smith, 1997
), then environmental conditions can influence the distribution of infected and uninfected plants in a population. Depending on the range of conditions present in a site and the extent of spatial structuring, infected and uninfected plants could be either interspersed (as in Population R) or distributed in relatively discrete patches (as in Populations L1 and L2). If infected plants have a higher nitrogen demand than uninfected plants, as our observation of tissue nitrogen concentration suggests, then an increased demand for nitrogen to support fungal tissue may cause the exclusion of infected plants from dry, low-fertility field locations.
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FOOTNOTES |
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5 Author for correspondence, current address: Smithsonian Environmental Research Center, P.O. Box 28, Edgewater, Maryland 21037 USA.
6 Current address: Department of Botany, Duke University, Durham, North Carolina 27708 USA.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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———, P. C. Lyons, J. K. Porter, and J. D. Robbins. 1986 Ergot toxicity from endophyte-infected grasses: a review. Agronomy Journal 78: 106–116
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