The effect of mycorrhizae on plant growth and reproduction varies with soil phosphorus and developmental stage.
|Abstract:||Determining the impact of both environmental variation and developmental stage on plant-mycorrhizal associations is important, as both can shift the association along the mutualism-parasitism continuum. This study examines the effect of phosphorus level on the response of Allium vineale to mycorrhizae across all plant life stages, including plant fecundity and the relative allocation of resources to three different reproductive modes (flowers, asexual underground offsets, and asexual aerial bulbils). For A. vineale, the impact of mycorrhizae varies significantly with life stage, as an early growth depression at 1 mo was reversed by 15 mo, resulting in mycorrhizal plants having larger bulbs over all P levels and producing more bulbils and larger offsets than nonmycorrhizal plants at lower P levels. However the presence of mycorrhizae did not affect the relative allocation of resources among the three reproductive modes. These results emphasize the importance of long-term studies of plant-mycorrhizal interactions that include fecundity estimates. In addition, they indicate that spatial variation in nutrient availability in the field has the potential to shift the overall effect of mycorrhizae from beneficial to neutral, with greater benefits found in sites with lower phosphorus levels.|
Soils (Phosphorus content)
|Author:||Ronsheim, Margaret L.|
|Publication:||Name: The American Midland Naturalist Publisher: University of Notre Dame, Department of Biological Sciences Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Earth sciences Copyright: COPYRIGHT 2012 University of Notre Dame, Department of Biological Sciences ISSN: 0003-0031|
|Issue:||Date: Jan, 2012 Source Volume: 167 Source Issue: 1|
|Topic:||Computer Subject: Company growth|
|Organization:||Organization: Soil Science Society of America|
The association between mycorrhizal fungi and plant roots was important in the evolution of land plants (Brundrett, 2002) and currently occurs in at least 80% of all plant species (Smith and Read, 1997). Colonization by arbuscular mycorrhizal (AM) fungi can provide multiple functions, such as increased nutrient uptake, drought tolerance, and resistance to pathogens (Newsham et al., 1995). Whereas many studies have shown that AM fungi can increase plant growth rates, it is widely recognized that there is considerable variation in response to colonization among plant species (Hart and Klironomos, 2002; Jones and Smith, 2004). This variation in response has been ascribed to a range of causes, including abiotic and biotic environmental factors, differential effects of colonization over the life cycle of the plant, and specificity in the association between the fungal-plant partners (Johnson et al., 1997; Jones and Smith, 2004).
Environmental factors such as light and nutrient availability may shift the plant-mycorrhizal balance from beneficial, to neutral, or even negative (Johnson et al., 1997). For example, under high phosphorus conditions plant biomass may be reduced in the presence of mycorrhizal fungi (e.g., Buwalda and Goh, 1982; Peng et al., 1993; Olsen et al., 1999; see Smith and Smith, 1996 for a review) as the fungus may continue to draw carbohydrates from the plant, despite the fact that the plant can obtain P directly from the soil. In addition, whereas plants often show the greatest positive growth response at low phosphorus conditions, some studies have found the opposite (e.g., Li et al., 2005).
The plant-mycorrhizal interaction may also shift between a mutualistic and parasitic interaction depending on the life stage of the plant. When plants are young, the cost of the carbohydrate drain by the fungus may be greater than the benefit received by the plant from increased phosphorus availability, resulting in growth depression (e.g., Bethlenfalvay et al., 1982; Koide, 1985). Age of the plant was also important for Hyacinthoides non- scripta, as the mycorrhizal associated shifted from facultative to obligate with plant age (Merryweather and Fitter, 1995). The relative cost-benefit of the association may also shift seasonally, as the mycorrhizae are costly to Erythronium americanum in the fall but beneficial in the spring (Lapointe and Molard, 1997). These shifts among parasitic, neutral, and mutualistic interactions over time indicate the importance of longer term experiments that incorporate all stages of the plant life cycle. Incorporating reproductive output and fitness estimates is of particular importance for understanding the ecological and evolutionary implications of plant-mycorrhizal associations.
Relatively few studies have included plant reproductive output, particularly for nonagricultural species (see Koide, 2000; Varga, 2010 for reviews). Although increases in plant size often result in greater fecundity, the effects are not consistent (Jones and Smith, 2004); and extrapolating linearly from short term growth experiments could lead to incorrect assumptions about future fecundity. In addition, whereas the presence of mycorrhizae can increase seed output, the effect on reproduction can vary with environment (e.g., Carey et al., 1992), plant genotype (e.g., Bryla and Koide, 1990), and plant density (e.g., Koide et al., 1994). For species that can reproduce vegetatively, mycorrhizae have the potential to significantly alter allocation to clonal growth (e.g., Streitwolf-Engle et al., 1997) and to shift relative resource allocation between vegetative propagules and flowers (e.g., Scagel and Schreiner, 2006) thus further complicating assumptions about mycorrhizal effects on fitness. If mycorrhizae alter the allocation patterns to different reproductive modes, it could have important implications for the genetic and spatial structure of the population.
In this study I investigated the effect of phosphorus level on the response of Allium vineale (wild garlic or onion grass) to mycorrhizal colonization across all life stages of the plant. Specifically, I asked how variation in P level affects the plant-fungal association, including affects on overall plant size, resource allocation patterns, and fecundity. By using P levels within the same range found in the field from which the plants originated, the responses measured here give an indication of whether variation in nutrient availability in the field could cause the effect of mycorrhizae to shift along the mutualistic-parasitic continuum (Johnson et al., 1997). Allium vineale reproduces via three kinds of propagules, sexually produced seeds, underground asexual offsets, and aerial asexual bulbils; thus I was able to test for shifts in the allocation of resources to different reproductive modes as well as overall effects of mycorrhizal colonization on plant fecundity.
Study species and site description.--Allium vineale L. (Liliaceae) is a naturalized introduced species commonly found in fields and along roadsides from Michigan to Georgia (Radford et al., 1968). It is a winter perennial that sprouts in early autumn, grows throughout the winter and dies back in Jun. Plants produce a new bulb each year, as well as up to three types of propagules. Offsets are underground asexual propagules analogous to the cloves of domesticated garlic. They are the largest of the propagule types (mean mass = 217 mg, ranging from 40-600 mg), and, unlike the bulb that resprouts in the fall, they may remain dormant in the soil for up to 5 y (Stritzke and Peters, 1972). As the leaves die back in early summer, A. vineale produces a scape with an inflorescence containing bulbils (asexual reproduction), flowers (sexual reproduction), or a combination of both. Seeds and bulbils ripen in early fall and disperse to a mean distance of 34 cm from the parent (Ronsheim, 1994). Seeds weigh approximately 1 mg each, whereas bulbils range from 5-60 mg (mean mass = 19.8 mg; Ronsheim, 1996). A. vineale roots are coarse (0.25-1 mm in diameter), rarely branched, and colonized by arbuscular mycorrhizal (AM) fungi in the field (Richens, 1947; M. Ronsheim, pers. obs.).
The field site is on the Vassar College Ecological Preserve in Dutchess County, New York. The field was previously used for agriculture but was abandoned in the late 1950s and is currently maintained by mowing every few years. It is dominated by Bromus inermis Leyss., Galium mollugo L., Poa pratensis L., Comus racemosa Lam., Rhus radicans L., and Solidago sp. Allium vineale is a common species (reproductive individuals were present in 21 out of 49 one [m.sup.2] quadrats sampled). P availability ranges from 39-155 [micro]g x [g.sup-1] readily extractable P, with a mean of 95.4 [micro]g x g-1 dw (all soil analyses conducted by A&L Eastern Agricultural Laboratories, Inc., Richmond VA, using methods from A. L. Page, 1982, see below).
Experimental design.--Allium vineale bulbils were collected from the field and planted in pots either with or without mycorrhizae at six levels of P fertilization. Bulbils were collected from 13 parents and randomly assigned to each treatment. Mycorrhizal pots were inoculated with roots of Plantago lanceolata L. and Bromus inermis collected from the field site that were heavily colonized by AM fungi. Because A. vineale plants in the field are dormant and have little active root material when the bulbils are mature, roots from these two co-occurring species were used; and thus the specific mycorrhizae present may be different from those found on A. vineale roots in the field. The roots were surface sterilized in a 5% bleach solution, chopped into 1-2 cm lengths, thoroughly mixed, and then approximately 20 mg (wet mass) was added to the soil. The bulbils were then weighed and planted slightly above the inoculum.
Plants were fertilized with Hoagland's solution modified to contain one of six different P concentrations (0, 50, 100, 150, 200, or 250 [micro]g x L P) once a week for 6 wk (19 replicates per treatment, [n.sub.tota] = 228). Twenty-five ml of fertilizer were added during the first two fertilizations and 20 ml during the remaining four fertilizations. The soil was a 1:1 mixture by volume of heat pasteurized field soil and sterile sand to improve drainage. At the start of the experiment the soil mixture had a pH of 5.5, with 1.8% organic matter and 91 [micro]g x g-1 dw readily available P (all soil analyses conducted by A&L Eastern Agricultural Laboratories, Inc., Richmond VA, using methods from A. L. Page, 1982). Soil pH was measured at 1:1 soil to water solution, percent organic matter was determined on dried screened soil, and total available P was determined using the Bray P-1 procedure. The pH of the soil used in this experiment is slightly higher than the original field soil (pH 5.2) and the soil organic matter is lower than the original field soil (4.0% organic matter). Soil was collected from several pots from each P treatment at the end of the experiment, and the level of readily extractable P across the six treatments was 89, 118, 138, 172, 201, and 193 [micro]g x g-1 dw respectively. The lack of difference between the last two P treatments may be due to the high sand content of the soil resulting in the leaching out of the additional added P.
Because Allium vineale roots produce few branches and tend to grow vertically in the soil, circular pots 3.8 cm in diameter, and 21 cm deep were used (Conetainers, Stuewe, and Sons, Inc., Corvallis, Oregon, USA). The plants were randomly arranged within trays and placed in a growth chamber set to average Oct. temperature and light conditions (12.5 h daylight, daytime T = 16 C, nighttime T = 7 C).
The first of three harvests was done 1 mo after planting (n = 72), the second after 6 mo (n = 62), and the final harvest was done after 15 mo (n = 70). Of the original 228 bulbils planted, 24 did not germinate and were not included in the analyses. Failure to germinate was random across treatments. The dry mass of shoots and roots and the percent AM fungal colonization was determined at 1 and 6 too. For those plants that had a subset of their roots examined for AM fungal colonization rates (all mycorrhizal plants and a subset of nonmycorrhizal plants), the total dry root mass was estimated using a regression of the wet and dry root mass. Percent AM fungi colonization was determined using the gridline intersect method described by Giovannetti and Mosse (1980) on roots stained using the procedure described by Grace and Stribley (1991). No AM fungal colonization was observed in plants from the noninoculated treatment.
The final harvest (15 mo) was done when the plants entered dormancy and all their roots and leaves had died back, leaving only underground bulbs, offsets and aerial reproductive stalks. Total dry biomass, bulb mass, and the number and mass of offsets, bulbils and flowers were recorded.
Data analysis.--Data were analyzed using the GLM procedure in SAS (SAS, 1986) with initial mass of the bulbils as a covariate. Response variables reported here include total biomass at 1, 6, and 15 mo, root:shoot allocation and percent root colonization at 1 and 6 mo, and the mass of bulbs, offsets, bulbils, and flowers at 15 mo. The number and mean mass of bulbils and offsets per plant were also analyzed. Biomass data from the first two harvests were log transformed to improve normality. Proportions were arcsine square root transformed. Post hoc comparisons of least squares means were made using Tukey's criterion to correct for multiple comparisons.
Differences in reproductive allocation patterns among plants in the mycorrhizal and P soil treatments were tested using two-way multivariate analyses of variance with profile contrasts using ranked data (Repeated Profile option in GLM procedure in SAS; Morrison, 1976; Ronsheim and Bever, 2000). Profile analysis tests whether the slopes of lines connecting the means of each reproductive character (bulb, offset, bulbil, and flower biomass) differ between the soil treatments, allowing all four characters to examined simultaneously. For example, a significant Mycorrhizae * Profile interaction would indicate that mycorrhizal and nonmycorrhizal plants differ in their allocation to different reproductive modes. The significance of these interactions was tested using Wilk's Lambda criterion because it is derived from a likelihood ratio approach (SAS, 1986); however, tests using Pillai's Trace and Hotelling-Lawley Trace gave similar results. Additional analyses of pairs of reproductive characters (e.g., bulbils vs. flowers) gave the same results as the overall profile analysis and will not be presented here.
Total biomass.--After 1 mo, mycorrhizal plants were significantly smaller than nonmycorrhizal plants (P < 0.001, Fig. 1a) ; and plant biomass increased at higher P fertilization levels (P = 0.003). There was not a significant interaction between the presence/absence of mycorrhizae and P fertilization levels (Myc * P interaction; P = 0.244).
After 6 mo, there was no significant effect of mycorrhizal treatment on biomass (P = 0.104, Fig. 1b) although there was a trend for mycorrhizal plants to be larger at lower P levels (Myc * P interaction; P = 0.087). The effect of P addition on total plant biomass did not change over this time period, as plant biomass was significantly larger with higher P levels (P < 0.001).
After 15 mo a significant Mycorrhizae * P interaction was seen for total biomass, with mycorrhizal plants being significantly larger than nonmycorrhizal plants at 0 and 50 [micro]g x g-1 P (P < 0.001, Fig. 1c). At higher P levels, there was no difference in the size of mycorrhizal and nonmycorrhizal plants. Thus, a significant mycorrhizal benefit in terms of increased total biomass was demonstrated only at lower P fertilization levels and only after 15 mo of growth.
[FIGURE 1 OMITTED]
Resource allocation and percent colonization.--A significant Mycorrhizae * P interaction for root:shoot ratio at 1 mo indicates that mycorrhizal and nonmycorrhizal plants differed in how they allocated resources in response to P fertilization level (P = 0.033, Fig. 2a). Specifically, whereas the root:shoot ratio for mycorrhizal plants did not vary, nonmycorrhizal plants allocated significantly more resources towards roots at 0 [micro]g x g-1 added P relative to 100, 200, and 250 [micro]g c g-1 added P. Percent mycorrhizal colonization of inoculated plants also did not vary significantly among any of the fertilization levels at the 1 mo harvest (P = 0.593, Fig. 2c).
The root:shoot allocation pattern at 6 mo was the same as at 1 mo, with mycorrhizal plants having the same root:shoot ratio regardless of P fertilization level; but nonmycorrhizal plants allocating significantly more resources towards roots at 0 and 50 [micro]g x g-1 added P (P < 0.001, Fig. 2b). Percent mycorrhizal colonization varied with P level (P < 0.001; Fig. 2c), with plants in the 0 and 50 [micro]g x g-1 added P treatments having significantly greater percent colonization than plants at 200 [micro]g x g-1 added P.
Reproduction.--Mycorrhizal and nonmycorrhizal plants had significantly different responses to increased level of P fertilization in the production of underground asexual offsets (Myc * P interaction, P = 0.004). The total biomass of offsets produced by mycorrhizal plants did not vary with P treatment. In contrast, the total mass of offsets for nonmycorrhizal plants growing at the two lowest P levels was significantly smaller than for nonmycorrhizal plants at higher P levels, as well as being significantly smaller than the total biomass of offsets produced by mycorrhizal plants at 0 [micro]g x g-1 added P. Whereas there was no significant variation in offset number for any of the treatments (offset number; Myc P = 0.270, P P = 0.550, Myc * P P = 0.282), the average mass of offsets was significantly smaller for nonmycorrhizal plants at low P levels relative to nonmycorrhizal plants at higher P levels and relative to mycorrhizal plants at 0 [micro]g x g-1 added P (Myc * P interaction, P = 0.001, Fig. 3a). Thus, the presence of mycorrhizae in low P treatments increased the relative size but not number of underground asexual propagules.
A similar pattern was seen for the total biomass of bulbils, which did not vary for mycorrhizal plants but was significantly lower for nonmycorrhizal plants growing with 0 [micro]g x g-1 added P relative to other nonmycorrhizal plants growing at 200 and 250 [micro]g x g-1 added P and to mycorrhizal plants at 0 [micro]g x g-1 added P (Myc * P interaction, P < 0.001). Most of this variation in total bulbil biomass was due to an increase in the number of bulbils rather than a change in the average size of individual bulbils (number of bulbils, Myc * P, P = 0.006, Fig. 3b). At 0 [micro]g x g-1 added P none of the nonmycorrhizal plants produced an aerial reproductive stalk, and at 50 [micro]g x g-1 added P only two of six nonmycorrhizal plants produced an aerial reproductive stalk. In all other treatments either five of six or six of six plants produced an aerial reproductive stalk.
Mycorrhizal plants produced larger bulbs than nonmycorrhizal plants across all levels of P added (P < 0.001, Fig. 3c). Mycorrhizal plants also produced more flowers than nonmycorrhizal plants (P = 0.016). Plants in both treatments produced few flowers, with nonmycorrhizal plants producing a mean of 1.6 flowers and mycorrhizal plants producing a mean of 2.6 flowers.
The profile analyses indicate that resource allocation to the different propagule types (bulb, offsets, bulbils, and flowers) was marginally different for mycorrhizal and nonmycorrhizal plants (Myc * Profile interaction, P = 0.059). However, most of this variation was due to the difference in bulb size for mycorrhizal vs. nonmycorrhizal plants, and there was no evidence for a significant shift in the relative allocation to offset, bulbil or flower production for mycorrhizal vs. nonmycorrhizal plants. In particular, there was no difference in allocation to flowers vs. bulbils, with an overall 13.7% flowers/(flowers + bulbils). There was no significant difference in allocation to different propagule types among the phosphorus treatments (P * Profile interaction, P = 0.122), nor was a significant interaction effect found (Myc * P * Profile, P = 0.065).
[FIGURE 2 OMITTED]
[FIGURE 3 OMITTED]
For Allium vineale plants, the impact of mycorrhizal infection varies significantly with life stage. Young plants (1 mo) experience a significant growth depression, which disappears as the plants grow (6 mo), and finally switches to a positive association when the plants reach their reproductive stage (15 mo). Mycorrhizal induced growth depressions are often assumed to be a result of the balance between benefits and costs of the plant- fungal association, in which fungal demands for C from the plant are not balanced by the benefits of P transport to the plant (see Jones and Smith, 2004), and this negative effect can persist through the life of the plant. The growth depression seen in this study clearly does not fall into this category, as the presence of mycorrhizae at later life stages results in significantly larger plants and more reproductive output at lower P levels. Given recent evidence for P uptake even when there is no growth advantage (e.g., Li et al., 2008; Smith et al., 2009), young mycorrhizal A. vineale plants may have been receiving and accumulating P in their bulb that was then used when the carbon assimilating potential of the plants reached a threshold level. Without information on P uptake and transport by the fungus and the plant, coupled with information on rates of C assimilation and transport by the plant, we cannot determine what, if any, role the C-P cost-benefit balance played in the growth depression and its reversal in this study, underscoring the need for further mechanistic investigation of early growth depression (see review by Smith et al., 2009).
Mycorrhizal induced growth depressions can also occur at higher levels of nutrient availability when P is not limiting, as plants experience the carbon cost of the fungus but without the benefit of increased available P (Johnson et al., 1997; Jones and Smith, 2004). In this study we found no evidence for environmental parasitism of the plant by mycorrhizae at high levels of P, although the plant-fungal association does shift from a relative benefit at lower P levels to neutral at higher P levels. In particular, there was no effect of variation in P level on overall size of mycorrhizal plants at 15 mo or on their reproductive output. As seen in some other species (e.g., Hepper, 1983; Jensen, 1983; Thomson et al., 1986; Schroeder and Janos, 2004; see also Smith and Smith, 1996), the percent of Allium vineale roots colonized by mycorrhizae was significantly lower at higher levels of P after 6 mo of growth. It is possible that this reduction in colonization by the mycorrhizal fungus lowers the cost of the association for the plant, thereby resulting in an overall neutral effect rather than a negative effect on total plant biomass (Johnson et al., 1997).
In contrast to mycorrhizal plants, P level had a significant effect on nearly all traits measured for nonmycorrhizal plants, indicating that nonmycorrhizal plants in the low P treatment were limited by P availability. Nonmycorrhizal plants in higher P treatments allocated less resources to roots, were significantly larger at 15 mo, and produced more bulbils and larger offsets. At the lowest P level none of the nonmycorrhizal plants produced an aerial scape, whereas at higher P levels their total size, root:shoot allocation and reproductive output was not significantly different from mycorrhizal plants. Plants often allocate more to roots when belowground resources such as P are limiting (Ericsson, 1995; Jones and Smith, 2004). The fact that mycorrhizal plants had larger bulbs and higher reproductive rates at maturity may be at least partly due to the fact they were able to allocate less resources to roots at low P levels.
Information on the impact of mycorrhizae on plant reproduction is clearly important for developing an ecological/evolutionary perspective on plant-mycorrhizal dynamics. In general, species with positive vegetative responses also have positive reproductive responses, but this pattern is not universal and varies with environment and plant genotype (e.g., Scagel and Schreiner, 2006) and mycorrhizal inoculum (e.g., Oliveria et al., 2006). In this study, mycorrhizal plants at lower P levels had higher fecundity than nonmycorrhizal plants, as they produced more bulbils and larger offsets. In addition, the presence of mycorrhizae resulted in larger bulbs at all levels of P. As larger bulbs produce greater numbers of flowers and bulbils the following year (Ronsheim, 1997), this increase in bulb size is likely to translate into greater lifetime fitness, and this benefit may be increased further if the specific fungal associates of Allium vineale are present. Whereas mycorrhizal plants also produce, on average, an additional flower relative to nonmycorrhizal plants, it is difficult to determine if this increase would have a significant effect on overall fitness. Both seed set (mean of 0.7 seeds/flower in the field, M. Ronsheim, pers. obs.) and seedling survival (Ronsheim, 1996) are relatively low in the field thus the impact of one additional flower on fitness and overall population dynamics is likely to be small.
The presence of mycorrhizae did not shift the relative allocation of resources to different reproductive modes (bulbils vs. offsets vs. flowers). Thus, the relative allocation of resources to sexual vs. asexual reproduction as well as to above vs. belowground asexual reproduction is unaffected by mycorrhizal status. Mycorrhizal Allium vineale plants did produce more bulbils and larger offsets than nonmycorrhizal plants but only at lower P levels. A previous study demonstrated that A. vineale plants produce more bulbils and larger offsets with increased nutrient availability (Ronsheim and Bever, 2000) thus it is likely that the increase in reproductive output found in this study is also consequence of improved nutritional status, specifically an increase in P availability. Selection for aerial dispersal ability could be one factor that would favor producing a greater number of smaller aerial bulbils rather than fewer larger ones, but the potential advantages of increasing the size vs. number of underground offsets is unknown.
The P concentrations used in this experiment (89-201 [micro]g x g-1) reflect the upper range in P availability found in the field from which these plants were collected (39-155 [micro]g x g-1). The results from this study indicate that, within this population of Allium vineale, spatial heterogeneity in P in the field is likely to result in the plant-mycorrhizal association ranging from beneficial to neutral in its effect on plant growth and reproduction. Recent work by Johnson et al. (2010) demonstrates the presence of local co-adaptation in plant- AM fungal symbioses, resulting in a geographic mosaic that maximizes benefits in P limited soil and minimizes costs in P rich soil. Whether variation within a field in nutrient availability and in the relative benefit of mycorrhizae could result in small scale local adaptation of plant-fungal communities is unknown.
In summary, these results emphasize the importance of long term studies that include all life stages of the plant, especially those relating to reproduction and overall fitness. In addition, spatial variation in nutrient availability in the field has the potential to shift the overall effect of mycorrhizae from beneficial to neutral, with greater benefits found in microsites with lower phosphorus levels. Finally, whereas colonization by mycorrhizae does increase overall bulb size and thus potentially the long term fitness of the plant, it does not affect how resources are allocated among propagule types.
Acknowledgments.--I would like to thank K. Sharma, B. Gumbs, and S. Anderson for their help with this project and L. Christenson and two anonymous reviewers for comments on the manuscript.
SUBMITTED 15 MARCH 2011
ACCEPTED 16 JUNE 2011
BETHLENVALVAY, G. J., M. S. BROWN AND R. S. PACOVSKY. 1982. Parasitic and mutualistic associations between a mycorrhizal fungus and soybean: development of the host plant. Phytopathology, 72:889-893.
BRUNDRETT, M. C. 2002. Coevolution of roots and mycorrhizas of land plants. New Phytol., 154:275-304.
BRYLA, D. R. AND R. T. KOIDE. 1990. Regulation of reproduction in wild and cultivated Lycopersicon esculentum Mill. by vesicular-arbuscular mycorrhizal infection. Oecologia, 84:74-81.
BUWALDA, J. G. AND K. M. GOH. 1982. Host-fungus competition for carbon as a cause of growth depressions in vesicular-arbuscular mycorrhizal ryegrass. Soil Biol. and Biochem., 14:103-106.
CAREY, P. D., A. H. FITTER AND A. R. WATKINSON. 1992. A field-study using the fungicide benomyl to investigate the effect of mycorrhizal fungi on plant fitness. Oecologia, 90:550- 555.
ERICSSON, T. 1995. Growth and shoot:root ratio of seedlings in relation to nutrient availability. Plant Soil, 168-169:205-214.
GIOVANNETTI, M. AND B. MOSSE. 1980. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol., 84:489-500.
GRACE, C. AND D. P. STRIBLEY. 1991. A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Myc. Research, 95:1160-1162.
HART, M. M. AND J. N. KLIRONOMOS. 2002. Diversity of arbuscular mycorrhizal fungi and ecosystem functioning, p. 225-242. In: M. G. A. van der Heijden and I. Sanders (eds.). Mycorrhizal ecology. Springer-Verlag, Berlin.
HEPPER, C. M. 1983. The effect of nitrate and phosphate on the vesicular- arbuscular mycorrhizal infection of lettuce. New Phytol., 92:389-399.
JENSEN, A. 1983. The effect of indigenous vesicular-arbuscular mycorrhizal fungi on nutrient uptake and growth of barley in two Danish soils. Plant Soil, 70:155-163.
JOHNSON, N. C., J. H. GRAHAM AND F. A. SMITH. 1997. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol., 135:575-585.
--, G. W. T. WILSON, M. A. BOWKER, J. A. WILSON AND R. M. MILLER. 2010. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc. Natl. Acad. Sci., 107:2093-2098.
JONES, M. D. AND S. E. SMITH. 2004. Exploring functional definitions of mycorrhizas: Are mycorrhizas always mutualisms? Can. J. Bot., 89:1089-1109.
KOIDE, R. T. 1985. The nature of growth depressions in sunflower caused by vesicular-arbuscular mycorrhizal infection. New Phytol., 99:449-462.
--. 2000. Mycorrhizal symbiosis and plant reproduction, p. 19-46. In: Y. Kapulnik and D. D. Douds Jr (eds.). Arbuscular mycorrhizas: Physiology and function. Kluwer Academic Publishers, Dordrecht, the Netherlands.
--, D. L. SHUMWAY AND S. A. MABON. 1994. Mycorrhizal fungi and reproduction of field populations of Abutilon theophrasti Medic. (Malvaceae). New Phytol., 126:23-130.
LAPOINTE, L. AND J. MOLARD. 1997. Costs and benefits of mycorrhizal infection in a spring ephemeral, Erythronium americanum. New Phytol., 135:491-500.
LI, H. Y., F. A. SMITH, S. DICKSON, R. E. HOLLOWAV AND S. E. SMITH. 2008. Plant growth depressions in arbuscular mycorrhizal symbioses: not just caused by carbon drain? New Phytol., 178:852-862.
--, Y. G. ZHU, P. MARSCHNER, F. A. SMITH AND S. E. SMITH. 2005. Wheat responses to arbuscular mycorrhizal fungi in a highly calcareous soil differ from those of clover, and change with plant development and P supply. Plant Soil, 277:221-232.
MERRYWEATHER, J. AND A. FITTER. 1995. Arbuscular mycorrhiza and phosphorus as controlling factors in the life history of Hyacinthoides non-scripta (L.) Chouard ex Rothm. New Phytol., 129:629-636.
MORRISON, D. F. 1976. Multivariate statistical methods. McGraw-Hill Book Company, New York, New York. 222 p.
NEWSHAM, K. K., A. U. FITTER AND A. R. WATKINSON. 1995. Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol. Evol., 10:407-411.
OLIVERIA, R. S., P. M. L. CASTRO, J. C. DODD AND M. VOSATKA. 2006. Different native arbuscular mycorrhizal fungi influence the coexistence of two plant species in a highly alkaline anthropogenic sediment. Plant Soil, 287:209-221.
OLSEN, J. K.,J. T. SCHAEFER, D. G. EDWARDS, M. N. HUNTER, V.J. GALEA AND L. M. MULLER. 1999. Effects of mycorrhizae, established from an existing intact hyphal network, on the growth response of capsicum (Capsicum annuum L.) and tomato (Lycopersicon esculentum Mill.) to five rates of applied phosphorus. Aust. J. Agric. Research, 50:223-237.
PAGE, A. L. 1982. Methods of soil analysis: part 2 Chemical and microbiological properties, 2nd ed. American Society of Agronomy and Soil Science Society of America, Madison, Wisconsin. 1159 p.
PENG, S., D. M. EISSENSTAT, J. H. GRAHAM, K. WILLIAMS AND N. C. HODGE. 1993. Growth depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiol., 101:1063-1071.
RADFORD, A. E., H. E. AHLES AND C. R. BELL. 1968. Manual of the vascular flora of the Carolinas. University of North Carolina Press, Chapel Hill. 1183 p.
RICHENS, R. 1947. Biological flora of the British Isles. J. Ecol., 34:209-226.
RONSHEIM, M. L. 1994. Dispersal distances and predation rates of sexual and asexual propagules of Allium vineale L. Am. Midl. Nat., 131:55-64.
--. 1996. Evidence against a frequency-dependent advantage for sexual reproduction in Allium vineale. Am. Nat., 147:718-734.
--. 1997. Distance-dependent performance of asexual progeny in Allium vineale (Liliaceae). Am. J. Bot., 84:1279-1284.
-- AND J. D. BEVER. 2000. Genetic variation and evolutionary trade-offs for sexual and asexual reproductive modes in Allium vineale (Liliaceae). Am. J. Bot., 87:1769-1777.
SAS INSTITUTE. 1986. SAS user's guide: Statistics. SAS Institute, Cary, North Carolina. 956 p.
SCAGEL, C. F. AND R. P. SCHREINER. 2006. Phosphorus supply alters tuber composition, flower production, and mycorrhizal responsiveness of container-grown hybrid Zantedeschia. Plant Soil 283:323-337.
SCHROEDER, M. S. AND D. P. JANOS. 2004. Phosphorus and intraspecific density alter plant responses to arbuscular mycorrhizas. Plant Soil, 264:335-348.
SMITH, F. A., E. J. GRACE AND S. E. SMITH. 2009. More than a carbon economy: Nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol., 182:347-358.
-- AND S. E. SMITH. 1996. Mutualism and parasitism: diversity in function and structure in the "arbuscular" (VA) mycorrhizal symbiosis. Adv. Bot. Res., 22:1-43.
SMITH, S. E. AND D. J. READ. 1997. Mycorrhizal symbioses. 2nd ed. Academic Press, London. 605 p.
STREITWOLF-ENGEL, R., T. BOLLER, A. WIEMKEN AND I. R. SANDERS. 1997. Clonal growth traits of two Prunella species are determined by co-occurring arbuscular mycorrhizal fungi from a calcareous grassland. J. Ecol., 85:181-191.
STRIZTKE, J. F. AND E. J. PETERS. 1972. Dormancy and sprouting cycles of wild garlic. Weed Sci., 18:112-114.
THOMSON, B. D., A. D. ROBSON AND L. K. ABBOTT. 1986. Effects of phosphorus on the formation of mycorrhizas by Gigaspora calospora and Glomus fasciculatum in relation to root carbohydrates. New Phytol., 103:751-765.
VARGA, S. 2010. Effects of arbuscular mycorrhizas on reproductive traits in sexually dimorphic plants. Spanish J. Agric. Res., 8:S11-S24.
MARGARET L. RONSHEIM (1)
Department of Biology, Vassar College, 124 Raymond Avenue, Poughkeepsie, New
(1) e-mail: email@example.com
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