relationship between mycorrhizal dependence and competitive ability of two tallgrass prairie grasses

Relationship between mycorrhizal dependence and competitive ability of two tallgrass prairie grasses1

B A D HE TRICK^ AND G W T WILSON Department of Plant Pathology Throckmorton Hall Kansas State UniversiQ Manhattan KS 66506 USA

AND

D C HARTNETT Division of Biology Ackert Hall Kansas State UniversiQ Manhattan KS 66506 USA

Received November 14 1988

HETRICK B A D WILSON G W T and HARTNETT D C 1989 Relationship between mycorrhizal dependence and competitive ability of two tallgrass prairie grasses Can J Bot 67 2608-2615

The impact of mycorrhizal symbiosis on growth of Andropogon gerardii (big bluestem) and Koeleriapyranidata (junegrass) was compared Andropogon gerardii was 98 dependent on the symbiosis whereas K pyranidata displayed less than 002 dependence Mycorrhizal fungus inoculation resulted in 50 times larger A gerardii plants but did not alter growth of K pyranidata When competing in pairs A gerardii dominated when the mycorrhizal symbiosis was present and K pyranidata dominated when it was not present Dry weight of mycorrhizal A gerardii was altered whether grown alone or with K pyranidata but mycorrhizal K pyranidata grew well only in the absence of competition and failed to grow appreciably if A gerardii was present Without mycorrhizal fungus inoculation A gerardii did not grow and had no deleterious effects on K pyranidata When P fertilization was substituted for mycorrhizal fungus inoculation A gerardii grew better alone than in competition with K pyranidata at low P levels but was not affected by competition at high P levels Koeleriapyranidata was not affected by competition at low P levels but high P fertilization resulted in reduced dry weight of K pyranidata plants when in competition with A gerardii Phenologic separation of growing seasons avoids interspecific competition between these two grasses and may be one mechanism contributing toward their coexistence Since low temperatures limit mycorrhizal nutrient uptake phenologic separation of growing seasons could also avoid the competitive advantage of warm-season grasses conferred by their mycorrhizal dependence

HETRICK B A D WILSON G W T et HARTNETT D C 1989 Relationship between mycorrhizal dependence and competitive ability of two tallgrass prairie grasses Can J Bot 67 2608-2615

Les auteurs ont compak linfluence de la symbiose mycorhizienne sur la croissance de lYAndropogon gerardii et le Koeleria pyranidata Andropogon gerardii montre une dkpendance de 98 alors que chez le K pyranidata la dkpendance nest que de 002 Linoculation mycorhizienne augmente de 50 fois la croissance des plants du A gerardii alors que celle du K pyranidata nest pas modifike Lorsquils compktitionnent en paires A gerardii domine sil y a symbiose mycorhizienne alors que cest le K pyranidata qui domine en absence de symbiose Les poids secs de A gerardii mycorizks ne sont pas modifies quils soient cultivks seuls ou en prksence du K pyranidata cependant le K pyranidata mycorhizien ne pousse bien quen absence de compktition et narrive pas I crottre si le A gerardii est pdsent En absence dinoculation mycorhizienne le A gerardii ne se dkveloppe pas et nexerce aucun effet nkgatif sur le K pyranidata Lorsque la fertilisation avec du P remplace linoculation mycorhizienne le A gerardii se dkveloppe mieux seul quen compktition avec le K pyranidata avec de faibles additions de P mais nest pas affectk par la compktition en pksence de fortes additions de P Le K pyranidata nest pas affectk par la compktition avec de faibles additions de P mais de fortes additions de P entrainent une r6duction de la croissance des plants de K pyranidata lorsquils sont en compktition avec le A gerardii 11 existe une skparation phknologique entre ces deux plantes quant aux saisons de croissance ce qui prkvient la compktition interspkcifique entre ces deux herbes cette skparation phknologique pourrait bien Ctre un mkcanisme qui contribue i leur co-existence Puisque les basses tempkratures limitent labsorption des nutriments par les mycorhizes la skparation phknologique des saisons de croissance pourrait aussi permettre dkviter chez les herbes pkfkrant les saisons chaudes lavantage compktitif qui leur est confkd par leur dkpendance mycorhizienne

[Traduit par la revue]

Introduction Tallgrass prairie is a diverse community composed of warm-

and cool-season grasses and forbs growing in close association Warm-season grasses such as Andropogon gerardii Vit Sor- ghastrum nutans L (Nash) Panicum virgatum L and Boute- loua curtipendula Michx are generally of tropical origin grow most rapidly in warm summer months and bloom in August or September The warm-season grasses are deep rooted (up to 5 - 8 ft depth 1 ft = 0304 m) and are favored by spring burning (Weaver and Clements 1938 Clements 1949) In contrast cool-season grasses such as Koeleria pyranidata

L Elymus canadensis L and Stipa spartea Trin are of temperate affiliation grow most rapidly in spring and fall when soil temperatures are cooler and flower in late spring or early summer While some cool-season grasses may be deep- rooted others are shallow-rooted and may occupy only the upper 50 cm of the soil profile (Weaver 1954) Clearly there are distinct differences in the growth strategies of these two plant groups This temporal and belowground niche separation as well as partitioning along other niche axes such as pol- linator use may be important mechanisms contributing toward species coexistence and diversity in tallgrass prairie comrnuni- ties CBazzaz and Pamsh 1982 Pamsh and Bazzaz 1979 Wil- liams and Markley 1973) and in other grasslands (Berendse

Contribution No 89-168-~ Kansas ~ g r i c u l t u ~ l Experiment sta- 1982 1983) In addition other nonequilibrium processes tion Kansas State University Manhattan KS 66506 USA such as disturbances operating at different scales also influ-

Author to whom all correspondence should be addressed ence prairie community structure (Collins 1987 Pickett 1980)

Rinted in Canada Imprimt au Canada

Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL 2609

Although both warm- and cool-season tallgrass prairie grasses are mycorrhizal they differ significantly in dependence on mycorrhizal symbiosis for nutrient acquisition and growth (mycorrhizal dependence is estimated as (dry weight of inoculated plants - dry weight of noninoculated plants) divided by dry weight of inoculated plants Hetrick et al 1988~) The warm-season grass seedlings display extremely high dependence (ca 99) failing to grow appreciably in the absence of the symbiosis whereas cool-season grass seedlings are more variable in dependence some significantly inhibited by mycorrhizal infection (- 15 to 76)

Mycorrhizal symbiosis can alter the competitive ability of plants (Fitter 1977 Hall 1978) Most studies of plant competition have been phenomenological measuring the negative effects on the performance o f plants imposed by their neighbors (interference sensu Harper 1977) and the specific mechanism(s) of interference (ie competition for limiting nutrients light or water) or the specific mechanism(s) by which mycorrhizal symbiosis alter competition are very dif- ficult to identify experimentally because they are interdepen- dent Mycorrhizal symbioses are likely to directly influence the relative abilities of plants to compete for limiting nutrients but enhanced relative growth rates resulting from increased nutrient uptake may in turn increase their ability to compete for light above ground Regardless of the specific mechanism(s) or interference this known relationship between mycorrhizal dependence and competitive ability may influence patterns of species richness and relative abundance and other spatial and (or) temporal aspects of plant community structure Whether mycorrhizal symbioses influence plant community structure by suppression of mycorrhiza-inhibited (opposite of mycorrhiza- dependent) dominants or enhancing evenness of species abun- dances through translocation of resources to subordinate species via hyphal interconnections or other mechanisms has been the subject of recent debate (Grime et al 1987 1988 Bergelson and Crawley 1988) Regardless of the specific mechanism by which mycorrhizal fungi affect resource availability to a given plant they may increase plant species diversity (species richness and (or) evenness) if they decrease the competitive ability of abundance of competitive dominants relative to subordinate species or they may reduce diversity if the symbiosis is of greater relative benefit to the dominant species in the community Few studies have examined the influence of mycorrhizal symbiosis on competitive interactions between naturally cooccurring plant species

These studies explore the mycorrhizal dependence of two important tallgrass prairie species A gerardii (warm season) and K pyranidata (cool season) and assess the consequences of the mycorrhizal symbiosis for competition between them in a greenhouse setting The study was designed to assess the

effect of interspecific interference on target plants under vary- ing conditions of mycorrhizal symbiosis and soil fertility levels

I Materials and methods

To determine the importance of vesicular-ahuscular myconhizal (VAM) fungi for growth of big bluestem (A gerardii Vit) and prairie junegrass (K pyranidata L) 2-week-old seedlings of each species were planted in 6 x 25 cm pots containing 425 g (dry weight) of pasteurized prairie soil (steam pasteurized for 2 h at 80degC) Soil was freshly collected from Konza Prairie Research Natural Area Man- hattan KS (Chase silty clay loam) and contained 10 ppm plant- available phosphorus (Bray test 1) Seed of big bluestem was provided

by the Soil Conservation Service Plant Materials Center Manhattan KS and junegrass seed was supplied by the Upper Colorado Environ- mental Plant Center Meeker CO One-half of the pots received 30 ppm P applied to the soil surface in 10-mL aliquots of a KH2P04 solution Six phosphorus-amended pots and six nonamended pots were selected as controls The seedlings of the remaining pots were each inoculated with 400 Glomus etunicatum Becker and Gerd spores This isolate originally obtained from Konza Prairie was sub- cultured on sudangrass (Sorghum vulgare var sudanense (Piper) Hitch) Spores were then collected from pot cultures by wet sieving decanting and sucrose density gradient centrifugation (Daniels and Skipper 1982) Spores were suspended in distilled water and pipetted (400 sporesmL) onto the roots of each seedling at transplanting These pots were then amended with 10 mL of a 0 15 30 or 45 ppm (active ingredient) Benomyl (Tersan 1991 E I duPont de Nemours amp Co Wilmington DE) solution Thus there were 10 treatments (two P treatments (amended and nonamended) x four fungicide levels) applied to myconhizal fungus inoculated plants and a noninoculated control for each of the two prairie grasses with six replicate pots per treatment

To assess the effect of interspecific competition on big bluestem and prairie junegrass growth and root colonization A gerardii and K pyranidata seeds were germinated in vermiculite Two weeks after emergence an A gerardii a K pyranidata or one of each seedling was transplanted into 6 x 25 cm plastic pot containing 450 g (dry weight) of steam-pasteurized soil or nonsterile soil Seedlings planted alone were centered in the pot whereas seedlings that were planted two per pot (one A gerardii and one K pyraniduta) were spaced approximately 2 cm apart Although resulting in different plant densities this additive rather than substitutive design (Harper 1977) was chosen as the most appropriate because the goal was not to compare the competitive effect of a big bluestem versus junegrass on a target plant (intraspecific vs interspecific interference) but rather to compare the effect of interspecific interference in the presence versus absence of the myconhizal symbiosis

Pots containing pasteurized soil were subdivided into three groups of 28 pots The seedlings of one group were inoculated with 400 G etunicatum spores per pot The second subgroup received 10 mL of a KH2P04 solution (20 ppm P) applied onto the soil surface The third subgroup was left noninoculated and nonarnended All nonsterile soil was left untreated Thus there were 16 treatments each containing seven replicate pots

Experimental approaches such as this one invevitably involve com- promises between maximum precision realism and generality (Harper 1982) The Benomyl treatments used in the above experiment likely alter other components of the soil microflora and thus the responses observed cannot be attributed solely to an abundance of myconhizal fungi Thus this competition study was subsequently repeated but expanded to include several additional treatments Soil treatments included pasteurized soil nonsterile soil and pasteurized soil amended with 50 mL sieved suspension of nonsterile soil to return other components of the natural soil microflora while still experimentally controlling fungal abundance Nonsterile soil sieved suspension was obtained by blending 1100 g nonsterile prairie soil into 55 L (200 gL) sterile distilled water using a Waring blender and passing the mixture through a 38-pm sieve to remove indigenous VAM fungi The sieved suspension contained 470 colony-forming units (cfu)mL of fungi and 66 x lo6 cfumL of bacteria as estimated by dilution-plating sieved suspensions onto either peptone yeast extract agar or 06 potato dextrose agar (Difco Laboratories Detroit MI) amended with 100 pgmL each of streptomycin sulfate and chloramphenicol Colonies were counted after 7 days at 22OC Either an A gerardii a K pyraniduta or one of each seedling was planted into a pot as before Each soil treatment was amended with either 0 25 or 50 ppm P (KH2P04) applied as a soil drench One-half of the treatments received 400 spores G etunicatum as described earlier Thus this study had 60 treatments with six replicate pots per treatment

For all three experiments pots were arranged in randomized com-

Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

2610 CAN J BOT VOL 67 1989

TABLE 1 Influence of Benomyl fungicide and phosphorus fertilization on mycorrhizal growth response and root colonization of Andropogon

gerardii and Koeleria pyranidata (14 weeks growth)

Total dry weight (g) Root colonization ()

Fungicide rate No P 30 pprn P+ No P 30 pprn P

A gerardii Not inoculated 00 0 4 0 ~ Oc Oc Inoculated

0 ppm Benomyl 2 5 4 ~ 2 8 1 ~ 8 0 5 ~ 7 9 0 ~ 15 ppm Benomyl 0 0 4 ~ 148b Oc 350b 30 ppm Benomyl 00 073bc Oc 9 4 ~ 45 ppm Benomyl 0 0 4 ~ 0 5 4 ~ Oc 3 8 ~

K pyranidata Not inoculated 1 6 4 ~ 1 7 3 ~ oz oz Inoculated

0 ppm Benomyl 1 5 1 ~ 1 4 7 ~ 1 ly 7~ 15 ppm Benomyl 1 4 8 ~ 1 5 7 ~ 22 oz 30 ppm Benomyl 1 4 4 ~ 1 4 5 ~ oz oz 45ppmBenomyl 1 5 6 ~ 1 9 1 ~ oz oz

NOTE Means for dry weight or root colonization followed by the same letter are not significantly different (P = 005) as determined using Duncans multiple-range test

Inoculated with 400 Glomus etu~~icotum spores ~elivered as KHPO

plete block designs in a greenhouse maintained at 60-7SdegC and fertilized biweekly with Peters No-Phos special fertilizer solution (25-0-25 Peters Fertilizer Products Fogelsville PA) Although plants in the field are subjected to broader temperature fluctuations the temperatures used in these greenhouse experiments were chosen because they support growth of both cool- and warm-season plants Plants were harvested after 14 weeks and shoot root and total dry weights were determined The dried roots were subsampled stained in trypan blue (Phillips and Hayman 1970) and examined micro- scopically to assess percent root colonization with a Petri plate scored into 1-rnrn squares (Daniels et al 1981) Differences in total dry weights and percent root colonization were subjected to analysis of variance (P = 005) followed by Duncans multiple-range test for mean separation

Results Andropogon gerardii showed a much greater mycorrhizal

dependence than K pyranidata (Table 1 ) Mycorrhizal A gerardii plants were 50 times larger than noninoculated controls or those inoculated and treated with fungicide Growth of the noninoculated plants and those treated with 15 30 or 45 pprn fungicide was negligible The fact that noninoculated plants and Benomyl-treated plants were indistinguishable in dry weight suggests that the Benomyl treatment effectively inhibits the mycorrhizal association without causing other significant direct or indirect effects on the plants While all concentrations of Benomyl effectively eliminated mycorrhizal growth response in nonfertilized plants Benomyl was only effective at higher concentrations in fertilized plants Application of Beno- my1 to nonfertilized plants prevented establishment of mycorrhizae and the plants died While mycorrhizal establishment in fertilized plants may have been similarly inhibited the loss of mycorrhizae was not fatal for these plants Since mycorrhizal colonization did occur in fertilized plants treated with 15 pprn Benomyl this level of fungicide may not have killed all inoculum and colonization occurred perhaps after the Benomyl leached from the soil For nonfertilized plants however failure to colonize at the outset of the experiment pre- cluded plant growth and any later colonization that might have

occurred The close relationship between root colonization and plant dry weight data suggests that Benomyl can effectively inhibit G etunicatum and is not phytotoxic

Unlike A gerardii K pyranidata plants grew equally well whether or not they were inoculated P fertilized or treated with fungicide This suggests that K pyranidata is not dependent on mycorrhizal symbiosis although root colonization does occur Whether this low level of colonization is biologi- cally meaningful is questionable since no differences in dry weight were observed The mycorrhizal dependence of A gerardii calculated from the data in Table 1 is 98 whereas K pyranidata is -009 to 002 dependent These data are consistent with those of Hetrick et al (1988a)

When competing in pairs A gerardii dominated when mycorrhizal fungi were present and K pyranidata dominated when the symbiosis was absent (Table 2) Dry weight of mycorrhizal A gerardii was not altered whether grown alone or in combination with K pyranidata In contrast mycorrhizal K pyranidata grew well in the absence of competition but failed to grow appreciably if A gerardii was present In the nonmyco=hizal condition A gerardii did not grow and had no deleterious effects on K pyranidata When plants were fertilized to partially compensate for the symbiosis A gerardii grew significantly better alone than in combination with K pyranidata whereas K pyranidata grew equally well alone or in competition with A gerardii (Table 2) In nonsterile soil containing indigenous mycorrhizal fungi A gerardii was unaffected by K pyranidata whereas K pyranidata growth was significantly reduced by the presence of A gerardii While absolute dry weight of A gerardii in nonsterile soil was not as great as that achieved in steamed soil its competitive relationships with K pyranidata were similar in steamed and nonsterile soils (Table 2)

Mycorrhizal root colonization of A gerardii was not altered by competition with K pyranidata either in steamed or in nonsterile soil (Table 2) For K pyranidata however the presence of A gerardii significantly increased root colonization of K pyranidata in steamed soil Improved colonization of a less dependent plant when grown in combination with a highly dependent plant has been demonstrated in other competition studies (Fitter 1977) It is interesting that in the present study this improved colonization occurred only in steamed soil and not in nonsterile soil In nonsterile soil competition from A gerardii was deleterious to percent colonization of K pyranidata

In a second competition experiment the impact of P fertilization and soil sterilization on the com~etitive relationshi~s of A gerardii and K pyranidata was explored in greater detail In steamed soil mycorrhizal A gerardii responded to P fertilization and was not effected by competition from K pyranidata (Table 3) As in the previous experiment growth of mycorrhizal K pyranidata was significantly reduced when in competition with A gerardii In fact K pyranidata responded to P fertilization only when grown alone Noninoculated A gerardii did not grow unless P fertilized but at 25 pprn P competition from K pyranidata significantly limited A gerardii growth (Table 3) At 50 pprn P however no deleterious competition effect of competition was observed perhaps because the need for mycorrhizal symbiosis was minimal at that high P level Noninoculated K pyranidata was unaffected by P fertilization or competition except at the highest P level where competition was again deleterious to K pyranidata

In steamed soil amended with nonsterile soil sievings

Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL

(mycorrhizal fungi removed but other soil microflora replaced) inoculated A gerardii was again unaffected by competition with K pyranidata although dry weight was not as great as that achieved in steamed soil (Table 3) The growth- limiting effect of the soil microflora has been demonstrated repeatedly (Hetrick et al 1986 1988b Wilson et al 1988) and has been attributed to microbial competition with mycorrhizae for nutrients such as P For inoculated K pyranidata the growth-suppressive effect of the soil microflora masked any difference between K pyranidata grown alone and K pyranidata grown with A gerardii except at the highest P level The deleterious effect of the soil microflora was not overcome by P fertilization of mycorrhizal K pyranidata For nonmycorrhizal A gerardii competition from K pyranidata was not significant

In nonsterile soil where the influence of the soil microflora is probably most pronounced no comparisons between mycorrhizal and nonmycorrhizal plants can be made because the indigenous mycorrhizal fungus populations in nonsterile soil affect root colonization As in other mycorrhizal treatments A gerardii was unaffected by competition from K pyranidata whereas K pyranidata growth-was significantly limited by competition from A gerardii (Table 3) In nonsterile soil however A gerardii and K pyranidata grown alone did respond to P fertilization perhaps because fertilization allevi- ated microbial suppression of plant growth as suggested by Hetrick et al (1988b)

Mycorrhizal root colonization of VAM fungus-inoculated A gerardii or K pyranidata grown alone in steamed soil decreased as the P fertilization rate increased (Table 4) This high P inhibition of root colonization did not occur however - when the two species were grown together This was most likely due to the increased nutrient demand and therefore increased dependence on the symbiosis when two plants were competing together in one pot In steamed soil amended with soil sievings and in nonsterile soil levels of root colonization were lower than in steamed soil a phenomenon observed repeatedly (Hetrick et al 1986 1988b Wilson et al 1988) Colonization was reduced even further by high levels of P fertilization The tendency for K pyranidata to be more colo- nized when in competition with A gerardii was evident in steamed soil amended with nonsterile soil sievings but not in nonsterile soil (Table 4)

Root to shoot ratios remained fairly constant for A gerardii (Table 5) In contrast K pyranidata root to shoot ratios increased significantly when competing with A gerardii in noninoculated treatments

Discussion These results confirm that A gerardii is highly dependent

on mycorrhizal symbiosis (obligate mycotroph) whereas K pyranidata has little or no requirement for the symbiosis (facultative mycotroph) These results also demonstrate that when competing in pairs A gerardii has a much greater competitive ability than K pyranidata under conditions of mycorrhizal symbiosis or high available phosphorus In the absence of VAM or in low P soils K pyranidata dominates in competition with A gerardii and grows well alone or with A gerardii In an earlier competition study (Fitter 1977) a plant growing alone was restricted to half the soil volume that was available when two plants were grown together or two plants of the same species were grown together and compared with

Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

CAN J BOT VOL 67 1989

TABLE 3 Influence of mycorrhizae and phosphoms fertilization on competition between Andropogon gerardii and Koeleria pyranidata (14 weeks growth)

Total dry weight (g)

A gerardii K pyranidata

Soil treatment Alone With K pyranidata Alone With A gerardii

Steamed soil Inoculated

0 PPm P 25 pprn P 50 pprn P

Noninoculated 0 P P ~ P

25 pprn P 50 pprn P

Steamed soil with sievings Inoculated

0 P P ~ P 25 pprn P 50 pprn P


25 pprn P 50 pprn P

Nonsterile soil 0 P P ~ P

25 ppm P 50 pprn P

NOTE Means within a soil treatment followed by the same letter are not significantly different (P = 005) as determined using Duncans multiple-range test

Inoculated with 400 Glomus etunicatum spores

TABLE 4 The influence of phosphoms fertilization and plant competition on mycorrhizal root colonization of Andropogon gerardii and Koeleria pyranidata

Root colonization ()


Alone With K pyranidata Alone With A gerardii


0 PPm P 25 ppm P 50 ppm P


25 pprn P 50 pprn P


0 PPm P 25 pprn P 50 ppm P


25 pprn P 50 pprn P


25 ppm P 50 pprn P

-- - - - -



Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL

TABLE 5 The influence of phosphorus fertilization and plant competition on root to shoot ratios of Andropogon gerardii and Koeleria pyranidata

Root to shoot ratio





Noninoculated 0 PPrn P

25 pprn P 50 pprn P




25 pprn P 50 pprn P

Nonsterile soil 0 PPrn P

25 pprn P 50 pprn P

NOTE Means within a soil treatment followed by the same letter are not significantly different (P = 005) as detemlined using Duncans multiple-range test Differences showing statistical significances are in boldface

Inoculated with 400 Glornus etunicaturn spores

growth of two dissimilar species (Christie et al 1978) As dis- cussed above this approach was unnecessary in the present experiments because of the particular comparisons and ques- tions addressed and because the dominance conferred by mycorrhizal fungi or P fertilization was complete ie when mycorrhizal A gerardii experienced little if any competition from K pyranidata and showed growth responses similar to a single A gerardii growing alone Similarly without mycorrhizae or P fertilization A gerardii did not grow appreciably and conferred no competitive stress on K pyranidata We are currently expanding our studies of the relationship between mycorrhizal symbiosis and plant competition to include substitutive (replacement series) experiments in the presence and absence of VAM fungi and further studies on the specific mechanisms by which VAM fungi alter patterns or competition for nutrients among neighbors

In plant communities mycorrhizal hyphae may form interconnections between plants of similar or dissimilar species (Chiariello et al 1982) Nutrient levels might be stabilized within a local neighborhood by transfer of nutrient from nutrient-rich plants to nutrient-poor plants (Whittingham and Read 1982) Francis and Read (1984) further proposed that seedling establishment may be promoted by mycorrhizal hyphal connections since nutrient transfer to seedlings is enhanced if they are shaded Thus mycorrhizal nutrient transfer may result in an even distribution of available resources among neighboring plants similar to the pattern resulting from rhizomatous nutrient transfer among adjacent shoots in clonal herbs (Hartnett and Bazzaz 1983 1985) It may be hypo- thesized therefore that mycorrhizal-mediated nutrient distribution among neighboring plants may contribute toward

coexistence and reduced dominance by promoting equivalence of competitors rather than niche partitioning Goldberg and Werner (1983) proposed that equivalence of competitors may allow coexistence but suggested a very different mechanism involving selection for equivalence in competitive effects among cooccurring species

Although potential nutrient transfer was not measured directly in this study interplant transfer of nutrients can be indicated by plant growth responses in experimental studies (Francis et al 1986) The growth responses of plants in these pairwise competition experiments are inconsistent with the hypothesis of mycorrhizal-mediated equivalence of competitors due to nutrient transfer Rather these competition studies suggest that mycorrhizal dependence of the plant species may be the most important determinant of whether or in which directions nutrients may be transferred via mycorrhizae Cer- tainly in the mycorrhizal condition A gerardii vegetation is large enough that K pyranidata is shaded However if nutrient transfer to K pyranidata did occur it resulted in no significant plant growth response Considering the poor growth performance of K pyranidata when paired with mycorrhizal A gerardii transfer from K pyranidata to A gerardii (ie parasitism on the lesser dependent plant species) could more easily be explained Variation in the degree of mycorrhizal dependence among interspecific neighbors in the field may greatly influence patterns of interspecific nutrient transfer between them This variation and its consequences for competitive relationships and community structure have not been considered in previous studies

These results strongly suggest that mycorrhizal symbiosis may be a crucial determinant of a given plants competitive

Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

2614 CAN J BOT VOL 67 1989

ability allowing mycorrhizal-dependent plants to out- compete less dependent or nondependent species This could explain the dominance of mycotrophic species in sites of low mineral availability and why nondependent or only faculta- tively dependent species tend to dominate in soils with low mycorrhizal fungus inoculum potential such as mine spoils or other disturbed sites (Miller 1987) The present results indicate that mycorrhizal fungi can determine the balance between win- ners and losers in local neighborhood competition and thus patterns of coexistence species richness and dominance may be modulated by mycorrhizal associations This also suggests that neighborhood competition may be influenced by abiotic or biotic soil factors that do not necessarily affect competing plants directly but rather indirectly by influencing mycorrhizal colonization and abundance

In tallgrass prairie the temporal niche partitioning of the C3 and C4 grasses and forbs into warm- and cool-season guilds may contribute to their persistent coexistence by reducing competition (Williams and Markley 1973) The results reported here suggest that phenologic separation of these groups would also prevent competitive suppression of several species by the warm-season grasses conferred by their mycorrhizal dependence Hayman (1983) demonstrated that mycorrhizal fungi cannot take up P at low temperatures (lt 7degC) Considering the ubiquitous nature of these fungi and their abundance in tallgrass prairie soils (Hetrick and Bloom 1983) the competitive advantage they confer on warm-season species could best be avoided by growing in cooler seasons when these fungi are metabolically inactive

Since K pyranidata and A gerardii grow most rapidly in different seasons competition between them may be limited to periods in early and late summer when environmental conditions support some growth of both plant species It is interesting to speculate whether mycorrhizal fungi might contribute to the transition from dominance of cool-season to warm-season plants in late spring and vice versa in fall For instance when soils warm in early summer could increased mycorrhizal activity contribute toward shifting the balance of dominance from cool- to warm-season plants by altering their relative competitive abilities In fall could declining mycorrhizal activity in cooler soils again shift dominance to less mycorrhizal dependent cool-season species Christie and Detling (1982) showed that the relative competitive abilities of C3 and C mixed-grass prairie species reversed under different day - night temperature regimes but the degree to which temperature-dependent mycorrhizal development mediated this reversal is unknown Further research will be necessary to test these hypotheses

Acknowledgement This research was partially supported by the National

Science Foundation Long-Term Ecological Research Program (grant BSR- 85-14327)

BAZZAZ F A and PARRISH J A D 1982 Organization of grassland communities In Grasses and grasslands systematics and ecology Edited by J R Estes R J Tyrl and J N Brunker University of Oklahoma Press Norman OK pp 233-254

BERENDSE F 1982 Competition between plant populations with different rooting depths Oecologia 53 50 -55

1983 Interspecific competition and niche differentiation between Plantago lanceolata ind Anthoxanthum odoratum in a natural hayfield J Ecol 71 379-380

BERGELSON J M and CRAWLEY J M 1988 Mycorrhizal infection and plant species diversity Nature (London) 334 202

CHIARIELLO N HICKMAN J C and MOONEY H A 1982 Endo- mycorrhizal role for interspecific transfer of phosphorus in a community of annual plants Science (Washington DC) 217 941 -943

CHRISTIE E K and DETLING J K 1982 Analysis of interference between C3 and C grasses in relation to temperature and soil nitro- gen supply Ecology 63 1277 - 1284

CHRISTIE P NEWMAN E I and CAMPBELL R 1978 The influence of neighboring grassland plants on each others endomycorrhizas and root-surface microorganisms Soil Biol Biochem 10 521 -527

CLEMENTS F E 1949 Dynamics of vegetation Edited by B W Allred and E S Clements H W Wilson Co New York

COLLINS S L 1987 Interaction of disturbances in tallgrass prairie a field experiment Ecology 68 1243 - 1250

DANIELS B A and SKIPPER H D 1982 Methods for the recovery and quantitative estimation of propagules from soil In Methods and principles of mycorrhizal research Edited by N C Schenck American Phytopathological Society St Paul MN pp 29- 37

DANIELS B A MCCOOL P M and MENGE J A 1981 Compar- ative inoculum potential of spores of six vesicular-arbuscular mycorrhizal fungi New Phytol 89 385 -391

FITTER A H 1977 Influence of mycorrhizal infection on competition for phosphorus and potassium by two grasses New phytoiT 79 119- 125

FRANCIS R and READ D J 1984 Direct transfer of carbon between plants connected by vesicular-arbuscular mycorrhizal myce- lium Nature (London) 307 53-56

FRANCIS R FINLAY R D and READ D J 1986 Vesicular- arbuscular mycorrhiza in natural vegetation systems IV Transfer of nutrients in inter- and intra-specific combinations of host plants New Phytol 102 103 - 11 1

GOLDBERG D E and WERNER P A 1983 Equivalence of competitors in plant communities a null hypothesis and a field experimental approach Am J Bot 70 1098- 1104

GRIME J P MACKEY J M L ITILLIER S H and READ D J 1987 Floristic diversity in a model system using experimental microcosms Nature (London) 328 420 -422

1988 Reply Nature (London) 334 202 HALL I R 1978 Effects of endomycorrhizas on the competitive abi-

lity of while clover NZ J Agric Res 21 509-515 HARPER J L 1977 Population biology of plants Academic Press

London 1982 After description In The plant community as a work-

ing mechanism Edited by E I Newman Blackwell Scientific Publications Oxford pp 1 1 -26

HARTNETT D C and BAZZAZ F A 1983 Physiological integration among intraclonal ramets in Solidago canadensis Ecology 64 779-788

1985 The integration of neighborhood effects by clonal genets in Solidago canadensis L J Ecol 73 415 -427

HAYMAN D S 1983 The physiology of vesicular-arbuscular endo- mycorrhizal symbiosis Can J Bot 61 944-963

HETRICK B A D and BLOOM J 1983 Vesicular-arbuscular mycorrhizal fungi associated with native tall grass prairie and culti- vated winter wheat Can J Bot 61 2140-2146

HETRICK B A D KITT D G and WILSON G T 1986 The influence of phosphorus fertilization drought fungal species and soil microorganisms on mycorrhizal growth response in tallgrass prairie plants Can J Bot 64 1199- 1203

1988a Mycorrhizal dependence and growth habit of warm- season and cool-season tallgrass prairie plants Can J Bot 66 1376-1380

HETRICK B A D LESLIE J F WILSON G T and KITT D G 19886 Physical and topological assessment of VA-mycorrhizal fungus effect on root architecture of big bluestem New Phytol 110 85-96

Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL 2615

MILLER R M 1987 The ecology of vesicular-arbuscular mycorrhizae in grass- and shrublands In Ecophysiology of VA mycorrhizal plants Edited by G R Safir CRC Press Inc Boca Raton FL pp 135- 170

PARRISH J A D and BAZZAZ F A 1979 Differences in pollina- tion niche relationships in early and late successional plant communities Ecology 60 597 -610

PHILLIPS J M and HAYMAN D S 1970 Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection Trans Br Mycol Soc 55 158-160

PICKETT S T A 1980 Non-equilibrium coexistence of plants Bull Torrey Bot Club 107 238-248

WEAVER J E 1954 North American prairie Johnson Publishing Co Lincoln NE

WEAVER J E and CLEMENTS F E 1938 Plant ecology McGraw- Hill Book Co Inc New York

WHITTINGHAM J and READ D J 1982 Vesicular- arbuscular mycorrhiza in natural vegetation systems 111 Nutrient transfer between plants with mycorrhizal interconnections New Phytol 90 277-284

WILLIAMS J HI and MARKLEY E J L 1973 The photosynthetic pathway type of North American shortgrass prairie species and some ecological implications Photosynthetica (Prague) 7 262-270

WILSON G W T HETRICK B A D and KITT D G 1988 Sup- pression of mycorrhizal growth response of big bluestem by nonsterile soil Mycologia 80 338-343

Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

This article has been cited by

1 A Montesinos-Navarro J G Segarra-Moragues A Valiente-Banuet M Verduacute 2012 The network structure of plant-arbuscularmycorrhizal fungi New Phytologist 1942 536-547 [CrossRef]

2 H Chen R Q Wang X L Ge J Zhang N Du W Wang J Liu 2012 Competition and soil fungi affect the physiologicaland growth traits of an alien and a native tree species Photosynthetica 501 77-85 [CrossRef]

3 Johann P Muumlller Ceacuteline Hauzy Florence D Hulot 2012 Ingredients for protist coexistence competition endosymbiosis anda pinch of biochemical interactions Journal of Animal Ecology 811 222-232 [CrossRef]

4 Nicolas Gross Yoann Le Bagousse-Pinguet Pierre Liancourt Carlos Urcelay Roumet Catherine Sandra Lavorel 2010 Trait-mediated effect of arbuscular mycorrhiza on the competitive effect and response of a monopolistic species Functional Ecology245 1122-1132 [CrossRef]

5 Aline Danieli-Silva Alexandre Uhlmann Joseacute Vicente-Silva Sidney Luiz Stuumlrmer 2010 How mycorrhizal associations and plantdensity influence intra- and inter-specific competition in two tropical tree species Cabralea canjerana (Vell) Mart and Lafoensiapacari ASt-Hil Plant and Soil 3301-2 185-193 [CrossRef]

6 Manzoor A Shah Zafar A Reshi Damase P Khasa 2009 Arbuscular Mycorrhizas Drivers or Passengers of Alien Plant InvasionThe Botanical Review 754 397-417 [CrossRef]

7 Yan Chen Jian-gang Yuan Zhong-yi Yang Guo-rong Xin Ling Fan 2008 Associations between arbuscular mycorrhizal fungiand Rhynchrelyrum repens in abandoned quarries in southern China Plant and Soil 3041-2 257-266 [CrossRef]

8 Somereet Nijjer William E Rogers Cin-Ty A Lee Evan Siemann 2008 The effects of soil biota and fertilization on the successof Sapium sebiferum Applied Soil Ecology 381 1-11 [CrossRef]

9 References 637-768 [CrossRef]10 Ragan M Callaway Judy Kim Bruce E Mahall 2006 Defoliation of Centaurea solstitialis Stimulates Compensatory Growth

and Intensifies Negative Effects on Neighbors Biological Invasions 86 1389-1397 [CrossRef]11 Nicole Cavender Michael Knee 2006 Relationship of seed source and arbuscular mycorrhizal fungi inoculum type to growth

and colonization of big bluestem (Andropogon gerardii) Plant and Soil 2851-2 57-65 [CrossRef]12 Q Yao H H Zhu J Z Chen P Christie 2005 Influence of an Arbuscular Mycorrhizal Fungus on Competition for Phosphorus

Between Sweet Orange and a Leguminous Herb Journal of Plant Nutrition 2812 2179-2192 [CrossRef]13 James Umbanhowar Kevin McCann 2005 Simple rules for the coexistence and competitive dominance of plants mediated by

mycorrhizal fungi Ecology Letters 83 247-252 [CrossRef]14 Ragan M Callaway Giles C Thelen Sara Barth Philip W Ramsey James E Gannon 2004 SOIL FUNGI ALTER

INTERACTIONS BETWEEN THE INVADER CENTAUREA MACULOSA AND NORTH AMERICAN NATIVESEcology 854 1062-1071 [CrossRef]

15 Miranda M Hart Richard J Reader John N Klironomos 2003 Plant coexistence mediated by arbuscular mycorrhizal fungiTrends in Ecology amp Evolution 188 418-423 [CrossRef]

16 Carlos Urcelay Sandra Daz 2003 The mycorrhizal dependence of subordinates determines the effect of arbuscular mycorrhizalfungi on plant diversity Ecology Letters 65 388-391 [CrossRef]

17 M-M Kytoumlviita M Vestberg J Tuomi 2003 A TEST OF MUTUAL AID IN COMMON MYCORRHIZAL NETWORKSESTABLISHED VEGETATION NEGATES BENEFIT IN SEEDLINGS Ecology 844 898-906 [CrossRef]

18 Marcel G A van der Heijden Andres Wiemken Ian R Sanders 2003 Different arbuscular mycorrhizal fungi alter coexistenceand resource distribution between co-occurring plant New Phytologist 1573 569-578 [CrossRef]

19 Ragan M Callaway Bruce E Mahall Chris Wicks Joel Pankey Catherine Zabinski 2003 SOIL FUNGI AND THE EFFECTSOF AN INVASIVE FORB ON GRASSES NEIGHBOR IDENTITY MATTERS Ecology 841 129-135 [CrossRef]

20 Catherine A Gehring Julie E Wolf Tad C Theimer 2002 Terrestrial vertebrates promote arbuscular mycorrhizal fungaldiversity and inoculum potential in a rain forest soil Ecology Letters 54 540-548 [CrossRef]

21 Linda J Kennedy Ronald L Tiller Jean C Stutz 2002 Associations between arbuscular mycorrhizal fungi and Sporoboluswrightii in riparian habitats in arid South-western North America Journal of Arid Environments 503 459-475 [CrossRef]

22 Ragan Callaway Beth Newingham Cathy A Zabinski Bruce E Mahall 2001 Compensatory growth and competitive ability ofan invasive weed are enhanced by soil fungi and native neighbours Ecology Letters 45 429-433 [CrossRef]

23 Duane A Peltzer 2001 Plant responses to competition and soil origin across a prairie-forest boundary Journal of Ecology 892176-185 [CrossRef]

Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

24 Jana Rydlovaacute Miroslav Vosaacutetka 2001 Associations of dominant plant species with arbuscular mycorrhizal fungi during vegetationdevelopment on coal mine spoil banks Folia Geobotanica 361 85-97 [CrossRef]

25 Jeffrey W Matthews Keith Clay 2001 INFLUENCE OF FUNGAL ENDOPHYTE INFECTION ON PLANTndashSOILFEEDBACK AND COMMUNITY INTERACTIONS Ecology 822 500-509 [CrossRef]

26 MD Smith DC Hartnett CW Rice 2000 Effects of long-term fungicide applications on microbial properties in tallgrassprairie soil Soil Biology and Biochemistry 327 935-946 [CrossRef]

27 John N Klironomos Jenny McCune Miranda Hart John Neville 2000 The influence of arbuscular mycorrhizae on therelationship between plant diversity and productivity Ecology Letters 32 137-141 [CrossRef]

28 David C Hartnett Gail W T Wilson 1999 MYCORRHIZAE INFLUENCE PLANT COMMUNITY STRUCTURE ANDDIVERSITY IN TALLGRASS PRAIRIE Ecology 804 1187-1195 [CrossRef]

29 Marilyn J Marler Catherine A Zabinski Ragan M Callaway 1999 MYCORRHIZAE INDIRECTLY ENHANCECOMPETITIVE EFFECTS OF AN INVASIVE FORB ON A NATIVE BUNCHGRASS Ecology 804 1180-1186 [CrossRef]

30 David D Tarkalson Von D Jolley Charles W Robbins Richard E Terry 1998 Mycorrhizal colonization and nutrient uptakeof dry bean in manure and compost manure treated subsoil and untreated topsoil and subsoil Journal of Plant Nutrition 2191867-1878 [CrossRef]

31 David D Tarkalson Rosemary L Pendleton Von D Jolley Charles W Robbins Richard E Terry 1998 Preparing and stainingmycorrhizal structures in dry bean sweet corn and wheat using a block digester Communications in Soil Science and Plant Analysis2915-16 2263-2268 [CrossRef]

32 Hana Skaacutelovaacute Miroslav Vosaacutetka 1998 Growth response of threeFestuca rubra clones to light quality and arbuscular mycorrhizaFolia Geobotanica 332 159-169 [CrossRef]

33 Sylvia D Torti P D Coley David P Janos 1997 Vesicular-arbuscular mycorrhizae in two tropical monodominant trees Journalof Tropical Ecology 1304 623 [CrossRef]

34 Erica A Corbett Roger C Anderson Cassandra S Rodgers 1996 Prairie Revegetation of a Strip Mine in Illinois Fifteen Yearsafter Establishment Restoration Ecology 44 346-354 [CrossRef]

35 Walter K Dodds Geoffrey M Henebry 1995 Simulation of responses of community structure to species interactions driven byphenotypic change Ecological Modelling 791-3 85-94 [CrossRef]

36 Laura L Nelson Edith B Allen 1993 Restoration of Stipa pulchra Grasslands Effects of Mycorrhizae and Competition fromAvena barbata Restoration Ecology 11 40-50 [CrossRef]

37 Edith B Allen Joseph P Cannon Michael F Allen 1993 Controls for rhizosphere microorganisms to study effects of vesicular-arbuscular mycorrhizae on Artemisia tridentata Mycorrhiza 24 147-152 [CrossRef]

38 IR Sanders AH Fitter 1992 Evidence for differential responses between host-fungus combinations of vesicular-arbuscularmycorrhizas from a grassland Mycological Research 966 415-419 [CrossRef]

39 D J Read 1991 Mycorrhizas in ecosystems Experientia 474 376-391 [CrossRef]40 Chantal Hamel Donald L Smith 1991 Plant development in a mycorrhizal field-grown mixture Soil Biology and Biochemistry

237 661-665 [CrossRef]41 M BrundrettMycorrhizas in Natural Ecosystems 21 171-313 [CrossRef]

Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL 2609

Although both warm- and cool-season tallgrass prairie grasses are mycorrhizal they differ significantly in dependence on mycorrhizal symbiosis for nutrient acquisition and growth (mycorrhizal dependence is estimated as (dry weight of inoculated plants - dry weight of noninoculated plants) divided by dry weight of inoculated plants Hetrick et al 1988~) The warm-season grass seedlings display extremely high dependence (ca 99) failing to grow appreciably in the absence of the symbiosis whereas cool-season grass seedlings are more variable in dependence some significantly inhibited by mycorrhizal infection (- 15 to 76)

Mycorrhizal symbiosis can alter the competitive ability of plants (Fitter 1977 Hall 1978) Most studies of plant competition have been phenomenological measuring the negative effects on the performance o f plants imposed by their neighbors (interference sensu Harper 1977) and the specific mechanism(s) of interference (ie competition for limiting nutrients light or water) or the specific mechanism(s) by which mycorrhizal symbiosis alter competition are very dif- ficult to identify experimentally because they are interdepen- dent Mycorrhizal symbioses are likely to directly influence the relative abilities of plants to compete for limiting nutrients but enhanced relative growth rates resulting from increased nutrient uptake may in turn increase their ability to compete for light above ground Regardless of the specific mechanism(s) or interference this known relationship between mycorrhizal dependence and competitive ability may influence patterns of species richness and relative abundance and other spatial and (or) temporal aspects of plant community structure Whether mycorrhizal symbioses influence plant community structure by suppression of mycorrhiza-inhibited (opposite of mycorrhiza- dependent) dominants or enhancing evenness of species abun- dances through translocation of resources to subordinate species via hyphal interconnections or other mechanisms has been the subject of recent debate (Grime et al 1987 1988 Bergelson and Crawley 1988) Regardless of the specific mechanism by which mycorrhizal fungi affect resource availability to a given plant they may increase plant species diversity (species richness and (or) evenness) if they decrease the competitive ability of abundance of competitive dominants relative to subordinate species or they may reduce diversity if the symbiosis is of greater relative benefit to the dominant species in the community Few studies have examined the influence of mycorrhizal symbiosis on competitive interactions between naturally cooccurring plant species

These studies explore the mycorrhizal dependence of two important tallgrass prairie species A gerardii (warm season) and K pyranidata (cool season) and assess the consequences of the mycorrhizal symbiosis for competition between them in a greenhouse setting The study was designed to assess the

effect of interspecific interference on target plants under vary- ing conditions of mycorrhizal symbiosis and soil fertility levels

I Materials and methods

To determine the importance of vesicular-ahuscular myconhizal (VAM) fungi for growth of big bluestem (A gerardii Vit) and prairie junegrass (K pyranidata L) 2-week-old seedlings of each species were planted in 6 x 25 cm pots containing 425 g (dry weight) of pasteurized prairie soil (steam pasteurized for 2 h at 80degC) Soil was freshly collected from Konza Prairie Research Natural Area Man- hattan KS (Chase silty clay loam) and contained 10 ppm plant- available phosphorus (Bray test 1) Seed of big bluestem was provided

by the Soil Conservation Service Plant Materials Center Manhattan KS and junegrass seed was supplied by the Upper Colorado Environ- mental Plant Center Meeker CO One-half of the pots received 30 ppm P applied to the soil surface in 10-mL aliquots of a KH2P04 solution Six phosphorus-amended pots and six nonamended pots were selected as controls The seedlings of the remaining pots were each inoculated with 400 Glomus etunicatum Becker and Gerd spores This isolate originally obtained from Konza Prairie was sub- cultured on sudangrass (Sorghum vulgare var sudanense (Piper) Hitch) Spores were then collected from pot cultures by wet sieving decanting and sucrose density gradient centrifugation (Daniels and Skipper 1982) Spores were suspended in distilled water and pipetted (400 sporesmL) onto the roots of each seedling at transplanting These pots were then amended with 10 mL of a 0 15 30 or 45 ppm (active ingredient) Benomyl (Tersan 1991 E I duPont de Nemours amp Co Wilmington DE) solution Thus there were 10 treatments (two P treatments (amended and nonamended) x four fungicide levels) applied to myconhizal fungus inoculated plants and a noninoculated control for each of the two prairie grasses with six replicate pots per treatment

To assess the effect of interspecific competition on big bluestem and prairie junegrass growth and root colonization A gerardii and K pyranidata seeds were germinated in vermiculite Two weeks after emergence an A gerardii a K pyranidata or one of each seedling was transplanted into 6 x 25 cm plastic pot containing 450 g (dry weight) of steam-pasteurized soil or nonsterile soil Seedlings planted alone were centered in the pot whereas seedlings that were planted two per pot (one A gerardii and one K pyraniduta) were spaced approximately 2 cm apart Although resulting in different plant densities this additive rather than substitutive design (Harper 1977) was chosen as the most appropriate because the goal was not to compare the competitive effect of a big bluestem versus junegrass on a target plant (intraspecific vs interspecific interference) but rather to compare the effect of interspecific interference in the presence versus absence of the myconhizal symbiosis

Pots containing pasteurized soil were subdivided into three groups of 28 pots The seedlings of one group were inoculated with 400 G etunicatum spores per pot The second subgroup received 10 mL of a KH2P04 solution (20 ppm P) applied onto the soil surface The third subgroup was left noninoculated and nonarnended All nonsterile soil was left untreated Thus there were 16 treatments each containing seven replicate pots

Experimental approaches such as this one invevitably involve com- promises between maximum precision realism and generality (Harper 1982) The Benomyl treatments used in the above experiment likely alter other components of the soil microflora and thus the responses observed cannot be attributed solely to an abundance of myconhizal fungi Thus this competition study was subsequently repeated but expanded to include several additional treatments Soil treatments included pasteurized soil nonsterile soil and pasteurized soil amended with 50 mL sieved suspension of nonsterile soil to return other components of the natural soil microflora while still experimentally controlling fungal abundance Nonsterile soil sieved suspension was obtained by blending 1100 g nonsterile prairie soil into 55 L (200 gL) sterile distilled water using a Waring blender and passing the mixture through a 38-pm sieve to remove indigenous VAM fungi The sieved suspension contained 470 colony-forming units (cfu)mL of fungi and 66 x lo6 cfumL of bacteria as estimated by dilution-plating sieved suspensions onto either peptone yeast extract agar or 06 potato dextrose agar (Difco Laboratories Detroit MI) amended with 100 pgmL each of streptomycin sulfate and chloramphenicol Colonies were counted after 7 days at 22OC Either an A gerardii a K pyraniduta or one of each seedling was planted into a pot as before Each soil treatment was amended with either 0 25 or 50 ppm P (KH2P04) applied as a soil drench One-half of the treatments received 400 spores G etunicatum as described earlier Thus this study had 60 treatments with six replicate pots per treatment

For all three experiments pots were arranged in randomized com-

Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

2610 CAN J BOT VOL 67 1989




















Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL







Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y









25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 ppm P 50 pprn P










25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 ppm P 50 pprn P

-- - - - -



Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL


Root to shoot ratio






25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 pprn P 50 pprn P








Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

2614 CAN J BOT VOL 67 1989

































Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL 2615










Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

























Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y


















Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

2610 CAN J BOT VOL 67 1989




















Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL







Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y









25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 ppm P 50 pprn P










25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 ppm P 50 pprn P

-- - - - -



Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL


Root to shoot ratio






25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 pprn P 50 pprn P








Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

2614 CAN J BOT VOL 67 1989

































Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL 2615










Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

























Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y


















Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL







Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y









25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 ppm P 50 pprn P










25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 ppm P 50 pprn P

-- - - - -



Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL


Root to shoot ratio






25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 pprn P 50 pprn P








Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

2614 CAN J BOT VOL 67 1989

































Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL 2615










Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

























Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y


















Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y









25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 ppm P 50 pprn P










25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 ppm P 50 pprn P

-- - - - -



Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL


Root to shoot ratio






25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 pprn P 50 pprn P








Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

2614 CAN J BOT VOL 67 1989

































Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL 2615










Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

























Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y


















Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL


Root to shoot ratio






25 pprn P 50 pprn P




25 pprn P 50 pprn P


25 pprn P 50 pprn P








Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

2614 CAN J BOT VOL 67 1989

































Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL 2615










Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

























Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y


















Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

2614 CAN J BOT VOL 67 1989

































Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL 2615










Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

























Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y


















Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

HETRICK ET AL 2615










Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

























Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y


















Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

























Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y


















Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y


















Can

J B

ot D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y U

NIV

CH

ICA

GO

on

082

613

For

pers

onal

use

onl

y

relationship between mycorrhizal dependence and competitive ability of two tallgrass prairie grasses

Documents