OIKOS 8l:495-510. Copenhagen 1998

Vesicular-arbuscular mycorrhizae influence Mount St. Helenspioneer species in greenhouse experiments

Jonathan H. Titus and Roger del Moral

Titus, J. H. and del Moral , R. 1998. Vesicular-arbuscular mycorrhizae inf luenccMount St . Helens pioncer species in greenhouse exper imcnts. Oikos 81: ,+95 510.

Vesicular-arbuscular mycorrhizae (VAM) are present in most terrestrial ecosystemsand play a major role in community structure and fr-rnction. However. their role inprimary succession remains poorly undcrstood. Two greenhouse studies examined therole of VAM in Mount St. Helens pioneer species under thrcc nutrient regimes andfour competitivc scenarios. Nulricnt levels were complete, complete without phospho-rus ( - P). and tap water (very low nutrient levels). In tap water a ncgative effect fromVAM colonization was observed perhaps due to parasitic action of the VAM fungi.A weak but apparcnt benefit liom VAM occurred in the -P treatment since plantsin the P treatmcnt were usually not less in biomass than those in the completenutrient treatment and VAM colonizalion levels were greater in the P treatment.VAM colonization wns more bcneficial to plants under the complete nutrienttreatment than undcr the tap water treatment. VAM assisted the facultativelymycotrophic Hypotltaeris rndicatu in competition with thc non-mycotrophic Care-rrnertensii. Lack of VAM improved the competitive ability of Curer ntertensii when incompelition with lacultatively mycotrophic species. However, VAM did not signifi-cantly influence competitive outcomes between facultatively mycotrophic species.

J. H. Tirus antl R. del Morul. Dept ol Botuny, KB-15. Ltnir. of Wasltirtgton, Seattlc,WA 98195, USA (presenr address o.f JHT: Dept o/ Botany, Fat'ultr,o/ BiologitalStiences. Unit. o.f South Bohenia, Brutiiorska 31, CZ-37005 Cc;kt BuLllj,'ri,e. C:r'r'ltRe puh I k [t itus(ii.b io.hl. j r: u.t :]).

The 1980 eruption of Mount St. Helens produced adevastated landscape devoid of both plants and vesicu-lar-arbuscular mycorrhizae (VAM) (Al len et al. 1992, J.H. Titus unpubl.). This catastrophic disturbance cre-ated a barren landscape and initiated primary succes-sion. The role of VAM in primary succession is poorlyunderstood and is the subject of this study.

The role of VAM in nutrient uptake, particularlyphosphorus, is central to the symbiosis. Plants colo-nized by VAM fungi usually exhibit improved growthdue to enhanced nutrient uptake (e.g., Smith et al.1986). This is due to the addit ional absorbing surfaceprovided by the external hyphae (Hatt ingh et al. 1973).However, in some situations the association may beneutral or even detrimental to the host plant (Allen and

Allen 1986; Fit ter 1986, Hetr ick et al. 1986, Andersonand Liberta 1989). There are many reasons for a lack ofbenefits from VAM, these include high phosphoruslevels (Fit ter 1977. Schwab et al. 1983). Under nutr ient-poor conditions. a parasitic effect may occur becauseVAM fungi continue to receive photosynthate from aplant but have little phosphorus to offer in return(Allen 1991, Boerner 1992). In addit ion, VAM maybenefit the plant only during a brief period (tritter1989). Thus, the manner in which VAM act underdiff-erent nutrient regimes is of interest.

Competitive interactions among plants can shapedistribution patterns and relative species abundanceand may also affect the adaptive traits of competingplant species (Keddy 1989). VAM may mediate com-

Accepted 22 Septcmber 1997

Copyright iO OIKOS 1998rssN 0030-1299Printed in lreland all rights rescrvecl

o lKoS 8 l :3 ( le9 t l ) 495

Table l. Percent VAM colonization under three fertilizer treatments. Comparisons were by the nonparametric Kruskal-Wallistest with chi-square correction for ties with P indicating significance. Different superscripts show mycorrhizal levels that differat z:0.05 based on thc nonparametric variant of Tukey's honcstly signilicant difference test (mean * standard deviation,n: 12).

Species Nutr ient addi t ion le le ls

None Complete minus P Complete

Anaphctlis margar itat'eaCurex ntertensiiEpi lob iun an gusl il0 li un1E p il o h ittnt h r ut hv t; ar p u ntHieraciunt alhifloruntHypctchaeris rudicatuPenstemon urAtellii

l 0 + 6 '0'

37 + 16b22 + l8 .b27 +21"l t + 6 .l 9 + 6 '

1 3 + 1 5 .0'

3 5 + 9 b3 5 + l 7 b1 9 + l 9 '2 9 + 2 l b1 2 + 1 6 ,

4 + 5 "0'

16 + 8 '8 + 6 .

25 + l8 '9 + 1 2 ' �

l 0 + l 6 '

0.096

0.0030.0030.7630.0070.066

Iable 2. ANOVA tables for the biomass of seven pioneer species under three fertilizer and two mycorrhizal treatmentslA G). Post-hoc shows the resul ts ofTukey's honest ly s igni f icant d i f ference test at . r :0.5 k:12). Fert i l izat ion1 : no nutrient addition, 2 : complete without phosphorus addition, 3 : complete nutrient addition. Mycorrhizae1 : inoculated. 2 : r'rot inoculated.

Species Source x- post-hoc

(see Figs.treatment:treatment:

PD F

Anaphali.snnrgarilacea

Carexnarlensii

Epibbiumangust(bliun'r

Epilohiunthrat:h.ycarpum

Hierat iuntctlbiflctrunt

Hypochaerisrudit'atu

Penstemont:urdvellii

FertilizationMycorrhizaeInteract ionFertilizationMycorrhizaeIntcraction

FertilizationMycorrhizaeIntcraction

FertilizationMycorrhizaeInteraction

FertilizationMycorrhizaeI nteraction

FertilizationMycorrhizaeInteractiou

Fert i l izat ionMycorrhizaeInteractior.r

I < 2 : 3

l < 3 < 2

l < 2 < 3

2I22I22I22I22I22I22I2

3s1.920.651 . 6 5

292.400.291 . 2 8

1 78 .5 82 . 1 80 .98

217.414 . l 50.60

68.801.623 . 3 8

l 1 7 . 5 90.003 . 1 3

182.627.41

14.24

0.0000.1220.2000.0000.5900.2830.0000.1450.3800.0000.0460.5490.0000.2070.0400.0000.9560.0s00.0000.0080.000

l < 22 < l

l < 2

< 3

< 3

| < 2 : 3

I < 2 < 32 < l

petitive interactions between plants and influence theresultant community structllre. Most plants form theVAM mutualism; thus. in order for VAM to change thecompetitive balance between plants the relationshipmust affect competing plants differentially. These inter-actions are especially important in dynamic communl-ties where both the density and type of VAM fungi andplant species are changing (Johnson et a1. 1991). Studiesof competition between early and late seral species havegenerally shown that late seral species exhibit bothgreater response to mycorrhizal colonization andgreater competitive ability with mycorrhizal coloniza-t ion (Al len and Allen 1990).

We conducted two experiments under greenhouseconditions: Experiment I tested lor interactions betweenmycorrhizae and nutrient levels among common pio-

496

neer species that are found on the Pumice Plain ofMount St. Helens. The hypotheses were as follows: Hn:Levels of mycorrhizal colonization of host plants donot differ at different soil nutrient levels, and H,,:Non-mycotrophic and facultatively mycotrophic speciesdo not dilfer in their response to mycorrhizal inoculumat different soil nutrient levels. Experiment II testedhow VAM might affect competitive outcomes betweenfour pioneer species. The hypotheses for this experi-ment were H,,: Mycorrhizal colonization levels of hostplants do not change with increased number of com-petitors or with competitor species, and H0: Non-mycotrophic and facultatively mycotrophic species dif-fer in their competitive relationships with other speciesdepending upon the presence or absence of VAM fun-gal inoculum.

a ) l K ( , S E l : l ( l 9 q b )

A Anap ha I i s ms rga ri t s c e a

T--r-

I-t-

*

3T

---t-

L"lI

I

o _' l--r-I l t r lI _

l-"1 |-rI

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o

+o

cTreaunents

Carex mertensii

c

oo; 4

. 9 r

Methods

Source and preparation of soil

Soil was collected from the Pumice plain during August1992. The Pumice Plain, which ranges in elevation from1150 to 1300 m, occupies an area of approximately 20km2 immediately north of the Mount St. Helens crater.The area was formed in the volcanic eruption of 1980by the deposit of over 100 m of pumice from theeruption. The material is extremely nutrient poor con-taining only trace levels of nutrients (del Moral and

OIKOS 81:3 f1998)

Mean+SDMean-SDMean+SEMean-SE

o Mean

-T- Mean+SDMean-SD

l---.l Mean+SEMean-SE

o Mean

Bliss 1993). Pumice Plain soil rarely contains VAMspores except in specialized microsites (J. H. Titusunpubl.).

Soil was sifted in a 0.4-cm mesh sieve to remove allcoarse particles. Plastic pots (10 cm x l0 cm) were fllledwith 80 g soil as well as 20 g of sterile perlite, tolncrease porosity. Mycorrhizal treatments were estab-lished by the addition of 30 g Bear Meadow soii(located l0 km northeast of the Pumice Plain, outsidethe blast zone, at a similar elevation as the PumicePlain) to each pot to provide VAM inoculum. Only onemorphological spore type was detected in Bear

I

tf

DB

B.

24

20

l 6bo@IA

E t z

DA

TreatnentsFig. 1. Box. and whisker plots of the biomass of seven pioneer species under three fertilizer and two mycorrhizal treatments.Treatment Abbreviations: A: inoculated, no nutrients acqea; n:-not inoculated, no nutrients added; C: inoculated, completenutr ients -P; D:not inoculated, complete nutr ients. . Pt E- inoculated, complete nutr ients; F:not inoculated, "o-plet .nutrients. Inoculated : pots with soil containing mycorrhizal propagules added. Nbt inoculated : pots with sterilized soil addedand mycorrhizal activity inhibited-by benomyl (n:12). See Table) for ANoVA tables. A. Anaphalis murgaritacea, B. Carexnertensii' C- Epilobiwn angustiJblium, D. Epitobium brachycarptun, E. Hieraciunt albiJlorum,'F. Hypoci)aeris raulicata, G.Penst emon car dw'e llii.

J.l o l-1-I

T-_t-_l " lt-I

g

Tl o l

T

TI

l o l

TI

*+

497

II

IEpilob ium angust ifo I ium

B C D E

Treainents

Epi I o b ium b roc hycarpum

I Mean+SDMean-SD

l---l Mean+SEMean-SE

D Me,an

-f Mean+SDMean-SD

T- Mean+SEMean-SE

o Mean

Treabnents

Figs. 1C, D.

c.

5 l ?

D

oo

E ?

Meadow soi l (14.6 * 13.9 spores per 100 ml soi l , deter-mined to be Glomus macrocarpum (Tul. & Tul) (J. H.Titus unpubl.)). Mycotrophic species collected at BearMeadow were VAM colonized and in the greenhouse,plants were readily VAM colonized when grown inBear Meadow soil. Bear Meadow soil was steamed for15 min, cooled and added to pots for the non-mycor-rhizal treatment. Steaming effectively eliminates mycor-rhizal inoculum potential (J. H. Titus unpubl.).

Maintenance of non-mycorrhizal conditions was as-sured by applying benomyl (benlate 50%r active ingredi-ent; Southern Mill Creek Products, Tampa, FL) atapproximately 25 mg (active ingredient) per I kg of soil(dry mass). Benomyl was applied in 50-ml aliquots perpot I week after planting and every 4 weeks thereafter.

498

Paul et al. (1989) found Benomyl to have no elfect onplants in the absence of fungi and is often used tocreate and maintain non-mycorrhizal conditions (e.g.Fit ter 1986, Fit ter and Nichols 1988, Hetr ick et al.1989, Hartnett et al. 1993). Benomyl suppresses patho-genic fungi as well as mycorrhizal fungi. To the extentthat pathogens are also suppressed, measured growthenhancement of untreated plants compared to thosetreated with fungicide may underestimate mycorrhizalbenefit (Carey et al. 1992).

Design

Experiment IThis experiment was conducted to determine if nutrientlevels affect the response of facultatively mycotrophic

il o lt l-rI

-rI

l o l

IT

l o l-rI

:

Tt=t-f

I

*+

8

T-'lL:_rI I

I ' lT

o-rtf,-6-

OIKOS 81:3 (1998)

E. Hieracium albiflorum

Treatments

Hypochoeris rudicato

:T

I

II I

l . l_TII

TT It f J

t l

l o l I- r tI

o

Tl o l-T.--t_o

o

+ -*rr-*-

--f---J.- L

T o

C DTreatments

trigs. 1E, F

oE ?

:rE

Mean+SDMean-SDMean+SEMean-SE

o Mean

F.

a 5

f r t

J

I

-

tr

Mean+SDMean-SDMean+SEMean-SEMean

and non-mycotrophic pioneer species to mycorrhizalinocula. Plants in both mycorrhizal and non-mycor-rhizal treatments were subjected to three different nutri-ent reglmes: tap water (i.e., very iow nutrient levels),10'% Colwell's solution without phosphorus, and l0%,Colwell's solution. Colwell's solution resembles naturalproportions of nutrients (Colwell 1943, R. B. Walker,Univ. of Washington, pers. comm.). The dilute solution(i.e., l0'%) was used to simulate nutrient poor condi-tions on the Pumice Plain. All pots were watered dailywith tap water. Fertilizer was applied in 50-ml aliquotsper pot at planting and at weekly intervals throughoutthe experiment. Sample size was twelve pots per nutri-ent regime per species.

The following five facultatively mycotrophic peren-

OIKOS 81:3 (1998)

nial species were used: Anaphalis margaritacea (L.)Benth & Hook., Epilobium angustifolium L., Hieraciumalbiflorunt Hook., Hypochaeris radicata L., and Penste-mon cardttellli Howell. The non-mycotrophic perennialCarex mertensii Prescott and the facultatively my-cotrophic annual Epilobium brachycarpum C. Presl werealso used (Allen et al. 1992, Chapin 1995, J. H. Titusunpubl.). These are common pioneer species on thePumice Plain (del Moral and Bliss 1993). Seeds werecollected August and September of 1992 from thePumice Plain. On 21 February, 1993 seeds were placedin Petri plates on filter paper and watered with tapwater. Seedlings were transferred into pots on 28February, 1993. Plants were harvested on 4 and 5 July,1993.

irt+I

Ia

TL:_.1I

_r_t o l

T

499

G Penstemon cardwellii

Treatnents

Fig. I G

u ^v J

A 2

Experiment IIThis experiment was conducted to determine if VAMmediates competitive interactions between pioneer spe-cies common on the Pumice Plain. More specifically" weinvestigated how VAM affected intra- and interspecificcompetitive relationships among four pioneer species.An additive experiment" using three facultatively my-cotrophic species and one non-mycotrophic species, wasdesigned to determine the competitive effects of 'neigh-

bor' plants on a 'target'. The slopes of the regressionsof target plant performance (e.g., biomass) with in-creasing neighbor density provide a quantitative esti-mate of competitive effect and allow statisticalcomparisons of the effects of different treatments. suchas mycorrhizae, on competitive ability (Goldberg andScheiner 1993). Zero slopes indicate no signiflcant inter-actions or effects; significant negative slopes indicatecompetitive effects; and signilicant positive slopes indi-cate direct or indirect beneficial effects. This additivestudy was conducted at low nutrient levels to approxi-mate conditions actually experienced by the target spe-cies on the Pumice Plain.

Seeds of Carex mertensii, Anaphalis margaritacea,Epilobium angustfoliwn and Hypochaeris radicata werecollected August and September, 1993 from the PumicePlain. On 24 January, 1994 seeds were placed in Petriplates on fllter paper and watered with tap water.Seedlings were transferred into pots on I February,1994. Single target seedlings were planted centrally ineach pot and surrounded by 0, 2, 4, and 8 evenlyspaced seedling neighbors of the same age in eachpossible intraspecific and interspecific target neighbor

500

n

Mean+SDMean-SDMean+SEMean-SE

o Mean

combination with flve replicates (tritter 1977, Hartnettet al. 1993). Plants were watered daily with tap waterand a 10%r Colwell's solution without phosphorus wasapplied in 50-ml aliquots at planting, one week afterplanting and at 2-week intervals thereafter. Plants wereharvested on 4 and 5 Julv. 1994. after flve months ofgrowth.

Experintents I and IIPots were arranged in a randomized block design andmaintained at 20 25"C in the Univ. of WashingtonBotany Greenhouse. Natural lighting was supple-mented by sodium lamps to provide a l6-h photo-period. Flats were rotated at 2-week intervals. Afterharvest. roots were washed free of soil and frozen untilexamination. Plants were dried for 3 d at 80'C: androot, shoot and reproductive dry weights measured tothe nearest 0.01 g.

Roots were washed, cleared and stained with trypanblue (Brundrett et al. 1994). Percent VAM colonizationwas estimated by placing a grid of 1-cm squares belowa Petri plate which contained the root sample under adissecting microscope. One hundred locations in whicha root crossed a line on the grid were scored formycorrhizae. Many samples were examined underhigher power to ascertain that the fungi were indeedVAM. Root segments containing vesicles, arbuscles,hyphae or intercellular hyphal coils were recorded ascolonized. The number of mycorrhizal "hits" is used asan estimate of percent root colonized (Brundrett et al.199q.

I

DA

T - ro . 5 l3 l o l Il - r - t

A I I ' Il o l o

- f

T ' lI

Tt-Jt l-rI

OIKOS 81:3 (1998)

Table 3a. Percent VAM colonization under four competitive regimes with four competitors.addition portion of the mycorrhizal treatment only (mean * standard deviation, n:5). SeeCarex is not included as a target species due to lack of mycorrhizal colonization.

Data were from the mycorrhizalTable 3b for statistical analysis.

Targetspecles

Density ofcompetitors

Competing species

Anaphalknargarllateo

Carermertenstt

Epilobiumangusti/bliunl

Hypochaerisradicata

Anaphalisntargaritacea

Epilobitunangustilblium

Hypochaerisradicata

02/8

02I

8

0248

9 + I8 + 68 + 9

1 2 + 7

9 + l5 + 4

l l + 1 15 + 3

2 2 + 9l 5 + 8l 0 + 56 + 4

25+26/ t I

1 4 + 79 + 6

2 2 + 91 6 + 71 0 + 52 + 1

2 5 + 2 61 3 + 7l 1 + 62 4 + t 9

9 +9 +8 +

I A L

9 + 1l 0 + 41 5 + 41 8 + 6

2 2 + 91 2 + 5l + 11 + l

22+95 + 3

1 8 + 3l l + 525+265 + 28 + 4

l 1 + 7

25 +263 + 33 + 21 + l

Data analysis

Experiments I and Experiment IITo determine if nutrient level or neighbor specles ordensity affected mycorrhizal colonization, the degreeof VAM colonization of each species was assessed bythe nonparametric Kruskal-Wallis test with a chi-square correction for ties (Zar 1984, Norusis 1993).Post-hoc tests were conducted by using the nonpara-metric variant of the Tukey's honestly signilicant dif-ference test (Zar 1984: p. 199).

The root:shoot ratio was determined using thebiomass of each. Root, shoot, and total dry biomassand the root:shoot ratio of mycorrhizal and non-myc-orrhizal treatments were compared by two-wayANOVA. Biomass and ratios were log transformedto improve normality and homoscedasticity. Post-hoc comparisons were conducted using Tukey's hon-estly signiflcant dilference test (Zar 1984, Norusis1993). Due to the paucity of reproductive individuals,flowers were included with total abovesroundbiomass.

Experiment IIFor each treatment combination the relationship be-tween plant performance and neighbor density wasexamined using linear regression for each biomassmeasure of target plant performance. The relationshipbetween target plant biomass and neighbor densityvaried among treatments and were nonlinear (nega-tive exponential) because as the number of neighborsincreased, they compete more intensely with one an-

otKOS 81:3 (199 i t )

other and their per-individual effect on the targetplant decreases. Therefore, log transformation of thetarget plant biomass produced linear relationshipsand homoscedastic variances. Hartnett et al. (1993)

found that using either number of neighbors or totalneighbor biomass as the independent variable yieldedthe same results; in this analysis we used the numberof neighbors.

Competition coefficients for each of the seven spe-cies growing in competition in each treatment combi-nation were calculated as the slope of the regressionof log target plant biomass against number of indi-viduals of the neighbor species. Regression parame-ters were compared between mycorrhizal andnon-mycorrhizal treatments using analysis of covarr-ance. Significant differences in slopes indicate thatmycorrhizae have altered competitive relationships(Goldberg and Scheiner 1993, Hartnett et al. 1993).

Results

Experiment I

Myc ctr r h iz al c o lonizat ionBenomyl effectively suppressed mycorrhizal colonizationin the non-mycorrhizal treatments. In the mycorrhizaltreatments, Carex was not colonized (Table 1). For E.angusti/itlium, E. brachycarpum, and Hypochaeris, the- P treatment had significantly higher VAM coloniza-tion levels.

501

Table 3b. Percent VAM colonization under four competitive regimes with four competitors. Comparisons were by the two-waynonparametric Kruskal-Wallis test and the nonparametric variant of Tukey's honestly significant different test at d:0.5 (r:5).Carex mertensii is not included as a target species due to lack of mycorrhizal colonization. Competing species: I : Anaphalismargaritacea,2: Carex mertensii,3 : Epilobium angustifoliun, 4: Hypot:haeris radicata. Density of neighbors: 1 :0 neighbors,2 :2 ne ighbo rs , 3 :4 ne ighbo rs , 4 :8 ne ighbo rs .

Species Source DF x2 post-hoc

Anaphalismargarilacea

EpilobiwnangusfiJblium

Hypochaerisradicata

Competing speciesDensity of neighborsInteractionCompeting speciesDensity of neighborsInteractionCompeting speciesDensity of neighborslnteraction

339339339

10.204.624 . 1 7

17.2337.4326.5914.7 |20.39

l . - )+

0 .0170.2020 . 1 1 80.0010.0000.0030.0020.0000.825

f r 1 , 4

A - 1 - ) 2 1

4 < 3 : 2 < l

A - ) _ l _ 1

) A a z I

Biomass responseRoot and shoot biomass responses were similar tothose of total biomass. Therefore, we discuss only totalbiomass results to improve clarity. Root:shoot ratioresults were not significant and will not be discussed.Biomass signiflcantly increased with increased nutrientievel for five species, but not for Carex and Hypochaeris(Table 2, Fig. lA-G). Epilobium brachycarpum andPenstemon had greater biomass in the mycorrhizaltreatment.

Interactions occur due to a differential response tothe presence of mycorrhizae across nutrient input levels(Zar 1984). Interactions occurred in Hypochaeris andPenstemon because biomass was greater under mycor-rhizal conditions for the complete fertilizer and -P

treatments, but biomass was lower in the tap watertreatment under mycorrhizal conditions than undernon-mycorrhizal conditions. This effect implies abeneficial mycorrhizal effect with nutrient additions anda negative effect at low nutrient levels. The interactionfor Hieracium illustrated a different effect, that is,biomass was greater in the tap water treatment andlower in the -P treatment under mycorrhizal condi-tions than under nonmycorrhizal conditions.

Experiment II

My c orr hiz al c olonizat ionPlants in the non-mycorrhizal treatment lacked VAM.In the mycorrhizal treatment, all plants were VAMexcept for Carex (Table 3a, b). VAM colonization inAnaphali.s was influenced by the identity, but not by thedensity of neighbor species. VAM colonization ofAnaphalis was least in competition with the non-VAMspecies Carex and greatest in competition withHypochaeris. For E. ungustfolium, VAM colonizationwas greatest when in competition with Anaphalis anddecreased with increased neighbor density. There wasalso a strong interaction between neighbor species iden-tity and density. Hypochaeris showed signiflcant differ-ences in VAM colonization level in relation to both

502

identity and density of neighbor species. VAM colo-nization levels were lowest when in competition withconspecifics, and pots with single Hypochaeris plantshad significantly greater VAM colonization levels thanthose in whrch Hypochaeris plants were subjected tocompetition.

BiomassAs in experiment I only the results for total biomass aredescribed here. Significant biomass decreases with in-creasing neighbor density were observed for all species(Tables 4 and 5, Figs 2-5). At the conclusion of theexperiment plants were small and, with the exception ofsingly grown plants, rarely achieved dry weights greaterthan I g.

Mycorrhizal Anapfutlis plants were larger than non-mycorrhizal plants when in competition wtth Carex(Fig. 2B). In addition, when Anaphallr plants were rncompetition wtth Carer under mycorrhizal conditions,biomass decreased significantly with increased Carexdensity. However, under non-mycorrhizal conditionsthere was no signiflcant competitive effect, i.e., slope :

0. Thus there was competition under mycorrhizal con-ditions, but not under non-mycorrhizal conditions.However, the competitive intensity was not significantlydifferent between the two treatments. An oppositetrend occurred when Anaphalis was in competition withE. angustiJblium (Ftg. 2C). That is, the slope wassteeper under non-mycorrhizal conditions than undermycorrhizal conditions, meaning that competition wasmore intense without mycorrhizae.

When Carex was in competition wrth Hypochaeris,plants in the non-mycorrhizal treatment were signifi-cantly greater in biomass (Fig. 3D). In addition, theslope was 0, indicating no competitive effects. Undermycorrhizal conditions wrth Hypochaens, biomass de-creased significantly with increased neighbor number.The difference in competitive intensity was not signifl-cant at p : 0.08. However, this low value of p is sugges-tive that competition may be more intense undermycorrhizal conditions and that non-mycorrhizalHypochaeris plants were less competitive. When Carex

O I K O S 8 l : l ( 1 9 9 8 )

Table 4. ANOVA tables for log biomass under four competitive regimes with four competitor species. Post-hoc shows the resultsof Tukels honestly significant difference test at d:0.5 (n:5). Inoculated: pots with soil containing mycorrhizal propagulesadded. Not inoculated - pots with sterilized soil added and mycorrhizal activitv inhibited bv benomvl. tlensitv of-neish6ors:l - . 0 n e i g h b o r s . . 2 - 2 r r e i g h b o r s . J : 4 n e i g h b o r s . 4 - 8 n e i g - h b o r s . M l c o r r h i z a e r r . o r . e n i , l - s o i i u i r h V A M p r o l a g u l e sadded, 2: sterilized soil added.

Target species Competitor Source DF F P post-hoc

Anaphalism0rgatttacea

Carexmertensu

Anaphalist11Ar gor tta(ea

Curexmertensii

EpilohitunangustiJblium

Hypoc:huerisrctdicata

Anaphulismargaritacea

Carexmerlensii

Epilobium0ngustiJoliutlt

Hypochaerisradicata

Anuphalismargarrlace0

Carermertensii

Epilohiuntangustiloliunt

Hypochaerisradicatct

Anaphalisntargaritacea

Carermerlensii

EpibbiumangustiJblium

Hyochaerisradicata

DensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMyoorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteractionDensityMycorrhizaeInteraction

33I33

17.470.32l . l 4

14.674.421 . 3 37.381.150.17

26.001 . 3 70 . l 86 . 3 13.660.92

\2 .270.300 . 1 3

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1 1 . 2 012.202.296.246.210.62

10.381.010.456.94

18.451 . 0 38.481.230.66

13.008.97t . 2 l

15 .253 1 . 1 64.7 66 .82

29.930.89

22.593 . 3 30 . 3 1

0 . 0 0 0 4 : 3 < 2 < 10.5780.3460 . 0 0 0 4 : 3 : 2 < 10.044 2 < 10 .2810 . 0 0 1 4 < t , 3 < t , 2 - t , 4 : 3 - _ 20 . 1 9 50 . 5 1 90 . 0 0 0 3 : 2 < 1 . 4 : 3 , 4 < 20.2490.9100 . 0 0 0 4 : 3 < 2 - l0.0650.4420 . 0 0 0 4 : 3 < 2 < |0 .5890.9440 . 0 0 0 4 < 3 , 3 : 2 . 3 < 1 . . 2 - 10 .3350.9560 . 0 0 0 4 : 3 , 4 : 2 , 3 < 2 , 2 < l0 . 0 0 1 | < 20.0970 . 0 0 2 4 - 3 , 4 < 2 : 1 , 3 : 2 , 3 < 10 . 0 1 8 1 < 20.6070 . 0 0 0 4 : 3 , 4 < 2 < t , 2 - 30.3090.7200 . 0 0 1 4 : 3 : 2 < 10 .000 | <20.3920 . 0 0 0 4 : 3 : 2 < I0 . 0 1 1 | < 20 . 5 8 10 . 0 0 0 4 : 3 < 1 , 4 < 2 : 1 , 3 : 20.005 2 < |0.3240 . 0 0 0 4 : 3 : 2 < t , 4 < 2 < 10.000 2 < |0.0070 . 0 0 1 4 : 3 < 1 , 4 : 2 , 2 : l0.000 2 < |0.4580 . 0 0 0 4 : 3 , 4 < 2 : 1 , 3 : 2 , 3 < l0.0780.821

EpikthiuntangustiJblium

Hypot'haerisradicatu

33I-l3

3I3-lI-l

was competlng intraspecifically, with Anaphalis andwith -8. angustiJitlium, slopes of both mycorrhizal andnon-mycorrhizal treatments were significant and theslopes did not differ (Fig. 3A-C). Constants showed asignificant negative mycorrhizal effect, i.e., when grownsingly Carex plants were greater in biomass undernon-mycorrhizal conditions (Table 5).

Epiktbiunt angustiJbliunt biomass was greater fornon-mycorrhizal treatment plants, except when in com-petition with Curex (Fig. 4.A D). Slopes of E. angusti-

.folium competing intraspecifically and wrth Anaphalis,

OIKOS 8 l :3 (1998)

(larex and Hypochaeris were significant under bothmycorrhizal and non-mycorrhizal treatments. Theslopes were not significantly different. Thus, -8. angusti-

folium plants were larger when non-mycorrhizal but theintensity of competition did not change with mycor-rhizal status.

In all cases, the mycorrhizal Hypochaenr. plants werelarger than the non-mycorrhizal plants (Fig. 5,A D).When Hypochaeris was subjected to competition withCarex, both the mycorrhizal and non-mycorrhizalslopes were significant (Fig. 5B). Total biomass de-

503

Table 5. Competition coefficients.for target species growing in intra- and interspecific competition calculated as the slope of theregressior of_ log target plant biomass against number of neighbors. Inocuiated: plants with soil containing mycorrhizalpropagules added. Not inoculated : plants with sterilized soil added and mycorrhizal activity inhibited by benomyl. Iiegressionparameters were compared by analysis of covariance. Asterisks indicate slopes dilferent from zero at a:0.05. Within eachspecies combination, different letter superscripts indicate that slopes or constants ofthe inoculated and not inoculated treatmentsdiffer at e:0.05. The P value shows the significance of the comparison between the two slopes or constants

Targetspecles

Competing species Competition coefficients Constants

Inoculated Not inoculated lnoculated Not inoculated P

Anaphalismargaritacea

Carermerlensii

Epilobiuntangustifolium

Hypochaerisradi('ata

Anap ha li s mur gar itaceuCarex nterlensiiE p i b b iunt an gus t iJb liu tnH v-pochaeris radicata

A naphalis mar gar itat eaCarex mertensiiEp ilobiunt mgu stifbliunlHypochaeris radiruto

Anapha lis mar garitttceuCarex mertensiiEpilob iu m angust it'bl iuntHypochaeris radicata

Anaphalis marga.ritaceaCarer mertensiiEp i b b iunt an g us t iJb I iu mHypothaeris radicata

-0.24+"0 .1 I * '

- 0 .061 8 .0. I 2*.

- 0.062*'- 0.050*.

0.088+.- 0 .1 5* .

0.086*,- 0 . 1 2 * "- 0.076*.- 0 . 1 6 * .

- 0.052+'0 .01 0* "

- 0 . 0 1 9 * .- 0.063*"

-0.0728"0.077+"

- 0.071 *"- 0 .1 3*u- 0 .038* '- 0 .061* '

0.098*,- 0.048*"

0 .91 * .- 0 . 1 4 * .- 0.045*"- 0 . 1 0 * "

- 0.029*,,0 .076*b- 0.039*'- 0.062*"

0 .550 . 5 10.720.88

0.480.660.680.079

0.910.670.280 . 3 5

0 . l 00 . 0 1 30.280.87

0.32"- 0.088.

0.079'- 0 . 1 2 "

0.3 5"0 . 3 1 u0 . 3 1 '0.85' �

-0.42b0.37b042

- 0 .53"

0.29b0.097b0.22b0 . l g b

0.0027" 0.90- 0.49. 0.63

0.0026" 0.390.29" 0.39

0.44b 0.00280.38b 0.00040.43b 0.00030.22 0.64

0.94" 0.003- 0.45. 0.030-0 .16b 0 .0001

0.27^ 0.007

0.093* 0.00000.086" 0.00040.020. 0.00060.093. 0.0009

creased significantly more under non-mycorrhizal con-ditions with increasing density of Carex neighbors thanit did under mycorrhizal conditions. This was the onlycase in this experiment where a signiflcant difference incompetitive intensity was found between the mycor-rhizal and non-mycorrhizal treatments. In addition,competition between Carex as the target species andHypochaeris was a non-significant p - 0.08. In thatsituation, competition was more intense under mycor-rhizal conditions. Signiflcant interactions were alsofound with Carex as competitor. The interaction effectoccurred with the mycorrhizal treatment, wherebiomass decreased with two Carex competitors butthen increased with four competitors and then de-creased again with eight Carex competitors. Thus, theinteraction effects are due to the unusual biomass char-acteristics of the Hypochaeris plants with four Carercompetitors under mycorrhizal conditions.

Discussion

Experiment I

VAM colonization levels were higher at lower nutrientlevels for most species. Due to the smaller size of theroots in the tap water treatment the percent total rootexamined was much greater than in the fertilizationtreatments. Thus, the absolute quantity of VAM fungiwas probably much less. In any case, the evidencesupports the hypothesis that on per unit of root basisthe colonization density does not remain constantacross nutrient levels (Sparling and Tinker 1978).

504

Hetrick et al. (1986) found that VAM fungi aresuppressed in non-sterile soil. From this evidence theyconcluded that presumed beneflts from VAM as mea-sured in sterilized soils were overestimated. This sup-ports the hypothesis that applying benomyl to thenon-mycorrhizal treatment underestimates VAMbenefit, because the pathogens are eliminated from thenon-mycorrhizal treatment but not from the mycor-rhizal treatment (Carey et a\. 1992). In this experiment,VAM fungal propagules were added to Pumice Plainsoil in the form of non-sterile Bear Meadow soil possi-bly containing fungal pathogens, and the non-mycor-rhizal treatment had potential fungal pathogenseliminated. Therefore, the presence of pathogenic fungimay lead to an underestimate of mycorrhizal benefit.However, the roots examined contain no signs of fungiother than VAM.

As expected, fertilization generally increased plantbiomass. Two exceptions of this were: the lack of asignilicant dilference for Hypochaerus between -P andcomplete fertilizer treatments. and significantly greaterbiomass Carex plants in the - P treatment. These spe-cies appear to be adapted to low phosphorus envtron-ments (Turkington and Aarssen 1983).

Significant increases in biomass in VAM over non-VAM plants were observed in E. brachycarpum andPenstemon. Epilobiunt brachycarpum is a rapid growingfacultatively mycotrophic annual of disturbed envlron-ments. Such growth forms are not expected to respondto mycorrhizal colonization (Allen et al. 1992, Boerner1992). Pensteruon responds positively to mycorrhizalcolonization as would be expected from a woody peren-nial subalpine species.

O I K O S 8 l : l ( l 9 9 l J )

EI

\ Mycorrhizal'... Nonmycorrhizal

o **-r_ d

trtrB

FE

trtr

tr

A. B' o.o

0.0

CD

3 -o.4(5E3 -ot

(ud. -1.2d)ct),6 -r.oE )oJ -2.0

- 0.0a6(!

6 - u '

ifr-c -O.4(!

(!

6 -0.66)(5

F -0.8E )o- - t .o

2 3 4 5 6

Number of Neighbors

B o

^ 0

t r t r

-'e-- Mycorrhizal

'^... Nonmycorrhizal

6 . .

n

tr

a

tr

tr

: - - >

r . . oE '

0 1 2 3 4 5 6 7 8

Number of Neighbors

The absence of a signiflcant positive biomass responseto the mycorrhizal treatment for most species is consls-tent with the facultatively mycotrophic nature of thesespecies. It is possible that nutrient levels were not highenough for mycorrhizal mutualism to benefit the host. Atvery low nutrient levels. the VAM symbiosis can beparasitic on mycotrophic plants (Koide and Elliott1989). However, most species showed non-significantincreased biomass with VAM. The exceptions,Hypocltaeris and Penstemon, occurred in tap water wherebiomass was less under mycorrhizal conditions thanunder non-mycorrhizal conditions. The significant inter-

O I K O S 8 l : 3 ( I 9 9 8 )

E

A

2 3 4 5 6

Number of Neighbors

B -o-

Mycorrhizal

fr ".. Nonmycorrhizal

E

tr

0 1 2 3 4 5 6 7 8

Number of Neighbors

action elfects seen in these two species imply a possibleparasitic effect by mycorrhizae at 1ow nutrient levels.

The trend observed for most of the species was for themaximum benefit from VAM to occur in the - Ptreatment. This is in accordance with many mycorrhizalmodels, i.e., the mycorrhizal effect is greatest under lowphosphorus condit ions (e.g., Smith et al. 1986, Mullenand Schmidt 1993). Phosphorus is the principal benef,tplants receive from the mycorrhizal mutualism, thereforeincreased biomass in low phosphorus environments ap-pears to be due to the fungi supplying the nutrient to theolant.

-2.4

C' o.n

o.2

D' o.o

0.0q)

P -0.4c

b

-o

6 - 1 t(u

F

-3 -r.e

@ n n(!E. 9 ^ .rn -"..

6

d -0.4

o

,(! -0.6

o- -0.8

Fig. 2. The relationship between log target plant biomass and number of neighbors. Open squares and solid lines indicate theinoculated with mycorrhizae (+myc) treatments. Closed triangles and dashed lines indicate the not inoculated with mycorrhizae(-myc) treatments. Equations of the lines are in braces. A. Anaphalis margarilaceu in competition with Anaphalis margaritacea.*myc r r : 0 . 61 , P :0 .0000 { r : 0 . 032 + 0 .24X1 ; -myc r2 :0 .55 , p :0 .0002 { y : 0 . 0021 + 0 .0 ' 7 t x } . B . Anapha t i . smarga r i t acea i n compe t i t i on w i t h Ca re , r me r tens i i . *myc 12 :0 .53 , P :0 .0003 { y -0 .088+ 0 .11X} ; myc 12 :0 .12 ,P:0.14 t \Y: -0.49+ 0.077X|. C. Anaphal is margar i tacea in compet i t ion wi th Epi lobium angust iJbl ium. *myc 12-0.28,P : 0 . 0 1 6 1 Y : 0 . 0 7 9 + 0 . 0 6 1 x ) ; - m y c 1 2 : 0 . 5 1 , P : 0 . 0 0 0 4 l f : 0 . 0 0 2 6 + 0 . 0 7 1 X ) . D . A n a p h a l i s m a r g a r i t a c e a i n c o m p e -t i t i on w i t h Hypoch t t e r i s r ad i ca ta . *myc 12 :0 .52 , P -0 .0003 l y : 0 . 12+ 0 . l 2X l ; -myc 12 :0 .51 , P :0 .0004 { y : -0.29 + 0.13x] .

505

tr

T' ' ' . . t . . . .

-\ Mycorrhizal

tr ^.. Nonmycorrhizalo

E . E ^

r

tr

o

A. B' o.u

u.oct)ooE 0.4E

.9d]

6

Y' v.v

oF

0.6

g 0.4qaF 0.2

b o.oc

d -u' '

9 , - o o(!

-o -0.6o

-0.8

-1 .0

- 0.2oo6

b

G

o - r ' v

o6t- -1.t(')-

- 1 . 8

0.6

cna

G

6 " 'iEC U . U(u

(L

a - v z

oo

-u.o

2 3 4 5 6

Number of Neighbors

No negative effects by VAM propagules on Care.rbiomass was observed. In other studies negative im-pacts of VAM on non-mycotrophic species have beenfound (Allen et al. 1989). Propagule densities may betoo low in Bear Meadow soil or VAM fungus speciesfrom Bear Meadows are not as aggressive as those lnwhich a negative effect by VAM on non-mycotrophicspecies was observed.

At the conclusion of both experiments plants weresmall due to nutrient poor conditions. In comparing the

P treatment in the two experiments (that is, plantswith no competitors in the competition experiment),plants were greater in biomass in the nutrient addition

506

2 3 4 5 6

Number of Neighbors

Dnt

-

o

-\ Mycorrhizal^-. Nonmycorrhizal

t r r l

f . r . .6

tro

' ' ' . . 1 . . . . . . . .

o

^ t r

tr

trtr

2 3 4 5 6

Number of Neighbors

experiment than in the competition experiment. Whythis occurred is unknown since the greater length of thenutrient addition experiment was insufficient to providefor such a difference.

ln a field experiment conducted on the Pumice Plainusing these same species, biomass trends between my-corrhizal and non-mycorrhizal treatments were towardsgreater biomass plants in the non-mycorrhtzal treat-ment, the opposite of this greenhouse experiment (Titus

and del Moral 1998). A negative or parasit ic responseto mycorrhizal colonization in the field and not in thegreenhouse by facultatively mycotrophic species may bedue to several environmental factors (e.g., Hattingh et

2 3 4 5 6

Number of Neighbors

c. 0., D . r o

0.6

-0.8

-r- Mycorrhizal

i

r" NonmYcorrhizal

. F tr

o

{E

tr

o

oo

Fig. 3. The relationship between log target plant biomass and number of neighbors. Open squares and solid lines indicate theinoculated with mycorrhizae (+myc) treatments. Closed triangles and dashed lines indicate the not inoculated with mycorrhizae(^ myc) treatments. Equations of the lines are in braces. A. Carex mertensii in competition with Anuphalis margaritacea. +mycr ' : 0 . 1 7 , P : 0 . 0 7 0 { y : 0 . 3 5 + 0 . 0 6 2 X } ; - m y c 1 2 : 0 . 5 3 , P : 0 . 0 0 0 3 { Y : 0 . 4 4 + 0 . 0 3 8 X } . B . C a r e r m e r l e n s i i i n c o m p e t i -t i on w i t h Ca rex n te r t ens i i . +myc 12 :0 .25 . P :0 .027 1y :0 .31+ -0 .050X) ; -myc r2 :0 .56 . P :0 .0001 . { f : 0 . 38+

0.061X]. C. Carex mertensi i in compet i t ion wi lh Epi lohium angust iJ i t l iun. lmyc rr -0.48, P:0.0007 1f :0.31+ -0.088X1;-myc r2 0.84, P:0.0000 ly:0.43+ -0.098X1. D. Carer nter tensi i in compet i t ion wirh Hypot:haer is rad. icata. +myc1 2 : 0 . 3 4 , P : 0 . 0 0 7 1 y : 0 . 0 8 5 + 0 . 1 5 X j , - m y c i 2 : 0 . 1 5 , P : 0 . 0 9 3 l \ y : 0 . 2 2 + 0 . 0 4 8 X 1 .

-r- Mycorrhizal

o

F

Btr

Itr

tr

E

\ ' . 1 .

E

tr

o

' t * o t * ' ' t [ ' oo * '

-n- Mycorrhizal

''^... Nonmycorrhizal

tr

B

A. 0.,

0.0

B 'o .o

0.0

g -0.4$

o - _ib -u.6

c(E- - 4 )

q)

,d -r.e

ooF -0.4e

.9(Dt c -u.o

Eog -1.2

o,-9 -r.o

2 3 4 5 6

Number of Neighbors

2 3 4 5 6

Number of Neighbors

c' o.o

0.2

-E- Mycorrhizal''^....

Nonmycorrhizaln ^

no ^' ' ' ' ; . . . . .o - . . . . .

l

o

tr

otr

Bo

-B- Mycorrhizal''r...

Nonmycorrhizal

t

6' . . - . . E - . .

tr

D' o.o

0.0

- -0.4ao(trE -o.aifrc - t . z

.g

6 -1.6

6F _2.0

J -2.4

g 0.0ooI -o.2tr

ii -0.4

d -u.o

oP -0.8oro r - 1 0o

- 1 . 4

Fig. 4. The relationship between log target plant biomass and number of neighbors. Open squares and solid lines indicate theinoculated with mycorrhizae (+myc) treatments. Closed triangles and dashed lines indicate the not inoculated with mycorrhizae( myc) treatments. Equations of the lines are in braces. A. Epilobium angusti/blium in competition with Anaphalis margaritacea.+myc r ' : 0 . 33 , P :0 .0083 { f : 0 . 42+ -0 .086X} ; +myc r2 : ( ) . 3 j , p : 0 .0043 \ y : - 0 . 94+ -0 .91X} . B . Ep i k t h i umangust iJbl ium in compet i t ion wi th Carer meftensi i . +myc 12:0.35, P-0.0061 \Y- -0.31 + -0.12X1; -myc 12:0.46,P:0.001 {f : -0.45 + 0.14X1. C. Epilobium angustilitlium in competition with Epilohiun't angustifblium. *myc 12:0.36,P:0.0054 t ,v- -0.42+ -0.076X1; myc 12 -- �0.32, P:0.010 1y: 0. 16+ 0.045x1. D. Epi lobium ansusr i /bt ium incompe t i t i on w i t h Hypochae r i s r ad i ca ta . *myc 12 -0 .34 , P :0 .0067 { r : - 0 .53+ -0 . l 6X } ; myc 12 :0 .45 , P :0 .0012tY - -0 .27 + 0 .10x1 .

2 3 4 5 6

Number of Neighbors

al. 1973, Allen and Allen 1986, Fitter 1986, Smith et al.1986, Anderson and Liberta 1989).

Experiment II

The presence or absence of mycorrhizae can alter thecompetitive outcome between plants and influence com-petitive hierarchies (Grime et al. 1987, Hetrick et al.1989, Hartnett et al. 1993). Unlike other studies onmycorrhizal-mediated competition, which involve a fac-ultative mycotrophic species versus an obligately my-

O I K O S 8 l : 3 ( 1 9 9 8 )

2 3 4 5 6

Number of Neighbors

cotrophic species (Fit ter 1977, Hetr ick et al. 1989,Hartnett et al. 1993) or between obligately mycotrophicspecies (Allen and Allen 1990), this study utilized threefacultatively mycotrophic species and one non-my-cotrophic species. The facultative nature is evidenced bythe lack of a signiflcant biomass response to the mycor-rhizal condition when grown alone or with conspecihcs,and by the absence of significant differences in compet-itive intensity between mycorrhizal and non-mycor-rhizal treatments. However, species vary in their degreeof facultativeness. Some species may be slightly moredependent or better able to take advantage of the VAM

\ Mycorrhizal^.. Nonmycorrhizal

tr

tr

n

507

A.0.5

0.4 D t rtr

-\ Mycorrhizal

'-^... Nonmycorrhizal

dtr

d

2 3 4 5 6

Number of Neighbors

B . ̂ ^u.o

0.4

o

3 0 26c. 9 ^ "mE(uo -u.z6o,6 -0.+

o- -0.6

CD- 0.3o@

b " 'inE 0.1-gr!o v v

(5l- -0.,1

o

3 0.2GE

m v u

od -0.2

0)CD

.(u -0.4-o)o- -0.6

I o.26

tr

dl

d -0.2

oED

.d -0.+

o- -0.6

-0.32 3 4 5 6

Number of Neighbors

-u- Mycorrhizal

tr r.. Nonmycorrhizal

Etr

6 - - - : "t . . - > - t r

Etr

2 3 4 5 6

Number of Neighbors

illustrates the difference in competition between thespecies at opposite ends of the hierarchy. VAM, there-fore, can have a significant effect on competition betweenfacultative and non-mycotrophic species at low nutrientlevels. VAM may be one of many interacting factorsdetermining competitive dominance and species changeover successional time.

Target species responded differently to VAM colonrza-tion under varying competitive scenarios. Anaphalis hadthe lowest colonization when in competition with thenon-mycotrophic Carex and highest with Hypochaeris.This supports the idea of greater colonization by VAM

D.C. o.o

0.4

0.6

-0.8

Fig. 5. The relationship between log target plant biomass and number of neighbors. Open squares and solid lines indicate theinoculated with mycorrhizae (+myc) treatments. Closed triangles and dashed lines indicate the not inoculated with mycorrhizae(-myc) treatments. Equations of the lines are in braces. A. Hypochaeris radir:atu in competition wrth Anaphalis margaritacea.+myc r ' : 0 . 60 , P :0 .0001 |Y :0 .29 + 0 .052x | ; myc 12 : 0 .45 , p :0 .0013 { v : 0 .093 + -0 .029x } . B . Hypo r :hae r i sracl icata in compet i t ion wi th Care, t mertensi i . *myc 12:0.0099, P:0.68 1f :0.097+ -0.010I) ; -myc 12:0.73. P:0.0000{y:0.086+ -0.076X}. C. H,vpochaer is rodicata in compet i t ion wi lh Epi tohium angust i /b l ium. +myc r2:0.26, P:0.022{Y:0.22 + -0.019X}: -my-c 12:0.23, P:0.033 [Y:0.020 + -0.039X]. D. Hypot:haer is radi t :ata in compet i t ion wi thH y p o c l n e r i s r a d i t ' a t a . f m y c r r : 0 . 5 8 , P - 0 . 0 0 0 1 { y - 0 . 1 8 + 0 . 0 6 3 x } ; - m y c 1 2 : 0 . 6 8 , p : 0 . 0 0 0 0 { r : 0 . 0 9 3 + _ � 0 . 0 6 2 x 1 .

2 3 4 5 6

Number of Neighbors

symbiosis than others. Thus, a hierarchy of increasingmycorrhizal dependence (or decrease in parasitic rela-tionship) is seen here. Care.r was the least mycotrophicspecies, as evidenced by greater biomass and greatercompetitiveness under non-mycorrhizal conditions. Epl-lobium angustifolium is facultatively mycotrophic andhad greater biomass under non-mycorrhizal conditions.Anaphalis had greater biomass under mycorrhizal condi-tions than under non-mycorrhizal conditions. 11]?o-chaeris had greater biomass and was more competitiveunder mycorrhizal conditions. The significant effect oncompetitive intensity between Hypochaeris and Carex

508

t r -D U

E

-ur Mycorrhizal

'''L... Nonmycorrhizal

or =\_

o' ' . . F

t ' . .tr

Etr

6

t r t r

tI

O I K O S 8 l : - 1 ( l q q g )

fungi when more mycotrophic hosts are available(Hartnett et ai. 1993). The remaining species were inf lu-enced by density, i.e., colonization was greater withoutcompetitors. Competition may reduce VAM colonrza-tion due to reduced vigor of the host plant and reducedquanti ty of photosynthate to translocate (Koide 1991a,Hartnett et al. 1993). In addition, the interaction effectsillustrate that the change in biomass across neighbordensities differs between the mycorrhizal and non-myc-orrhizal treatments. Plant density is an important factorthat influences the degree of benefit derived from myc-orrhizae by the host plant (Hetrick et al. 1989, Koide1991a, b, Carey et al. 1992). For example, Hartnett etal. (1993) found that mycorrhizae were beneficial to amycotrophic species at low densities, but increasedcompetitive effects of high neighbor densities overrodethe mycorrhizal effect. As succession proceeds, changesin plant densities and neighbor identity will influencethe effects of VAM on the host plant.

Conclusion

In general, at very low nutrient levels the role of VAMis negligible. As nutrients increase, a positive effect olVAM is observed and the difference in biomass be-tween mycorrhizal and non-mycorrhizal plants in-creases. These results imply that as soil ameliorationcontinues on the Pumice Plain. VAM will assume amore important role in plant growth for some faculta-tively mycotrophic species. However, as VAM fungalpropagules enter the environment, pathogenic fungi arebound to increase as well making the positive effect ofVAM on piant growth difficult to assess.

When Hypochaeris competes with Care-r, the pres-ence of mycorrhizae changes competitive intensity. Inthe field, however, it is unlikely that competitive domi-nance is dependent solely upon mycorrhizal associa-tions. Mycorrhizae probably interact in important wayswith other factors. As primary succession proceeds therole of VAM in the mediation of competitive outcomesis predicted to increase.

The mycorrhizal mutualism is an intensive invest-ment for a plant. At this early stage in primary succes-sion on Mount St. Helens with nutrients levels still low.there are no strongly evident VAM effects that can bederived from this greenhouse experiment. VAM effectsare weak and contingent on at least neighbor identityand density and soil nutrient availability. As yet VAMare unl ikely to alter species competit ive outcomes orsurvival of individuals in the lield.

Atknovledgentents Thanks to D. Ewing. E. Bassett and J.Milne for taking oare of the plants in the Greenhouse and forgood advice. Greenhouse labor was contributed by P. Titus,M. Tu and J. Albert. Extensive lab work was contributed bv J.VanDeMark and S. Gamiet. Statistical advice was provided byS. Zrtzer and J. Perez-Comas. S. Tsuyuzaki. W. Gold and J.

O I K O S 8 1 : 3 ( 1 9 9 8 )

Ammirati made useful comments on experimental design.Thanks to P. Titus for editing the manuscript and her gener-ous encouragement and support. NSF Grants BSR-89-06544and DEB-9406987 to R. del Moral helped support this re-search.

ReferencesAl len, E. B. and Al len, M. F. 1986. Water re lat ions of xer ic

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