The role of ecological significance of vesicular-arbuscular mycorrhizas in temperate ecosystems

137

Agrlculture, Ecosystems and EnVironment, 29 (lssg) Elaevler Science Publlshers B.V., Amsterdam Prlnted in Czechoslovakla

137-151

THE ROLE AND ECOLOGICAL SIGNIFICANCE OF VESICULAR-ARBUSCULAR HYCORRHIZAS IN A.H.

TEHPERATE ECOSY~TEH$

FITTER

Department o f B~ology,

University

o f York

York Y01 5DD ABSTRACT

Although vesicular-arbuscular mycorrhlzas (VAH) are abundant and widespread in m~ny v6getation types, the levels of Infection vary widely between species and sites. This Is Inconsistent with the usual explanation of their role and a number of possible alternative hypotheses are exarnlned.

Results of experimental manipulations suggest

that for much of the time, plants receive little benefit from VAH.

It is suggested

that most plants only derive benefits at times when their demand for P is much qreater than the capacity of their root systems to supply it.

Flowering and seedling

establishment may be examples of such times for many 101ants.

INTRODUCTION

Veslcular-arbuscular mycorrhizas (VAH) are both widespread and common In all climatic zones.

In the British flora, of 1092 species documented by Harley and Harley (1987),

64~ are listed as VAH-forming, as compared with 4~ forming ectomycorrhlzas and 4~ forming either type (Table 1).

As many as 21~ have not been recorded as mycorvhizal,

though many could probably be shown by further sampling to be occasionally so. of the VAH-formlng species of plant are recorded as either VAP, or non mycorrhiz,~, emphasislng the fscultatlve nature of the association.

Half

138

Althcugh many plants form VAM, therefore, the frequency and intensity of incecti~n is highly variable, and this phenomenon requires exD:anation.

The- conventional vie~ ot

mycorrhizai function is that the fungus supplies the plant Drlncil~ally with phosphorus in exchange for carbohydrate which, in the case of VAH, the fur.pus cannot otherwise obtain.

In addition, there Is abundant but rarely unequivocal evidence that

mycorrhlzal plants may receive benefits in water relations, in the uptake of mlcronutrlents (especially the poorly mobile Zn and Cu), or in protection from toxic Ions, pathogens or even extremes of physical factors.

The variation in infection

observed in VAH plant species may, therefore, be a reflection of the relative benefits different species require from the fungal partner.

It follows, for example, that

Table I Percentage o f t h e 8 r i t i s h f l o r a ( f o r t h a t form d i f f e r e n t types of mycorrhiza. H a r l e y , 198/o)

VAN o n l y VAH e i t h e r VAN o r a b s e n t VAH o r ECH ECH Ericoid/Arbutoid Orchid Other None

wh'ich r e c o r d s e x i s t ) (Data from H a r l e y and

All. plants

Woody p l a n t s

04

38 32 32

4 4 2 4 1 21

26 12 17 24 19 0 O 2

VAN : V e s i c u l a r - a r b u a c u l a r m y c o r r h i z a l ECN : E c t o m y c o r r h i z a l myoorrhlzal plants should be especially abundant on particularly resource-de::clent or toxic soils.

Heathlands tend to have acid, nutrient-poor soils and Read (1963) has

suggested that the ericold my~.~,-rhiza is particularly adapted to providing benehts to host plants in such soils.

Equally, ectomyoorrhlz~l (ECH) trees are often found on

more nutrient-deficient soils than VAH trees, and the very low root biomass

of some

ectomycorrhizal tree~ (Fogel, 1985) suggests that many root functions are subsumed by their fungal partner.

Some patterns in mycorrhizal Inf~ctlon are, therefore, wel: explained. low levels of infection in wetlands may'slmilarly be related to

The generally

anoxia or to the greater

mobillty of phosphate Ions in wet, peaty soils, which would reduce the need far root

1 39

(a) a l l geneea

(b) n a t i v e speciaa

50.

40-

,~ ,~

30 -

20

100

"~ ECM

ECM/ VAM

VAM

Ericold

ECM

ECM/ VAM

VAM

Eri©oid

Date £z.ole Harley & Harley (1987)

Fig.1 Frequency of various mycorrhizal types in woody plants of the B r i t i s h f l o r a ( data f~'om Harley ~and Harley, 1987). ECH - ectomycorrhizal; VAN - vasicular-arbuscular mycorrhizal. systems to ~'ely on mycorrhizally assisted transport. In two major types of tempsrate ecosystem, however, namely grasslands and deciduous woodlands, the patterns are much less clear.

Some important woody genera are ectomycorrhlzal (Q~ercus, Fagus, Betula)

but many can be either ECM or VAH (PoDulus, Salix, Ater), and a large number appeal" to be almost exclusively VAH-forming (Aesculus, f/ex, Ulmus, Fraxinus).

In the British

flora, over a third of woody plants appear to be normally YAH and un~ler a quarter exclusively ECM (Fig.l).

In grasslands, virtually all species (typically probably around

90~) show some VAH infection, but the intensity of the infection ~aries 9 ~ a t l y .

In

the survey by Read et= el. (197$), two thirds of sl0ecies in grasslands ~ampled hacl >50~ of their root length VAH it=letted, but a 3igniflcan¢ proloortion ha¢l little or no infectior, (Fig. 2).

140

70° woodlands

60. gr as s l a n d s

50.

40. t~t

30-

20.

J

7

j

i

10.

0 0-10

11-30

31-50

51-100

S root length infected

Fig.

2.

Frequency of frassland UK ( d a t a

infection

denctty

and woodland h a b i t a t s from Read e t a L . ,

tn species

from

near Shefftels,

1976).

141 HYPOTHESES

In any one plant community, and between any group of similar communities, a wide range in the level of infection can be found in the component species.

This produces

a paradox: if Infection is beneficial to the host plant, there should be selection to make the association more complete and effective; and It should disappear.

If not, there should be selection against it

I t appears tl~at the ecluilibrium point for the association

varies from place to place, time to time and species to species. explanation of VAM function is not tenable.

This wide range in

There are a number of possDble

explanations which might help in understanding the role and significance of the VAM as6ocl=tlor, ~Jnder field conditions.

I examine some of these below;

the list Is not •

exhaustive, nor are they mutually exclusive.

1. Di_.ff_e£enc.es_.bet~e..enP!@nt spec!es lD Jnf¢~tion !e~e!s are observed be~use the~: di_ffeC.Jn_theirneedfort!~eaSs~!atiow!~dHetodiff@renceseither i n phqsphate m~..a.,.~.o.!!..=..m. ,.~r_.!,n,......r....~t_,.,~r.p..,..h_ql.~gy

This Is perhaps the normal explanation, drawing support from Baylls' (1075) hypothesis that coarse-rooted species such as Magnolia and its relatives are obllgatsly mycotrophic, while fine-rooted speclas such as the Cypereceae are non-mycotrophlc.

Although at

these two extremes the suggestion seems well supported, there is no evldenco that a good quantitative relationship exists between root morphology and Infectedness.

It is

easy to find examples of fine-rooted plants (e.g. most grasses) which are consistently and strongly mycorrhizal, while some plants with very poorly-developed root systems (e.g. bluebell, Hyac/nthoides non-scripts) may be scarcely Infected for much of the lifespan of the roots (Fitter, unpubl.).

Clearly some whole groups of plants (Cruclferae,

Caryophyllacsae) normally resist Infection, and no simple explanation for this Is known. Many of these are oolonlsts and short-lived species, so that life-history characteristics may be important, though by no means all annuals are norma:ly non-mycorrhlzal.

Most

142 importantly, however, this hypothesis cannot eJtplain the vlr~ation in Tr,fection tl~at m a y

be found in a single species between or even within sites.

2.

O!fferences between plant species in infection levels are observed because each has

a distinct seasonal pattern, b u t e a c h has a need for the association at some stage

There i$ no doubt that infection levels vary seasonally.

Read e t el. (1976) found that,

of 13 species, none had maximum infection in winter, and McGonigle (1987) and Brundrett and KencHck (1988), too, had evidence of a summer peaK.

In these studies

there was rather I~ttle synchrony between species. Gay et al, (1982), in contra$1~ found that the infection levels were lowest in summer and that all species showed the same pattern.

If times of peak infection d¢ differ between species, much ot the

evidence of differences between species in infection levels c~uld be a simple consequence of that.

More studies where infection is monitored throughout the year

and preferably over several years are urgently needed.

Differences between co-

existing species in time of maximum productivity are well-established, both above (Wells, 1973) and below-ground (Fitter, 1986a).

I t remains to be established, therefore,

whether seasonal patterns In mycorrhizal Infectlon are species characteristics determined b) Inherent growth patterns, or are controlled by environmental factors.

3,

0iff.e,re.!!qes. between p!ant.spectes in Infect!on levels are 0bser:,'ed because there, is

speclftc!t¥ in their ability to form associations with different fungal species in the field, and the fungal community varies I n space and time

Although there are several hundred described species of VAH fungi, there is astonishingly little Information on their ecology. a single collection:

Hany fungal taxa are described from

are they endemics with specialised ecological requirements, local

segregates of more widespread species, or themselves widespread but over=coked? There is evidence that fungi from various sites perform differentially in new soils: for exarnple, Lambert e t a / . (1980) grew Lotus cornicu/af:us it; six soll.~ with lnoculum derived from three of those soils, and the shoot dry mass was always greatest when

143 the native ino~.ulum was used. speciallsation by VAM fungi.

There could, therefore, be eKtsnsive eclaphic Whether they also show any host s~ecificity is less clear.

Certainly t h e r e is little evidence for such specificity in culture, but in the field it could be more easily manifested.

HcGonigle (1987) showed that Holc us I~natus was

preferentially colonised by fine endophyte (presumed to be G/omus tenue), but the d i f f i c u l t y of identifying vegetative states of other VAH fungi has ~o far precluded f u r t h e r evidence on this point.

4.

Differences between plant species in infection levels are observed because

p hoeph~te ave!lability and o t h e r soil characteristics vary at all spatial and temporal sca!eS I t is well established that plants given high Ooses of P fertlliser resist infection by VAH fungi.

I t Is reasonable to suppose, therefore, that soils rich in available P will

be colonised by plants low in mycorrhizal infection and that for an~. one species growing on a range of sites t h e r e will be a negative relationship between infection and soil P.

Although some workers have found such a relation (e.g. Boerner, 1986), it Is

equally often found that soil P and infection are unrelated.

Dlckrnan et el, (1984)

found no relationship between infection in the roots of the prairie grass Schizachyrlurn scopariurn and the soil P level, though their data does suggest a relationship with soil organic matter.

It could be argued that soll P is an i;=dlrect causal factor, and that

plant P concentration is the more appropriate measure.

Ernst e t a / . (1984), however,

could find no relationship between Infection and leaf P concentration in Ca/amagrostis epigejos on sand-dunes.

While, therefore, it Is possible that variations in soil P availability may account for differences in infection Oe~ween plants, it is often hard to demonstrate any relationship between infection and P status of soil or plant.

In these circumstances it is tempting

to look f o r a f u r t h e r variable (soil moisture, copper or zinc concentration, pit, temperature and so on} which will explain the observed patterns, but such post hec reasoning ~s unconvincing,

i t is true that VAH have been reported a; having a

variety of effects on plants, that plants d i f f e r in t h e i r reaulrements for various

144 resources and that the availability of these resources varies in a complex way.

It

could be argued, therefore, that patterns of infection in nature will be equally complex, but it is perhaps premature to adopt such a counsel of despair.

A more hopeful

approach is to manipulate VAM associations under field conditions in experiments dsslgned to test for differences In performance between giants varying in mycorrhizal Infectlon.

EXPERIMENTAL MANIPULATION

The mttln reason why rather little progress has been made In manipulating VAM populatlons In the field Is the lack of an approprlate, specific technique. There are two possible approaches: addition of new species of fungus, or removal or reduction of the existing populations.

The two could be combined.

Removal can be attempted with

any of three techniquss: fumigation of soil with sterilants (e.g. methyl bromide), Irradiation and fungicides.

Hone of these approaches produces a simple and specific

change In the fungal flora, and until a VAM-specific, phloem-mobile fungicide Is produced, this will continue to be an elusive goal.

Inoculation has been used where new plant species are Introduced at the same time, for exmltple where white clover (Trifollum repens) was plante~l into upland grassland by Rangeley st al. (1982).

In that experiment there were no consistent effects of

inoculation on yield and P concentration.

In a detailed ana;ysls of published

Inoculation experiments in which changes in both yield and infection levels were reported, HcGonlgle (1988) found no relationship at all between &n index of yield increase and index of infection increase, although nearly 80 cases were recorded (Fig. 3),

Several attempts have been made to remove VAM fungi in natural commun*ties, using both fumigation (Wallace, 1987) and the fungicide benomyl (Fitter, 1986b).

~n five

prairie grasses (Panicum Wrgatum, $chizachyrium scoparium, Dicanthelium oltg~santhes,

Bouteloua gracllis andql Pasl~alum setaceum) soil fumigation had no effect on growti~ and ""

145

index of yield

increase

(dimensionless) ZO-

0

1.5"

o 0

@ @

|

0.5'

O.

•

@ @ @ @ D

• •

• @

@ • @O • • @ B@O @ @ • U@ • 40 @• @ 00 @ 0@ @ @ • @ • @ @

• @

@

•

• • •

@

O@

•

@ @ • ®

t "0.5"

@ 0

0

-111"

@

@

index of frac¢ional

infection

increase

(~dlans)

Fig. 3.

R e l a t i o n s h i p between i n d | c e s o f y i e l d i n c r e a s e and f r a c t i o -

nal infection

i n c r e a s e in 78 pub].ished f i e l d

VAM (from McGonigle, kind permission).

1988; reprinted from

Yield

~nocu]ation trials

with

Functional Ecology with

increase is expressed as the difference

between inoculeted and unlnoculated plants divided by the average of the two. The index of fractlonal infection increase

is the differen-

ce in percent root length infected between inoculated and unlnoculated plants, where b~th are subjected to an arc-sine square r ooh transformation.

146 there

was no r e l a t i o n s h i p

(Wallace, vels

in

1987).

several

centrations nally

between growth

Similarly, plants

actually

Fitter

i n two a l p i n e

increased

and VAM i n f e c t i o n

(1986b)

grasslands,

in those

levels

reduced i n f e c t i o n

plants

but

that

le-

Leaf P conwere o r i g i -

most mycorrhizal, only falling in plants originally scar-

cely infected (e.g. Carex concinnoides). Benomyl does not appear to alter availabel soil P concentrations may

tion and i r r a d i a t i o n , SOil

(Fitter, 1988) and so

be a more suitable agent for reducing infection than fumigaboth of which b r i n g

about

large

changes i n

chemistry.

These e x p e r i m e n t s has l i t t l e es. T h i s

seem to

or no e f f e c t paradoxical

show t h a t

on p l a n t

conclusion

altering

V&M i n f e c t i o n

performance conflicts

in n a t u r a l

with

levels

communiti-

the known behavioun

fo VAM in more controlled contitlons and in agricultural environments, and with the ubiquity of the assnciation. It is improbable that a symbi(

~s found in the roots of most species within a com-

munity can be having no effects. %t is of course possible that the effects are insensitive to the actual intensity of infection, 20~ of root Length infected being as beneficial to the host as 80%, and this would explain the aqulvocal results of experimental manipu lations. Howerer, since the association has a measurable cost for the plant

(Koch and Johnson, 1984~ Snellgrove et al., 1982), that

situation should have led to selection for lower infection generally. There ere good reasons why one might

expect

VAM to f u n c t i o n

efficiently in the field than in pot culture

levels less

(Fitter, 1985), but

It Is unlikely that they never offer benefits to their hosts. Th? most generally accepted explanation for VAN function is the assisted transport of P, but for this to be of benefit to a plant, it would be necessary for its root system to be unable to supply its need for P. Data on g uptake rates by plants in natural communities are scarce, but McGonlgle and Fitter (1988) planted Trifolium repens plants varying in VAN infection back ir~to a grassland site from which both plants and fungi had originated.

Although in

an early growth phase in pots, there was a good relationship between P inflow (uptake per unit root length) and infection, once in the

field

ficantly, a Level

this

relationship

the P i n f l o w at

rates

which m y c o r r h i z a ! l y

disappeared in the f i e l d assisted

(Fig.

4).

were v e r y P

transport

Most s i g n i Lows below

147

Phosphorus inflows (fmol cm" s"=) 5O 40 30. tj o

20'

° a 0

10'

IB

im A

0

&

•

|

0

i

|

!

0'1 012 0'3 0.4 0'5 016 Fractional infection (harvest interval mean)

0'7

F i g u r e 4 Relationship between P inNow during harvest

intervals and mean fractional infection ~ r plants either side of those intervals. Symbols refer to intervals ~ r days 0-27 ( ~ ) , 27-38 ( 0 ) , 3S--52 ( ~ ) , 52-66 ( A ) and 66-80

(D). would need to be i n v o k e d , nential

gr~)wth.

without

mycorrhizal

Since the p l a n t s

re was no e f f e c t flows (I.

of

plants

Sanders,

that

for

of

peps.

much of

infection a range of

may n o r m a l l y found

v e r y high

is give

2hat

assistance

to e x p l a i n

is

of

surprising

under n a t u r a l

are w e l l

little

the-

data)

conditions confirms

below v a l u e s at

Low, then m y c o r r h i z a l benefit.

At t i m e s of

may be of g r e a t

strawberries rate

had a b r i e f

v a l u e because t h e plant*s

while during

root

period developed. vegeta-

(Table 2 ) .

when being

system i s

demand f o r

Dunne

mycorrhizal

would have been r e q u i r e d be a p e r i o d

in-

high

value.

as the f r u i t s

observed i n f l o w s ,

the

that

Recent data on P i n -

unpublished

phase may t h e r e f o r e

satisfying

expo-

an adequate P supply

was n e c e s s a r y t o p o s t u l a t e

growth no a s s i s t a n c e

p a b l e of

maintained

would need to be i n v o k e d .

normally

cultivated

phase i t

mycorrhizaL

i s not

species

P demand a n d . u p t a k e

The r e p r o d u c t i v e

it

on g r o w t h .

the a s s o c i a t i o n

During t h i s tive

received

comm.; F i t t e r f i assistance

demand, however, (1987)

the p l a n t s

the t i m e P i n f l o w s

P demand by p l a n t s

fection

of

assistance,

of

which m y c o r r h i z a l If

although

inca-

P. S i m i l a r l y ,

148

young seedlings may' have inadequate root systems and this could explain the pronounced effect of VAH on seed;ing survival in the microcosm eKpe;'iment ot Grime et aL (1987). T a b l e 2. Changes i n w h o l e p l a n t and r e p r o d u c t i v e o r g a n b l o m s s s and P c o n t e n t , and e s t i m a t e d P ; n f l o w s , for cultivatea s~rawberries ( F r a g a r i a x anan'assa cv H a p ~ l ) i n f i e l d culture. Inflows a r e c a l c u l a t e d a s s u m i n g o n l y w h i t e r o o t s o r a11 r o o t s a r e a c t i v e (Dunne, 1987). time perJoU/~ays

Increaae in plant biomase/g Increase

in flower biomass/g

P inflow (white fmol cm-~s -~ P inflow fmol

56-84

84-112

24,4

188.3

601.5

in plant

P con~ent/mg

Increase and f r u i t

28.S6

(all

roots)/

?

64

1,9

35.9

228 444.3

82

770

2747

13

122

435

roots)/

o m - l s -1

The suggestion that for much of a plant's existence, the mycorrhizal fungu6 in its roots Is e, mild.parasite is not new (Rayner, 1928], but l 10ropose here specifically that VAM are beneficial to plants only at particular times in the life-cycle, when P demand is greater than the capacity of the root system. any other putative benefit.

A similar argument could be made for

Plants vary in the time in which they take Lip P

(Veresoglou and Fitter, 1984], in the extent to which they store P (Nassevy and Harley, 1971) and In their allocation of P to reproductive activ=ties (Abrahamson and Caswell 1982; Fitter and Setters, 1988), and therefore their need for VAH infection will vary to the same extent, both between species and in time.

Zf analyses of VAH activity in

plant communities are made at a single 10pint in time, a confusing picture will inevil~bly emerge,

What Is required are studies of the phosphate metabolism and mycorrh=zal

status of plant species over extensive time periods.

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