FUNGI IN ECOSYSTEM PROCESSES - CHAPTER 5 pptx

Wehave seen, however, that different species of arbuscular mycorrhizae may havecontrasting effects on the performance of the host plant species, thus, as in theectomycorrhizal scenario a

InChap 3we showed how primary production was positively influenced

by mycorrhizal fungi that assisted plants in obtaining essential nutrients andwater and by endophytes that reduced the effects of faunal grazing on theplant In addition, we saw how plant pathogenic fungi could reduce plantproduction, as measured by biomass, and also by the fecundity of the plant, asmeasured by seed production and offspring survival If the growth promotion

or suppression is asymmetric among plant species in a plant community (i.e.,not all species in the community respond in the same way or in the samedirection to the influence of a fungus), there will be selective pressures exerted

on members of the community Those species exhibiting enhanced growth andfecundity will increase their abundance and standing in the community,whereas those species exhibiting reduced growth and fecundity will be reduced

in their contribution to the community In a similar way we may consider thatfungal pathogens of animals could also influence both the population of theanimal and its occurrence in the community of animals of the same trophic orfunctional group Despite the extensive literature on the effects of fungalpathogens on a variety of faunal groups, however, there is little documentedevidence on the effects of fungi on animal communities Recent concerns,however, have been raised concerning the high incidence of fungal diseases of,for example, frogs, leading to a significant decline in their populations in

the tropics This is especially important, as tropical areas are being looked to

as havens of biodiversity

A variety of direct and indirect effects of fungi can both cause changes inpopulations of organisms and alter community composition The interactionsconsidered in this chapter are summarized inTable 5.1

Pedersen and Sylvia (1996) suggest that one of the major componentsdetermining the success of early colonizing plants during plant seral succession isthe availability of nutrients In this context the ability of plants to associate withmycorrhizal fungi and enhance their ability to sequester nutrients from a limitedresource is of benefit to the success of the plant species in the community Indeed,

it has been shown that the dispersal of spores of hypogeous fungi by rodents is animportant determinant of mycorrhizal inoculum for plants in the early stages ofsuccession on bare ground The distribution of mycorrhizal fungal spores byanimals is rarely random, however Small mammals defecate in middens and arelikely to deposit more spores in areas of active feeding sites than in otherlocalities This patchy distribution of mycorrhizal inoculum potential has aninfluence on the type of plant that can be successful in each microhabitat Forexample, M.F Allen (1991) suggested that the presence of mycorrhizae increasedthe diversity of plant species colonizing new areas The patchy distribution ofmycorrhizal spores, and hence inoculum potential, would allow the establishment

of both mycorrhizal and nonmycorrhizal plant species in the community It hasbeen shown that during primary colonization, mycorrhizal inoculum potentialcan vary from none to abundant in locations only centimeters apart (Allen andMacMahon, 1985) In his book, M.F Allen (1991) compares the importance ofmycorrhizae in the re-establishment of vegetation following disturbance in avariety of ecosystems From his own work he showed that vegetation colonizingMount Saint Helens consisted entirely of mycorrhizal species, both arbuscularmycorrhizal and ectomycorrhizal forms In contrast he cites the work of Schmidtand Scow and Hendrix and Smith in the Galapagos, where a mixture ofarbuscular mycorrhizal and nonmycorrhizal plants established In this case thedistribution of mycorrhizal associations was related to soil nutrient content, withnonmycorrhizal plants developing in the more fertile, lowland soils andmycorrhizal plants establishing in the poorer rocky soils From these and otherstudies, Allen and Allen (1990) hypothesized a number of patterns of mycorrhizaldependence in developing ecosystems in relation to nutrient and wateravailability The pattern for regulating plant competition is given in Fig 5.1

In a recent study of mycorrhizal colonization of plants in a primary succession onvolcanic substrates of Mt Koma, Japan, however, Titus and Tsuyuzaki (2002)found no effect of microsite on the arbuscular mycorrhizal colonization of

TABLE5.1 Ecosystem Services Provided by Fungi

Soil stability (aggregates) Saprotrophs, Arbuscular mycorrhizae

Note: Services and fungal groups discussed in this chapter are in bold face type Fungal groups in parentheses are regarded as of lesser importance in that function.

Agrsotis scabra Campanula lasiocarpa, on the other hand, showed a higher rate

of root colonization by arbuscular mycorrhizae near rock than on flat sites andthose occupied by Polygonum In all sites, willow (Salix reinii ) was heavilyectomycorrhizal These data suggest that the models proposed by Allen and Allen(1990) are not only dependent on environmental factors but are also plantspecies-dependent

Trappe and Maser (1976) showed that spores of the arbuscular mycorrhizalfungus Glomus macrocarpus and the hypogeous ectomycorrhizal fungusHymenogaster were dispersed by small mammals, such as the Oregon vole,Microtus oregoni, and the chickaree, Tamiasciurus douglasi A proportion of thespores survived passage through the gut of the animals and assisted in thecolonization of bare ground by primary colonizing plant species by providingmycorrhizal inoculm (Trappe, 1988) Similarly, Kotter and Farentinos (1984a,b)showed that a variety of ectomycorrhizal fungal spores could survive passagethrough the gut of the tassel-eared squirrel, Scurius aberti, and developmycorrhizal associations with ponderosa pine Cazares and Trappe (1994)showed that mycophagy of both hypogeous and epigeous mycorrhizal fungiresults in the deposition of viable spores in feces In part the local deposition offeces in middens by small mammals may account for the patchy distribution ofmycorrhizal spores in the environment, as seen by Allen (1991)

The appearance of spores of a variety of fungal genera in the feces of pika,voles, chipmunks, marmots, mountain goat, and mule deer on the forefront of

FIGURE 5.1 Hypothesized pattern of succession showing the importance ofmycorrhizae in regulating plant competition during seral succession Source: Data fromAllen and Allen (1990)

Lyman Glacier forms an inoculum source, allowing colonization of the newlydeveloping soils by early successional and slow-growing tree species (Abieslasiocarpa, Larix lyalii, Tsuga mertensiana, and Salix spp) Jumpponen et al.(1999) identified “safe sites” on this glacier outwash where plant colonizationwas most likely These sites consisted of concave surfaces of coarse rockyparticles, which were ideal for trapping tree seeds and protecting them fromdesiccation It is likely that these sites also formed foci for foraging smallmammals, as they were a site of abundant food in the form of seeds Thedeposition of mycorrhizal spore-laden feces in these microsites would thusfurther enhance the survival of germinating tree seedlings In these harshenvironmental conditions, Jumpponen et al (1998) showed that the dark-septatemycorrhizal fungus Phialocephalia fortinii significantly enhanced growth oflodgepole pine (Pinus contorta ), which is an early colonizer of the glacierforefront, but only in the presence of added nitrogen Total plant phosphorus,however, was significantly enhanced in the presence of the mycorrhiza with noadded nitrogen (Table 5.2) During the succession of plants in this recent glacialtill, microbial communities change from bacterial domination to fungal-dominated communities During this change, carbon-use efficiency changes from

a high rate of carbon respiration to an accumulating phase, thus indicating that

TABLE5.2 Effects of Mycorrhizal Colonization on the Growth and Nutrient Content ofLodgepole Pine (Pinus contorta ) Seedlings by the Dark-Septate Fungus Phialocephalalafortinii in the Presence and Absence of Added Organic Matter and Nitrogen to LymanGlacier Forefront Soil

Treatment

Plant dry weight(mg)

Total N(percentage dry wt.)

Total P(percentage dry wt.)

No N added

No OM, No Myco 52.9 0.69 0.074

OM, No Myco 40.3 0.63 0.076

No OM, Plus Myco 48.8 0.60 0.087

OM, Plus Myco 43.1 0.62 0.100

100 kg N ha21

No OM, No Myco 81.7 1.41 0.072

OM, No Myco 104.1 1.78 0.066

No OM, Plus Myco 129.9 1.64 0.092

OM, Plus Myco 146.2 2.11 0.128

Note: Organic matter only is significant in no N added treatment for biomass, but for P content only mycorrhiza is significant In the N added treatment, mycorrhiza is significant for biomass and P content and organic matter is significant only for N content.

Source: Data from Jumpponen et al (1998).

fungi are a stabilizing force in the developing ecosystem and facilitate net carbonfixation into biomass (Ohtonen et al., 1999).

The existence of successions of ectomycorrhizal species during primarysuccession is supported by the findings of Jumpponen et al (1999; 2002) on theLyman Glacier forefront In the different plant succesional stages they identified,they found 68 ectomycorrhizal species belonging to 25 genera, with no singleectomycorrhizal species occurring on all three successional sites The authorsalso found that ectomycorrhizal species diversity increased to a maximum wheretree canopies started to overlap This information corresponds to that of otherstudies (Dighton et al., 1986; Last et al., 1987; Visser, 1995), in which theincrease in diversity of ectomycorrhizal fungi at canopy closure may be related toboth the relative paucity of available nutrients (phosphorus) (Dighton andHarrison, 1990) and an increasing proportion of nutrients locked up in organicforms It has been speculated (Dighton and Mason, 1985) that this increaseddiversity of mycorrhizal fungi allows the greater expression of mycorrhizalfunction in order to utilize the mixed available resources of inorganic and organicnutrients Some degree of validation of this hypothesis has come from the study

of Conn and Dighton (2000), in which the diversity of ectomycorrhizae growinginto different tree litters reflects appropriate enzyme functions in relation to therelative availability of inorganic nutrients Where phosphorus is immobilizedduring early stages of leaf litter decomposition, the ectomycorrhizal community

of pine tree seedlings contained a greater proportion of acid phosphataseproducing mycorrhizal types

The succession of arbuscular mycorrhizal fungi on roots of herbaceousplant species is probably less obvious than that of ectomycorrhizal fungi Wehave seen, however, that different species of arbuscular mycorrhizae may havecontrasting effects on the performance of the host plant species, thus, as in theectomycorrhizal scenario above, we may anticipate changes in the arbuscularmycorrhizal community on plants in association with changes in availableresources in the environment Indeed, Hart et al (2001) propose two hypotheses

to explain the examples of successional changes in arbuscular mycorrhizal fungalspecies One of these hypotheses suggests that the mycorrhizal fungi are thedriving force (drivers); the second suggests that changes in mycorrhizal speciesare dependent on the plant and environmental conditions and the mycorrhizae areconsidered “passengers”(Fig 5.2)

The importance of maintaining a continuous mycelial mat of mycorrhizalfungi to encourage rapid development of mycorrhizal associations duringcolonization has been demonstrated Amaranthus and Perry (1989) showed thatwhen Douglas fir was planted into partially cleared sites in which mycorrhizalroots are maintained on the roots of the remaining trees, the survival of the newlyplanted trees was approximately 90% Where trees were planted into totallycleared areas, the newly planted tree survival after 2 years was only 50% They

FIGURE5.2 A model proposing two alternate mechanisms for changes in community structure of arbuscular mycorrhizal(AMF) communities through time The “passenger hypothesis” proposes that mycorrhizal communities are determined by theplant community, whereas in the “driver hypothesis” the mycorrhizae determine the plant species by interspecific differences incolonization and persistence potential of the fungi Source: From Hart et al (2001).

attributed the reduction in survival to the lack of a viable communalectomycorrhizal network into which the new trees could connect It is probablethat this existing mycelial network provided greater stability of the system,allowing carbon and nutrient exchange to take place between connected plants.This allows new recruits to access a larger pool of nutrients and carbon than theywould be able to on their own This synergistic activity between surviving matureplants and recruits into the ecosystem allows greater ecosystem stability andsurvival of the same plant species composition of the ecosystem followingdisturbance.

Even saprotrophic fungi can influence plant establishment Inoculation ofthe seed of the pulp wood tree Gmelina arborea with the fungus Chaetomiumbostrychodes has been shown to improve seed germination (Osonubi et al., 1990)(Fig 5.3) It is probable that enzyme production by the fungal hyphae assist inseed stratification or replacement of the scarification process

In addition to improving plant growth, the effect of mycorrhizal associations canlead to improvements in overall plant fitness This improved fitness, ifasymmetric, can be a method of providing competitive advantage to those plantspecies or individuals that respond the most to the effects of mycorrhizalcolonization These highly responsive plants will therefore become moredominant in the community Examples of improved fitness are scattered in theliterature For example, Sanders et al (1995) showed that plants with arbuscularmycorrhizae had improved phosphate nutrition In addition to the enhancement

of vegetative growth, which was supported by greater nutrient acquisition, therewas a significant increase in flower bud and seed production in mycorrhizal

FIGURE 5.3 Effect of seed inoculation with Chaetomium bostrychodes on thegermination of Gmelina arborea seeds Source: Data from Osonubi et al (1990)

plants These increases are related to overall plant growth and lead to greaterperformance of the plant as a whole rather that just becoming a larger plant Theeffects of mycorrhizae on the increase in reproductive potential of plants has beennoted by Koide et al (1988), Stanley et al (1993), Lewis and Koide (1990), Brylaand Koide (1990), and Koide and Lu (1992), the increased reproductive potentialleading to improvement in offspring vigor by increased seedling germination,leaf area, root:shoot ratio, and root enzyme production Heppell et al (1998)showed that offspring of arbuscular mycorrhizal-infected Abutilon theophrastiwere significantly larger than offspring of nonmycorrhizal parents, and underhigh-density conditions, improved even more because of the effects of early self-thinning in the mycorrhizal condition This advantage was also transferred to thenext generation in terms of total seed production (Table 5.3) The influence ofmycorrhizae can, however, differ significantly among plant species, andaccording to Janos (1980) can be a significant factor in determining plant speciescomposition in the tropics.

The effect of mycorrhizae on the composition of the plant community theycolonize was reviewed by Francis and Read (1994) Many of the examples theycited were of two species interactions They came to the conclusion that the effect

of arbuscular mycorrhizae is most beneficial to K-selected plant species and has

an adverse effect on ruderals Francis and Read (1995) thus proposed acontinuum of responses from mutualism, with positive mycorrhizal effects toantagonistic, negative effects of mycorrhizae, depending on the host plant species(Table 5.4)

Benefits of mycorrhizal colonization of the bluebell (Hyacinthoides scripta ) in natural ecosystems have been shown to enhance phosphorousnutrition of the host plant at specific times of the year Greatest phosphate uptake

non-TABLE5.3 Plant Fitness Parameters of Abutilon theophrasti Offspring of Mycorrhizal

or Nonmycorrhizal ParentsOffspring age

(days) Fitness parameter Mycorrhizal parent Nonmycorhizal parent

94 Survivors per box 59.1 26.6

Seeds per survivor 17.9 10.6

Source: Data from Heppell et al (1998).

occurred when there was reallocation of nutrients from the resting bulb to rapidlygrowing above-ground plant parts (Merryweather and Fitter, 1995a) The degree

of dependency of bluebell plants on their mycorrhizae appears to increasethrough age Young bulbs are phosphate rich and inhabit upper soil layers;however, because of their susceptibility to frost, summer desiccation, andherbivory, the bulbs at greater depth have higher rates of survival The trade-offfor this enhanced survival at depth is a reduction in the availability of soilphosphate at deeper depths; thus the plants supported by deeper bulbs becomemore dependent upon their mycorrhizal fungi (Merryweather and Fitter, 1995b)

In contrast, Sanders and Fitter (1992a) found that the level of arbuscularmycorrhizal colonization of roots of mixed plant assemblages in a naturalgrassland varied among plant species but not significantly within species overtime They could thus not come to any conclusion about the benefits ofmycorrhizal associations Sanders and Fitter (1992b) also could not correlateplant phosphorus, heavy metal content, and biomass to the degree of rootcolonization by mycorrhizal structures They thus suggest that the influence ofmycorrhizae in altering plant fitness may be nonnutritional, but as yet isunspecified

The distribution of fungal species in a mixed community of arbuscularmycorrhizal plant species is not homogenous Johnson et al (1992) showed thatthe arbuscular mycorrhizal community differed among five plant species of agrassland community In the same way, Eom et al (2000) showed that thedifferent species of plants in a tallgrass community have differing arbuscularmycorrhizal fungal associates(Fig 5.4).This information lends credence to theidea that there are feedbacks between the mycorrhizal fungal associate and

TABLE5.4 Responses of Different Plant Families to Arbuscular Mycorrhizal InfectionShowing a Continuum of Responses from Positive at One End to Negative at the Other

Mutualism Commensalism Neutralism AntagonismAsteraceae Burmanniaceae Gramineae Boraginaceae BrassicaceaeEricaceae Gentinaceae Caryophyllaceae ChenopodiaceaeFabaceae Monotroaceae Resedaceae PolygonaceaeLiliaceae Orchidaceae Scrophulariaceae

Pinaceae TriuridaceaePlantaginaceae

Ranunculaceae

Note: This variation in plant response is thought to invoke differences in competitive fitness of plant groups and thus determining plant community structure in any given set of environmental conditions Source: Data from Francis and Read (1995).

the plant that enable the plant species to dictate the fungal species assemblage andvice versa In a similar way, van der Heijden et al (1998) showed that thearbuscular mycorrhizal fungal community strongly influenced the plant speciescomposition of members of a European calcareous grassland ecosystem that wasconstructed in mesocosms At low mycorrhizal species diversity the plant speciesdiversity varied widely as the arbuscular mycorrhizal species in the community

we are altered Altering the species composition of the mycorrhizal fungi did notcause such large changes in the plant species composition at high mycorrhizalspecies diversity At these high mycorrhizal diversities, nutrient acquisition by

FIGURE 5.4 Cluster analysis of the similarity of arbuscular mycorrhizal fungalspecies associated with five host plants from: A, a mixed species tallgrass prairieecosystem (data from Eom et al., 2000); and B, garden plots in a native grassland (data fromJohnson et al., 1992)

the host plant community increased, leading to greater biomass accumulation.This information shows that the variability in function (nutrient acquisition)between a low diversity of mycorrhizal fungal species results in greaterasymmetric beneficial effects for plant growth The resultant patchy effect ongrowth among plant species would have considerable effects on the structure ofthe plant community if the growth of some species is enhanced more than others.

At high mycorrhizal diversity, however, each plant and each plant species has agreater chance of associating with an efficient mycorrhizal species In this case,the asymmetry in benefit is lost, a more even beneficial effect of the mycorrhizae

is seen throughout the plant community, and a shift in plant species communitystructure is unlikely

In a study of the effects of different arbuscular mycorrhizal fungi on thegrowth of the clonal plant Prunella vulgaris, Streitwolf-Engel et al (2001)showed that the number of ramets produced by the plant was significantly related

to the mycorrhizal species (Fig 5.5) They also showed, however, that stolonlength and spacing between daughter plantlets was determined by host genotype,not directly under the influence of the mycorrhizal partner As was the case inthe study of McHugh (unpublished) on Spartina spp., we can see that both thepresence of arbuscular mycorrhizal fungi and the species composition of themycorrhizal community influence the ability of clonal plants to colonize newareas by the production of stolons This attribute provides the plant with greatercompetitive abilities, which could be used to enhance site restoration

The differential influence of different mycorrhizal species in thecommunity may in part explain the effects of fungicide on plant species

FIGURE5.5 Mean number of ramets produced by the clonal plant Prunella vulgariswhen roots are colonized by a mixed community or specific strains of arbuscularmycorrhizae Source: Data from Streitwolf-Engel et al (2001)

diversity shown by Gange et al (1993) Here, the addition of fungicide reducedthe total root colonization of the plant community by arbuscular mycorrhizae,which in turn reduced plant species diversity It is possible that the fungicide haddifferential effects on different species of mycorrhizal fungi, thus reducingmycorrhizal diversity It must be remembered however, that soil factors may alsoconfound these interactions (Johnson et al., 1992).

The effect of the degree of mycorrhizal infection on the outcome of twocompeting plant species should explain the results shown above Watkinson andFreckleton (1997), however, modeled the interactions between the grassesHolcus lanatus and Dactylis glomerata in the presence and absence ofmycorrhizal infection Although the effect of mycorrhizal colonization of rootsaltered the competition/plant density response surface slightly, Holcus alwaysdominated over Dactylis, suggesting that the increase in plant performanceconferred on the plant by the mycorrhizal association was compensated for bychanges in the intra- and interspecific competition strengths

The competition among plants for nutrients is often given as a reason forthe evolution of specific plant assemblages, by which some plant species aremore able to access limiting nutrients than others This is one of the prime reasonswhy plant succession occurs The role of different mycorrhizal associates in theprocess of competition among plants for available soil phosphorus wasinvestigated by Pedersen et al (1999) They grew slash pine (Pinus elliottii )intentionally inoculated with the ectomycorrhizal fungus Pisolithus arhizus orfortuitously colonized by Thelephora terrestris and a native grass (Panicumchamaelonche ), which associates with arbuscular mycorrhizae Pine inoculatedwith P arhizus took up more P when competing with the nonmycorrhizal grassthan when competing with another pine, irrespective of the mycorrhizal status ofthe competing pine seedling From an analysis of the phosphate uptake kinetics, itwas found that pine is more competitive at higher nutrient concentrations, whilethe grass is more competitive at lower nutrient concentrations, suggesting aseparation in niche between the two plants

The degree of response to mycorrhizal infection by each of the componentplants in a community may or may not be similar Taking Simpson’s paradox asthe basic model, by which the response of the whole may not be based on theresponse of the individual parts, Allison and Goldberg (2002) explored theresponses of individual plant species in communities to both arbuscularmycorrhizal association and the availability of phosphorus in soil Their data setwas derived from the published literature Their conclusion was that they couldnot predict an overall community response that was the sum of consistent trends

in response of the component plant species They were therefore forced to rejectthe first hypothesis that the degree of dependence of all plant species increased asavailable phosphate levels declined, based on the fact that all individual plantspecies had consistent response trends in the same direction(Fig 5.6a) Their

second hypothesis stated that the direction of response of each individual plantspecies to degree of mycorrhizal infection in relation to P supply was different.

As a consequence, there was no net community response (Fig 5.6b) If thissecond hypothesis is really what happens in plant communities, it is easy to seehow the varied responses of the individual plant species to both mycorrhizalcolonization and environmental variables would lead to changes in communitystructure as conditions changed The magnitude of the effect of mycorrhizal fungi

to influence this change would be proportional to the relative effect of plantfitness enhancement provided by the mycorrhizal fungi to each individual plantspecies

The influence of mycorrhizae on plant performance is influenced byedaphic controls exerted by changes in soil chemistry Bever et al (1997)developed a model to explain the importance of feedback mechanisms betweenthe soil community and plant population dynamics Using mixtures of four plantspecies, they demonstrated that growth could be enhanced or inhibited by soils inwhich the same or different plant species had been previously grown(Fig 5.7).They suggest that changes in the soil organisms and nutrients or plant-antagonistic chemicals can act in either a positive or negative feedbackmechanism to affect growth of subsequently planted species Similar changes

in plant fitness can be related to small-scale in soil nutrient availabilityheterogeneity Farley and Fitter (1999) showed that root proliferation of seven

FIGURE 5.6 Models of the response between arbuscular mycorrhizal plants tomycorrhizal infection and soil phosphorus availability Graph a depicts each plant species

in the community responding in the same way, with a reduction of mycorrhizalcolonization of roots with increasing P supply In this situation, the net ecosystem effect isfor a general reduction in mycorrhizal associations Graph b depicts a variable response ofeach plant species in the community, resulting in a net lack of mycorrhizal responsethroughout the ecosystem Source: From Allison and Goldberg (2002)

co-occurring woodland plant species responded differently to localized rich patches in soil This difference in response was not affected by mycorrhizalstatus, but the differential growth response led to an improved level ofcompetition by the plant species that responded by producing more root biomass.The effect of leaf litter chemistry on the growth of roots andectomycorrhizal community structure has been shown many times (Baar and

nutrient-de Vries, 1995; Baar et al., 1994; Walker et al., 1999; Conn and Dighton, 2000;Dighton et al., 2000) The effect of weed species leaf litter on the growth andmycorrhizal development of a native tree species was shown by Walker et al.(1999) They showed that leaf litter of Rhododendron maximum, an invasiveweed of southern Appalachian forests, affected the growth of native hemlock(Tsuga canadensis ) Hemlock tree seedlings planted under hemlock litter hadthree times the intensity of ectomycorrhizal colonization of their root system,four times the root ramification (branching), and twice the biomass of treesplanted into leaf litter form rhododendron thickets(Fig 5.8).In addition, trees inrhododendron litter had a significantly higher proportion of Cenococcumgeophilum mycorrhizae than trees outside rhododendron litter It is suggested thatthese changes are important in driving the trajectory of vegetation communitydevelopment in regenerating forests in this ecosystem This gives us a hint of theeffects of leaf litter leachates or root exudates from one plant that affects a secondplant This activity is often referred to as allelopathy and will be discussed furtherlater in this chapter

FIGURE5.7 Test of feedback of soil communities and plant growth for the speciesAllium (All), Anthoxanthum (Anth), Panicum (Pan), and Plantago (Plan) The Y axis is thegrowth of plants in their own soil relative to that in each other’s soil Source: Data fromBever et al (1997)

Recently direct net transfer of carbon or nutrients between plants in thecommunity has been shown to occur in natural ecosystems Formerly this ability

of interplant linkage through mycorrhizal bridges has only been demonstrated incontrolled conditions Simard et al (1997a,b,c) showed transfer of carbon frompaper birch (Betula papyrifera ) to Douglas fir (Pseudotsuga menziesii ) in bothpartial and deep shade They showed that the amount of carbon transferredbetween plants represented 13 – 45% of the carbon contained in shoots for P.menziesii and 45% for B papyrifera, respectively This represents a considerablesupplement of photosythetically derived carbon to the recipient plant Wu et al.(2002) also showed that 24% of14C label occurring in the underground parts ofpine seedlings was allocated to the extraradical hyphal component of theirectomycorrhizal association They concluded that much of this carbon would beavailable to other plants that could share the same mycorrhizal symbiont Thissharing of resources between different plant species within the community thusalters our concept of the stability of plant assemblages being based oncompetition among plants for available resources (nutrients, water, and light).The new paradigm should incorporate both competition and synergism betweenplants within a community We do not know the extent of this sharing ofresources between plants via mycorrhizal connections, however The examplesshown here represent conditions in which one plant is at a disadvantage by being

in the shade If source-sink relations do not differ between connected plants, doesthe linkage become redundant? One could also envisage that these connectionscould be used for parasitism of one plant upon the other Examples exist in thenatural ecosystem in which this occurs, such as the achlorophyllous plantMonotropa, which shares mycorrhizal associations with the roots of trees (Smithand Read, 1997) This association was used as one of the first demonstrations ofcarbon transfer between plants, assumed to be via the mycorrhizal connection

FIGURE 5.8 Total mycorrhizal colonization (a) and proportion of Cenococcumgeophilum mycorrhizae (b) on hemlock trees in the presence (solid bars) and absence(hatched bars) of Rhododendron maximum leaf litter Source: Data from Walker et al.(1999)

(Bjo¨rkman, 1960) and considered by Bjo¨rkman to be an example ofepiparasitism.

These interplant connections may be important in determining thecoexistence of arbuscular mycorrhizal plant communities Walter et al (1996)demonstrated the existence of interplant transfer of phosphorus in tallgrass prairiecommunities The amount of phosphorus transferred from donor to recipientplant was species-dependent and decreased with increasing distance betweenneighboring plants The transfer between plants was greater within forbs and coolseason C3 grasses than in C4 grasses, indicating selectivity in the interplanttransfer This difference may alter the competitive abilities of the plant Theeffect of benomyl as a fungicide to reduce mycorrhizal infection did not alterrates of transfer of phosphorus, probably as mycorrhizae were still present in thebenomyl-treated plants In an experiment to demonstrate the effects of arbuscularmycorrhizal association on intraspecific interactions, Ronsheim and Anderson(2001) surrounded a target Allium vineale plant with genetically identicalneighbors, neighbors from the same population, or neighbors from a differentpopulation The presence of mycorrhizal fungi was beneficial for plant growth,especially if the neighbors were genetically identical or from the same population

as the target plant There is thus specificity in the interaction between A vinealeplants and the soil fungal community at the population level that specificallyfavors intraspecific interactions among plants from the same population Thisfinding suggests that plants from the same population are able to share a moreefficient hyphal network than if individual plants were spatially separated

Harper (1990) casts some doubt on the role of pathogens in altering populationsand communities of their hosts He cites examples of dramatic negative effects offungal pathogens on introduced or alien plants or on native plants by alien fungalpathogens He suggests, however, that such dramatic effects of pathogens arerarely seen where there has been evolution of communities of organisms in theirnatural environment Is it possible that the extreme interactions have already beenplayed out earlier in the development of the plant communities, and that thecurrent interactive responses of alien and native species of plants or fungi onlyrepresent what has happened in the past?

Much of the effect of plant pathogens on plant populations or plantproduction has been recorded from exotic pathogenic fungal species or the effect

of resident pathogens on exotic plant species Indeed, the problems associatedwith the global movement of invasive plants and fungi are attracting increasinginterest from researchers, farmers, and economists (Rossman, 2001) Inparticular, the rapid evolution of introduced plant pathogens by genetic change,induced by their new environmental conditions, is of great concern in terms of

devising potential control methods (Brasier, 2001) The survival of economicallyimportant exotic crops continues to be challenged by the emergence of localdiseases that adapt to new host plants Wingfield et al (2001) discuss the impact

of exotic fungi on exotic plantation forest trees in the tropics that can inducesevere loss of forest trees with disastrous economic consequences Brasier (1990)reviews the devastating effects of the chestnut blight fungus Cryphonectriaparasitica, which was probably imported from China, on chestnuts in NorthAmerica The rapid spread of this disease, at about 37 km per year, and significantreduction in fitness of the host tree, which now exists as an understory shrubspecies rather than a dominant canopy tree, is witness to the effect of anintroduced pathogen In a similar way, the fungus Ophistoma ulmi caused

America Resistance of the trees was seen to occur, however Some of thisapparent resistance is because of the genetic variation in host plantsproducing actual resistance (Burdon et al., 1990; Crute, 1990), but some wasdue to the presence of fungal pathogenic mycoviruses (Brasier, 1990) thatreduced the effectiveness of the fungal pathogen

In a similar way, the decline in oaks in southern Europe due to thedestructive effects of the oomycete pathogen Phytophthora cinnamomi has beenreviewed by Brasier (1996) In the Mediteranean regions, this fungus has beenresponsible for significant decline in the evergreen oaks Quercus suber and

Q ilex, thus significantly altering the community structure of the oak forestecosystems of this region in Spain, Portugal, Tunisia, and Morocco The spread

of this fungus through soil is by virtue of motile oospores that require wet orwaterlogged soil for optimum dispersal Climate change models of this areapredict increasing rainfall in these regions, which would result in a potentialincrease in the rate of spread of the disease Brasier (1996), however, suggeststhat the severity of cold winters in central and northern Europe would limit thenorthward spread of Phytopthora

Alexander (1990) chronicles the effect of a fungal pathogen (Ustilagoviolacea ) on the alien plant species (Silene alba ) in the eastern United States.This anthersmut fungus invades the stamens and replaces them with fungalstructures In female flowers, the fungus causes abortion of the ovary Even if thefungus systematically infects the plant, there appears to be little effect on thesurvival of the plant other than a loss of its reproductive potential Some plantswithin the community develop resistance to the pathogen, so the ready dispersal

of fungal spores and the patchy occurrence of resistant plants results in afragmented community of plants with varying degrees of fungal infection withinthem It is therefore likely that this heterogeneity maintains some equilibriumbetween the abundance of host plants and the pathogenic fungus This may bewhat occurs during the evolution of plant communities, exploring why there is noevident effect of fungal diseases on natural plant communities

Paul (1990) suggests that the interactions among the host plant, pathogenicfungus, and environment can significantly vary the outcome of the severity of thepathogenic symptoms For example, he suggests that the degree of loss ofphotosynthetic capacity of a plant due to fungal invasion will be greater in a plantgrowing in the shade than one growing in full light Similarly, he cites work tosupport the fact that fungal pathogen effects are greater in nutrient-poor ordroughty conditions, in which the fungus competes with the host plant for limitedresources The level of the impact of a pathogen thus may be greater on plantsgrowing in marginal habitats than those in optimal habitats This would certainlyalter the competitive abilities of plants growing in marginal conditions Thisreduction in fitness of a pathogen-infected plant is significant when the host plant

is grown in a mixture with a nonhost plant The reduced performance of Seneciovulgaris in the presence of the fungal pathogen Puccinia lagenophorae wasshown to improve the competitive abilities of Lactuca salvia (Paul and Ayres,1987), Euphorbia peplus (Paul, 1989), and Capsella bursa-pastoris with whichthey were grown

Hansen and Goheen (2000) reviewed the effects of the root rot fungusPhellinus weirii in coniferous forests western North America: which are, largelycomposed of hemlock and Douglas fir The fungal pathogen slowly kills trees andthe infection spreads from a central infected tree to neighbors in such a way that

on death, gaps are created in the forest, allowing invasion by other plant species.Within these gaps the diversity of vegetation during successional colonizationincreases in both species richness and evenness, compared to the original speciescomposition Changes in the resistance of trees to the pathogen appear to be due

to the nutrition of the host tree As the infection front advances, dead treescontribute to the nutrient pool in the soil, and the elevated level of nitrogenavailable to the succeeding generation of trees confers a greater resistance to thepathogen Indeed, Zhang and Zak (1998) showed that the changes in bacterial andfungal activity in gap soils was significantly different from that under closedcanopy forest in subtropical forest ecosystems This change in metabolic activityincreased plant litter decomposition in gaps, creating greater mineralization ofnutrients

Alexander and Mihail (2000) determined if the effect of seed and seedlingmortality due to a fungal pathogen on plant population dynamics depended on thedegree to which growth and reproduction of surviving individuals compensate fordeaths Using the annual plant Kummerowia stipulacea at three planting densitiesand the root fungal pathogen Pythium species, they found that high sowingdensity reduced seedling establishment and size In the presence of the pathogen,seed and seedling survival was low and plants were initially smaller, but atmaturity, the average surviving pathogen-infested plants were larger than in theother treatments This suggests that the effect of the pathogen allows the survivingplants to be released from intraspecific competition There thus may be a role for

fungal pathogens in determining interplant spacing to minimize competition andincrease fitness Interactions between shade and available water levels in thecompetition between oak and woody shrub species in savanna ecosystemssuggests that the intervention of oak wilt fungi can cause a difference betweencompetition between oaks and woody shrubs and facilitation of shrub layercommunities (Anderson et al., 2001) Water tables around healthy mature oakswere lowered, thus reducing shrub layer community development, but shrublayer communities were able to establish where oak wilt reduced the growth ofoak trees.

The effect of reduction of plant fitness during the process of primary orsecondary succession can alter the trajectory of the assembly of plant species inthe community Holah et al (1997) showed that the effect of the root-rottingfungus Phellinus weirii reduced the development of Douglas fir (Pseudotsugamenziesii ) in areas of pathogen abundance (infection centers) These areas werecolonized more successfully by shrubby growth of western hemlock (Tsugaheterophylla ), thus changing both the species composition and the canopyarchitecture of the forest (Fig 5.9) In contrast, the effect of introducedanthracnose of dogwood caused by Discula destructans has caused a change inthe plant community structure of forest ecosystems of the Cumberland Plateau inTennessee By selectively reducing the population of dogwood trees, thevegetation has become dominated by two bird-dispersed tree species, blackgumand spicebush In addition to the change in the forest community, loss of thedogwood trees has reduced the cycling of calcium in the ecosystem, with theconsequential effects of the reduced availability of calcium to birds through theirinsect food, resulting in poor egg survival (Hiers and Evans, 1997)

A rather more remote interaction between plant pathogens and plantperformance is discussed by Whitham and Schweitzer (2002) The ecosystem-level effects are brought about by changes in leaf litter chemistry as a result ofleaf-inhabiting fungal pathogens Pathogens induce the development of higherlevels of plant-defense chemicals (polyphenols), especially tannins The highercontent of these chemicals reduces the palatability of dead leaves to soil fauna,and by increasing the C:N ratio of leaf material, reduces the ability ofsaprotrophic and mycorrhizal fungi to decompose the leaf litter and obtainnutrients from within (Ha¨ttenschwiler and Vitousek, 2000) Ha¨ttenschwiler andVitousek conclude that with repeated or sustained high pathogen levels in plants,this positive feedback mechanism could reduce soil fertility at a local andpossibly regional level

Interest has also arisen in the potential role of fungal pathogens asbiocontrol agents for commercially important and exotic plant species Forexample, Pieckenstain et al (2001) showed that the fungus Epicoccumpurpuascens produces antifungal compounds to inhibit Sclerotinia head rot insunflowers In agriculture, Tsahouridou and Thanassoulopoulos (2002) have

shown that Trichoderma koningii is a good biological control agent for dampingoff of tomato by Sclerotium rolfsii In the tropics, Evans (1995) suggests that it isimpractical and undesirable to use herbicides in more fragile agroecosystems andnatural areas because of the unknown secondary effects of these chemicals Incontrast, biocontrol agents, such as pathogenic fungi, may be more desirable foruse in reducing the abundance of exotic plant species Although the science offungal biocontrol of weeds has not been perfected in these ecosystems, there areindications that the fungal pathogen flora of plants changes significantly from itsnative range to that its exotic range(Table 5.5).The fact that there is minimaloverlap of fungal pathogen species in both the native and exotic ranges suggests

FIGURE5.9 Changes in the relative basal area of Douglas fir trees in relation to latesuccessional trees (A) or shrubs (B) in the H J Andrews forest as a result of the root-rotting fungal pathogen Phelliunus weirii Changes are indicated by arrows showing trends

in response from plants outside infection centers (solid symbols) to areas within infectioncenters (open symbols) Source: Data modified from Holah et al (1997)

TABLE5.5 Tropical Weed Plant Species and the Number of Pathogenic Fungi Associated with Them in Their Native Range and in theRange in Which They Are Common Exotics

Plant species Native range

Number of

Number offungal species

Number of fungalspecies in commonChromolaena

odorata

Mikaniamicrantha

Lantanaacmara

Cyperusrotundud

Sudan,Pakistan,India

19 Neaotropics, Southeast Asia,

Oceania, Australia

Euphorbiaheterophylla

Euphorbiahirta

Source: Data from Evans (1995).

that there is scope for the selection of effective pathogen species in the plant’sexotic range to effectively reduce its fitness.

Interestingly, it is not only the plant whose fitness may be affected by apathogenic fungus The interactions between pathogens on a plant may affect thefitness of the pathogenic fungi themselves In a study of rust fungi on wheatleaves, Newton et al (1997) showed that the relative fitness of a number of strains

of the rust Puccinia graminis was controlled by density-dependent relationships.For example, relative fitness of the fungal strain SR22 was much greater at lowspore densities on the leaf than at high density At these low densities, which werewell below the carrying capacity, the high infection efficiency of SR22 gave it acompetitive edge As spore density of a mixed spore inoculum on the leafincreased, however, the strong competitive abilities of strain SR41 allowed it todominate in the community In the natural ecosystem, the effect of fungalpathogens on individual plants thus may depend upon the outcome ofcompetition of the fungal pathogens within their own community as much asthe competition between saprotrophic fungi and pathogens

BIOCONTROLThe presence of saprotrophic fungi on plant surfaces is a long accepted fact (Lastand Deighton, 1965) Leaves of terrestrial plants support extensive and diversecommunities of both pathogenic and nonpathogenic fungi (Dickinson and Preece,1976; Preece and Dickinson, 1971; Farr et al., 1989; Kenerley and Andrews,1990; Blakeman, 1992; Donegan et al., 1996) Many saprotrophic members of thephylloplane have been shown to be antagonistic toward plant pathogens Forexample, Omar and Heather (1979) showed that Alternaria and Cladosporiumspecies were more effective inhibitors of Melampsora larici-populina on poplarleaves than Penicillium(Fig 5.10).Sharma et al (1988) and Singh and Khara(1984) examined changes in radial growth of mycelial inoculum discs ininteractions of one saprotroph antagonist and a single pathogen (Alternariasolani ) In a study conducted by Blakeman and Brodie (1977) competition fornutrients among the epiphytic members of the phyllosphere of beetroot leaveswas shown to negatively affect the germination of spores of plant pathogens.Upadhyaya and Arora (1980) evaluated the effect of fungal growth-stalingproducts on phylloplane fungi In a study of the development of the fungalpathogen Pestalotiopsis funereal on Eucalyptus globules, they found that leafdiscs treated with the growth-staling products isolated from the leaf-inhabitingmicrofungi of E globulus resulted in a significant decrease in the number offungal pathogens

Most studies of this type have observed interactions between a singlesaprotroph and a single plant pathogen; very few have looked at two or moresaprotrophs in combination as antagonists Members of the phyllosphere fungalcommunity have been shown to coexist, however, but the functional role of theorganisms as a community rather than as isolated individuals has not beenadequately investigated (Fokkema, 1991; Bills, 1995).

The inhibitory attributes of phylloplane fungi have been used to developfungal pathogen biocontrol agents In a review of the interactions betweenphylloplane microorganisms and mycoherbicide efficacy, Schisler (1997)discusses only single species interactions or the effects of microbial metaboliteswithout discussing the individual organisms or communities of organisms thatmight produce these metabolites Janisiewicz (1996), however, evaluated theeffects of multispecies combinations of yeasts and bacteria for their abilities tocontrol blue mold (Penicilium expansum ) on harvested apples He suggested thatthe optimal species mix occurred when there was minimal niche overlap amongthe species The resultant minimal competition among antagonist microbialspecies allowed maximal competitive interaction between the antagonist and thepathogen

Because of the documented inhibitory effect of leaf saprotrophs againstfoliar pathogens, other work has evaluated the effects that current managementpractices of fungicide application has on the phylloplane community and how itmight increase the pathogen’s ability to initiate disease where the saprotrophicmembers of the phylloplane community have been eliminated or reduced by

FIGURE5.10 Effect of saprotrophic leaf surface fungi on the development of uredinalpustules of Melampsora larici-populina Saprotroph conidia incubated beforeuredinospores added (open bar), conidia, and uredospores as a mixed inoculum (solidbar) and uredinospores added before conidia (hatched bar) compared to infection withoutsaprotroph (control) Source: Data from Omar and Heather (1979)

the fungicide Fokkema and de Nooij (1981)found that some fungicides reducedthe ambient mycoflora while others had no effect Thomas and Shattock (1986)also tested this idea by applying three different fungicides (benomyl, triadimefon,and chlorothalonil) to Lolium perenne that had the pathogens Drechslera siccansand D dictyoides in addition to other saprotrophic filamentous fungi They foundthat the three fungicides altered the incidence of the phylloplane mycoflora invery different ways Benomyl reduced most saprotrophs but allowed the levels of

D siccans and D dictyoides to increase over control levels by 37% and 90%,respectively This showed that in the absence of saprotrophs to antagonize them,the pathogens were able to flourish beyond the established controls Triadimefonreduced the level of pathogenic species and increased the abundance of mostother common saprotrophs Chlorothalonil removed virtually all fungi from thesurface of the leaves For agricultural purposes, there thus needs to be a balancebetween encouraging natural competitors against plant pathogens and the use oftraditional fungicide treatments The importance of a protective saprotrophicfungal community on leaf surfaces, however, may only play an important part inreducing pathogenic fungal invasion during the short time the host plant issusceptible and when the spores of the pathogenic fungus are abundant for leafinoculation

The community interactions in the phylloplane and their ecologicalsignificance have been explored in the review by Be´langer and Avis (2002) Theysuggest that the diversity of fungal inhabitants on a leaf surface occur as a result

of niche separation based on the temporal and spatial diversity of resources Moy

et al (2000), however, showed that the fungal endophyte Neotyphodiumtyphinum formed epiphyllous networks of hyphae on the leaf surface of a number

of grass species, particularly Bromus setifolius and Poa ampla They suggest thatthese epiphyllous fungal networks could possible act antagonistically towardfungal pathogens The mechanism of this protection may be by direct fungal –fungal interactions or by virtue of prior space occupancy; thus, they contest,many of the fungi may not be in competition with each other, but are utilizingunique resources They argue further that if this niche separation is true thenevidence in the literature would not support the hypothesis of a saprotrophicfungal community affording protection to plant pathogens Citing theexperiments of Rishbeth (1963) on competition between Peniophora gigantaand the pathogen Fomes annosus, they argue that the defense is merely a delay inallowing access of the pathogen to its optimal resources Whether this is defense

or inadvertent competition is somewhat semantic, as the result is a delay in thecolonization of plant tissue by a pathogen Similarly, Be´langer and Avis (2002)suggest that the hyperparasitism shown by Trichoderma spp is probably the mainmode of action of members of this genus They reason, however, that thisparasitism of other fungi that occur in nature have rarely been shown to be aneffective means of biocontrol when the density of Trichoderma has been

artificially increased Jeffries (1997) reviewed the subject of mycoparasitism andcame to the conclusion that this modus operandi is difficult to quantify in regard

to its effect on populations of either fungal species Evidence is cited in hisreview of positive correlations between host fungal hyphal density and that of theparasitic fungus, suggesting a direct trophic effect He does, however, suggestthat this aspect of fungal ecology could have great importance in reducing plantpathogenic fungi, although much of this information originates from the study ofagricultural crops rather than the natural plant communities Marois and Coleman(1995) also suggest that understanding the ecology of successions of phylloplanefungi could point to the appropriate species to combat pathogenic fungi Theysuggest that the succession of fungi colonizing developing leaves is analogous tothe colonization of freshly fallen dead leaves in the decomposer community.Their hypothesis is that an r-selected plant pathogenic fungus would best becontrolled through competition, whereas a K-selected pathogen would beeffectively combated by a mycoparasite

The competitive interactions between saprotrophic and pathogenic fungialso occur in the rhizosphere Whipps (1997) reviewed some of these fungal –fungal interactions, showing that the types of interactions could be classified as

“direct antagonism” by mycoparsitism, antibiosis, or direct competition, orthrough “indirect interactions” by the fungal induction of resistance and by plantgrowth promotion An example of sustained mycoparasitism in the rhizosphere isthat of the control of Rhizoctonia by Verticillium biguttatum (Van den Boogertand Velvis, 1992; Van den Boogert and Deacon, 1994) The production ofantibiotics by fungi in the rhizosphere has been reviewed by Lynch (1990) Theintroduction of nonvirulent forms of pathogenic fungal species has been shown toinduce disease resistance to plants (Mandeel and Baker, 1991; Martyn et al.,1991) Most of these studies, however, have been conducted in agriculturalsettings or in artificial conditions; the importance of these interactions in naturalecosystems and their influence on plant fitness is largely unknown

Mycorrhizal fungi have been known to be effective in the prevention of rootpathogen fungal attack on the host plant (Garbaye, 1991) As Smith and Read(1997) suggest in their review of the effects of ectomycorrhizae in pathogenresistance, however, much of the work has been conducted in unrealistic nurseryconditions The actual role of these mycorrhizae as antagonists to plant pathogens

in nature are largely unknown Indeed, even recent work of Branzanti et al.(1999) that demonstrated the significant effect of inoculation of chestnut treeswith the ectomycorrhizal fungi Laccaria laccata, Hebeloma crustuliniforme,

H sinapizans, and Paxillus involutus on preventing chestnut ink disease caused

by Phytophthora cambivora and P cinnamomi was conducted on seedling trees

(Table 5.6) Suppression of root rot, caused by Cylindrocarpon destructans byarbuscular mycorrhizal inoculation of peach trees by Glomus aggeragatum, wassimilarly demonstrated in an experimental system with tree seedlings (Traquair,1995)(Fig 5.11).

In contrast, the effect of arbuscular mycorrhizae and defense against plantpathogenic fungi has been studied to a greater extent, especially in annual plants.Much of this work has concentrated on agricultural crops, however, and thereforemay be equated to the artificial conditions identified for research onectomycorrhizal fungi An example of this kind of work is that of Lui (1995)

on cotton Here the effect of inoculation with the arbuscular mycorrhizae Glomushoi, G mosseae, and G versiforme significantly improved growth andestablished a significant defense against the wilt fungi Verticillium dahliae(Table 5.7) Similarly, Abdalla and Abdel-Fattah (2000) showed that peanutplants had a reduced incidence of root fungal pathogens when inoculated with thearbuscular mycorrhizal fungus Glomus mosseae than they did in the absence ofmycorrhizae The benefit of mycorrhizal colonization of roots was both anantagonism against the two fungal pathogens, Fusarium solani and Rhizoctoniasolani, and a growth enhancement of the host plant, leading to greater fitnessexpressed in terms of seed production(Table 5.8)

From the data derived from mixed-species grassland, Sanders and Fitter(1992a,b) suggest that the role of arbuscular mycorrhizal colonization of plantroots may be nonnutritional In a study of the annual winter grass Vulpia ciliata in anatural plant community, Newsham et al (1994) used two fungicides, benomyland prochloraz, to selectively reduce infection by arbuscular mycorrhizae andpathogenic fungi, respectively Their determination of plant performancesuggested that there was direct interference between the mycorrhizal andpathogenic fungi, and although the plants did not show pathological symptoms,

TABLE5.6 Effect of Inoculation of Chestnut Seedlings (Castaneasativa ) with Ectomycorrhiza Against the Effects of the Chestnut Ink StainFungal Pathogen Phytopthora cambivora

Fungal treatment

Leaf area(cm2)

Plant weight(g)

Phytopthora alone 15.6 5.2Phytopthoraþ Laccaria laccata 28.1 9.4Phytopthoraþ Paxillus involutus 19.5 6.1Phytopthoraþ Hebeloma crustuliniforme 22.0 5.9Phytopthoraþ H sinapizans 28.1 10.2

Source: Data from Branzanti et al (1999).

the mycorrhizal fungi induced greater fitness in the plants as a result of competitionwith the pathogen It was also inferred from the data that this was the primefunction of the mycorrhizal association, rather than improving phosphorus uptake

by the host plant This type of study on natural plant communities is altering the

FIGURE5.11 Degree of cylindorcarpon root rot in peach tree seedlings inoculated withthe mycorrhizal fungus Glomus aggregatum Inoculated trees received a conidialsuspension of Cylindrocarpon destructans Source: Data from Traquair (1995)

TABLE5.7 Growth and Disease Status of Cotton PlantsGrown in Association with the Wilt Pathogen Verticilliumdahliae, Arbuscular Mycorrhizae, and Combinations of theTwo

Treatment Plant height (cm) Disease incidence (%)

Source: Data from Lui (1995).

dogma of the function of mycorrhizae as being enhancement of host plant nutritionalone Much more research needs to be done, however, to show the relativeimportance of mycorrhizae in nutrient uptake and plant defense A discussion ofthe arbuscular mycorrhizal benefits afforded to host plants in terms of nutrientacquisition and growth enhancement on the one hand and the protection of the hostplant against fungal root pathogens on the other led Newsham et al (1995) toconclude that the benefits were related to the root architecture of the host plant Intheir model(Fig 5.12),Newsham et al (1995) suggest that the derived benefit of amycorrhizal association is predominantly nutrient acquisition if the host plant rootsystem is poorly branched In contrast, the benefit shifts toward pathogenprevention where the host root system is highly branched.

The distribution of root pathogens in soil and their ability to infect hostplants may be an importance determinant in the germination and survival ofcertain plant species Augspurger (1990) shows how the effect of damping offfungi (Phytophothora, Rhizoctonia, Pythium, and Fusarium ) influences thedevelopment of tropical forest tree species that develop in forest gaps In many ofthese tropical tree species, seed dispersal is limited to within 100 m of the parenttree Augspurger’s research suggested that seedlings that germinated close to theparent tree had a higher percentage of loss due to damping off than seedlingsdeveloping further from the parent tree These findings substantiate thehypothesis proposed by Janzen (1970) and Connell (1971) referred to as theJanzen – Connell hypothesis The essence of this hypothesis is outlined by Clarkand Clark (1984), in which both the effects of root pathogens and the higher

TABLE5.8 Effect of the Arbuscular Mycorrhizal Fungus Glomus mosseae on Growthand Fecundity of Peanut Plants at Maturity Infected with the Root Pathogenic FungiFusarium solani and Rhizoctonia solani

Growthparameters

Yieldbiomass

Treatment Shoot weight (g)

Number

of branches

Pods perplant

100 seedweight (g)

Mycorrhizal 13.0 8.3 12.3 72.5

Mycoþ Fusarium 7.8 6.5 10.6 65.9Rhizoctonia 6.9 5.0 7.0 39.8Mycoþ Rhizoctonia 9.1 6.7 8.7 60.5Fusariumþ Rhizoctonia 5.8 5.0 5.3 38.4

Source: Data from Abdalla and Abdel-Fattah (2000).

incidence of herbivore grazing on seedling plants restricts the development ofconspecific species under the canopy of mature tropical trees (Fig 5.13) Thehypothesis suggests that this is a mechanism favoring dispersal of seeds awayfrom parent trees and stimulates colonization of forest gaps Recent evidencefrom controlled experiments supports this hypothesis (Packer and Clay, 2000;van der Putten, 2000) In their studies, the alleviation of the pathogenic effect ofsoils under a parent tree was achieved by soil sterilization This sterilizationprocess reduced the incidence of Pythium damping off of black cherry treeseedlings(Fig 5.14).It is difficult to argue, however, if the pathogen alone isinfluencing the spatial pattern of successful seedlings Seedlings growing in theshade of a parent tree probably exhibit signs of stress because they are growing atsuboptimal light levels This may make them more vulnerable to root pathogensthan those seedlings growing in optimal light conditions toward the centers of thegaps A similar mechanism has been shown to affect recruitment of Ocotea whiteiseedling trees under canopies of adults of the same tree species on BarroColorado Island, Panama, because of the presence of a fungal tree canker.Seedling survival is significantly higher under the canopy of a nonsusceptibletree, Beilschmiedia pendula (Gilbert et al., 1994).

In contrast to this hypothesis, the links among conspecific plants bymycorrhizal bridges has been shown to confer advantages to the seedlings because

of interplant transfers of carbon and nutrients (Amaranthus and Perry, 1994; Read,1998; Rayner, 1998) Amaranthus and Perry (1989) showed that when Douglas firseedlings were planted into forest gaps close to adult trees, survival approached90% Where seedlings were planted at great distances from parent trees, survivalafter 2 years was only 50% Amaranthus and Perry attributed the reduction insurvival to the lack of a viable, communal ectomycorrhizal network into which

FIGURE5.12 Nature and magnitude of the benefit derived from plant associations witharbuscular mycorrhizae, depending on the branching pattern of the host plant root system.Source: Redrawn from Newsham et al (1995)