FUNGI IN ECOSYSTEM PROCESSES - CHAPTER 5 pptx

5 Fungi and Population and Community Regulation Population and community regulation can result from either promotion or reduction in the growth, fitness, or reproduction potential of an organism. If the fitness of one organism in the community is altered to a greater extent than another, the result is a changed dominance of the favored species in the community that occurs over successive generations. In Chap. 3 we showed how primary production was positively influenced by mycorrhizal fungi that assisted plants in obtaining essential nutrients and water and by endophytes that reduced the effects of faunal grazing on the plant. In addition, we saw how plant pathogenic fungi could reduce plant production, as measured by biomass, and also by the fecundity of the plant, as measured 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 same direction to the influence of a fungus), there will be selective pressures exerted on members of the community. Those species exhibiting enhanced growth and fecundity 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 that fungal pathogens of animals could also influence both the population of the animal and its occurrence in the community of animals of the same trophic or functional group. Despite the extensive literature on the effects of fungal pathogens on a variety of faunal groups, however, there is little documented evidence 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 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. 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 in populations of organisms and alter community composition. The interactions considered in this chapter are summarized in Table 5.1. 5.1 MYCORRHIZAE AND PLANT SUCCESSIONS Pedersen and Sylvia (1996) suggest that one of the major components determining the success of early colonizing plants during plant seral succession is the availability of nutrients. In this context the ability of plants to associate with mycorrhizal fungi and enhance their ability to sequester nutrients from a limited resource 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 an important determinant of mycorrhizal inoculum for plants in the early stages of succession on bare ground. The distribution of mycorrhizal fungal spores by animals is rarely random, however. Small mammals defecate in middens and are likely to deposit more spores in areas of active feeding sites than in other localities. This patchy distribution of mycorrhizal inoculum potential has an influence on the type of plant that can be successful in each microhabitat. For example, M.F. Allen (1991) suggested that the presence of mycorrhizae increased the diversity of plant species colonizing new areas. The patchy distribution of mycorrhizal spores, and hence inoculum potential, would allow the establishment of both mycorrhizal and nonmycor rhizal plant species in the community. It has been shown that during primary colonization, myc orrhizal inoculum potential can vary from none to abundant in locations only centimeters apart (Allen and MacMahon, 1985). In his book, M.F. Allen (1991) compares the importance of mycorrhizae in the re-establishment of vegetation following disturbance in a variety of ecosystems. From his own work he showed that vegetation colonizing Mount Saint Helens consisted entirely of mycorrhizal species, both arbuscular mycorrhizal and ectomycorrhizal forms. In contrast he cites the work of Schmidt and Scow and Hendrix and Smith in the Galapagos, where a mixture of arbuscular mycorrhizal and nonmycorrhizal plants established. In this case the distribution of mycorrhizal associations was related to soil nutrient content, with nonmycorrhizal plants developing in the more fertile, lowland soils and mycorrhizal plants establishing in the poorer rocky soils. From these and other studies, Allen and Allen (1990) hypothesized a number of patterns of mycorrhizal dependence in developing ecosystems in relation to nutrient and water availability. 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 on volcanic substrates of Mt. Koma, Japan, however, Titus and Tsuyuzaki (2002) found no effect of microsite on the arbuscular mycorrhizal colonization of Chapter 5244 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. TABLE 5.1 Ecosystem Services Provided by Fungi Ecosystem service Fungal functional group Soil formation Rock dissolution Lichens, Saprotrophs, Mycorrhizae Particle binding Saprotrophs, Mycorrhizae Soil fertility Decomposition or organic residues Saprotrophs (Ericoid and ectomycorrhizae) Nutrient mineralization Saprotrophs (Ericoid and ectomycorrhizae) Soil stability (aggregates) Saprotrophs, Arbuscular mycorrhizae Primary production Direct production Lichens Nutrient accessibility Mycorrhizae Plant yield Mycorrhizae, pathogens Defense against pathogens Mycorrhizae, Endophytes, Saprotrophs Defense against herbivory Endophytes Plant community structure Plant–plant interactions Mycorrhizae, pathogens Secondary production As a food source Saprotrophs, mycorrhizae Population/biomass regulation Pathogens Modification of pollutants Saprotrophs, mycorrhizae Carbon sequestration and storage Mycorrhizae (Saprotrophs) 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. Fungi and Population and Community Regulation 245 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. Agrsotis scabra. Campanula lasiocarpa, on the other hand, showed a higher rate of root colonization by arbuscular mycorrhizae near rock than on flat sites and those occupied by Polygonum. In all sites, willow (Salix reinii ) was heavily ectomycorrhizal. These data suggest that the models proposed by Allen and Allen (1990) are not only dependent on environmental factors but are also plant species-dependent. Trappe and Maser (1976) showed that spores of the arbuscular mycorrhizal fungus Glomus macrocarpus and the hypogeous ectomycorrhizal fungus Hymenogaster were dispersed by small mammals, such as the Oregon vole, Microtus oregoni, and the chickaree, Tamiasciurus douglasi. A proportion of the spores survived passage through the gut of the animals and assisted in the colonization of bare ground by primary colonizing plant species by providing mycorrhizal inoculm (Trappe, 1988). Similarly, Kotter and Farentinos (1984a,b) showed that a variety of ectomycorrhizal fungal spores could survive passage through the gut of the tassel-eared squirrel, Scurius aberti, and develop mycorrhizal associations with ponderosa pine. Cazares and Trappe (1994) showed that mycophagy of both hypogeous and epigeous mycorrhizal fungi results in the deposition of viable spores in feces. In part the local deposition of feces in middens by small mammals may account for the patchy distribution of mycorrhizal 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 of mycorrhizae in regulating plant competition during seral succession. Source: Data from Allen and Allen (1990). Chapter 5246 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. Lyman Glacier forms an inoculum source, allowing colonization of the newly developing soils by early successional and slow-growing tree species (Abies lasiocarpa, Larix lyalii, Tsuga mertensiana, and Salix spp). Jumpponen et al. (1999) identified “safe sites” on this glacier outwash where plant colonization was most likely. These sites consisted of concave surfaces of coarse rocky particles, which were ideal for trapping tree seeds and protecting them from desiccation. It is likely that these sites also formed foci for foraging small mammals, as they were a site of abundant food in the form of seeds. The deposition of mycorrhizal spore-laden feces in these microsites would thus further enhance the survival of germinating tree seedlings. In these harsh environmental conditions, Jumpponen et al. (1998) showed that the dark-septate mycorrhizal fungus Phialocephalia fortinii significantly enhanced growth of lodgepole pine (Pinus contorta ), which is an early colonizer of the glacier forefront, but only in the presence of added nitrogen. Total plant phosphorus, however, was significantly enhanced in the presence of the mycorrhiza with no added nitrogen (Table 5.2). During the succession of plants in this recent glacial till, 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 TABLE 5.2 Effects of Mycorrhizal Colonization on the Growth and Nutrient Content of Lodgepole Pine (Pinus contorta ) Seedlings by the Dark-Septate Fungus Phialocephalala fortinii in the Presence and Absence of Added Organic Matter and Nitrogen to Lyman Glacier 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 ha 21 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 and Population and Community Regulation 247 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. fungi are a stabilizing force in the developing ecosystem and facilitate net carbon fixation into biomass (Ohtonen et al., 1999). The existence of successions of ectomycorrhizal species during primary succession is supported by the findings of Jumpponen et al. (1999; 2002) on the Lyman Glacier forefront. In the different plant succesional stages they identified, they found 68 ectomycorrhizal species belonging to 25 genera, with no single ectomycorrhizal species occurring on all three successional sites. The authors also found that ectomycorrhizal species diversity increased to a maximum where tree canopies started to overlap. This information corresponds to that of other studies (Dighton et al., 1986; Last et al., 1987; Visser, 1995), in which the increase in diversity of ectomycorrhizal fungi at canopy closure may be related to both the relative paucity of available nutrients (phosphoru s) (Dighton and Harrison, 1990) and an increasing proportion of nutrients locked up in organic forms. It has been speculated (Dighton and Mason, 1985) that this increased diversity of mycorrhizal fungi allows the greater expression of mycorrhizal function in order to utilize the mixed available resources of inorganic and organic nutrients. Some degree of validati on of this hypothesi s has come from the study of Conn and Dighton (2000), in which the diversity of ectomycorrhizae growing into different tree litters reflects appropriate enzyme functions in relation to the relative availability of inorganic nutrients. Where phosphorus is immobilized during early stages of leaf litter decomposition, the ectomycorrhizal community of pine tree seedlings contained a greater proportion of acid phosphatase producing mycorrhizal types. The succession of arbuscular mycorrhizal fungi on roots of herbaceous plant species is probably less obvious than that of ectomycorrhizal fungi. We have seen, however, that different species of arbuscular mycorrhizae may have contrasting effects on the performance of the host plant species, thus, as in the ectomycorrhizal scenario above, we may anticipate changes in the arbuscular mycorrhizal community on plants in association with changes in available resources in the environment. Indeed, Hart et al. (2001) propose two hypotheses to explain the examples of successional changes in arbuscular mycorrhizal fungal species. One of these hypotheses suggests that the mycorrhizal fungi are the driving force (drivers); the second suggests that changes in mycorrhizal species are dependent on the plant and environmental conditions and the mycorrhizae are considered “passengers” (Fig. 5.2). The importance of maintaining a continuous mycelial mat of mycorrhizal fungi to encourage rapid development of mycorrhizal associations during colonization has been demonstrated. Amaranthus and Perry (1989) showed that when Douglas fir was planted into partially cleared sites in which mycorrhizal roots are maintained on the roots of the remaining trees, the survival of the newly planted trees was approximately 90%. Where trees were planted into totally cleared areas, the newly planted tree survival after 2 years was only 50%. They Chapter 5248 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. FIGURE 5.2 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 the plant community, whereas in the “driver hypothesis” the mycorrhizae determine the plant species by interspecific differences in colonization and persistence potential of the fungi. Source: From Hart et al. (2001). Fungi and Population and Community Regulation 249 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. attributed the reduction in survival to the lack of a viable communal ectomycorrhizal network into which the new trees could connect. It is probable that 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 they would be able to on their own. This synergistic activity between surviving mature plants and recruits into the ecosystem allows greater ecosystem stability and survival of the same plant species composition of the ecosystem following disturbance. Even saprotrophic fungi can influence plant est ablishment. Inoculation of the seed of the pulp wood tree Gmelina arborea with the fungus Chaetomium bostrychodes 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 in seed stratification or replacement of the scarification process. 5.2 MYCORRHIZAE AND PLANT FITNESS In addition to improving plant growth, the effect of mycorrhizal associations can lead to improvements in overall plant fitness. This improved fitness, if asymmetric, can be a method of providing competitive advantage to those plant species or individuals that respond the most to the effects of mycorrhizal colonization. These highly responsive plants will therefore become more dominant in the community. Examples of improved fitness are scattered in the literature. For example, Sanders et al. (1995) showed that plants with arbuscular mycorrhizae had improved phosphate nutrition. In addition to the enhancement of vegetative growth, which was supported by greater nutrient acquisition, there was a significant increase in flower bud and seed production in mycorrhizal FIGURE 5.3 Effect of seed inoculation with Chaetomium bostrychodes on the germination of Gmelina arborea seeds. Source: Data from Osonubi et al. (1990). Chapter 5250 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. plants. These increases are related to overall plant grow th and lead to greater performance of the plant as a whole rather that just becoming a larger plant. The effects of mycorrhizae on the increase in reproductive potential of plants has been noted by Koide et al. (1988), Stanley et al. (1993), Lewis and Koide (1990), Bryla and Koide (1990), and Koide and Lu (1992), the increased reproductive potential leading 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 theophrasti were significantly larger than offspring of nonmycorrhizal parents, and under high-density conditions, improved even more because of the effects of early self- thinning in the mycorrhizal condition. This advantage was also transferred to the next generation in terms of total seed production (Table 5.3). The influence of mycorrhizae can, however, differ significantly among plant species, and according to Janos (1980) can be a significant factor in determining plant species composition in the tropics. The effect of mycorrhizae on the composition of the plant community they colonize was reviewed by Francis and Read (1994). Many of the examples they cited 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 a continuum of responses from mutualism, with positive mycorrhizal effects to antagonistic, negative effects of mycorrhizae, depending on the host plant species (Table 5.4). Benefits of mycorrhizal colonization of the bluebell (Hyacinthoides non- scripta ) in natural ecosystems have been shown to enhance phosphorous nutrition of the host plant at specific times of the year. Greatest phosphate uptake TABLE 5.3 Plant Fitness Parameters of Abutilon theophrasti Offspring of Mycorrhizal or Nonmycorrhizal Parents Offspring age (days) Fitness parameter Mycorrhizal parent Nonmycorhizal parent 20 Shoot height (cm) 12.5 9.4 Shoot dry mass (g) 61.2 30.9 Leaf number 3.6 3.0 47 Shoot height (cm) 30.6 19.8 Shoot dry mass (g) 521 154 Leaf number 4.4 3.4 94 Survivors per box 59.1 26.6 Seeds per survivor 17.9 10.6 Source: Data from Heppell et al. (1998). Fungi and Population and Community Regulation 251 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. occurred when there was reallocation of nutrients from the resting bulb to rapidly growing above-ground plant parts (Merryweather and Fitter, 1995a). The degree of dependency of bluebell plants on their mycorrhizae appears to increase through age. Young bulbs are phosphate rich and inhabit upper soil layers; however, because of their susceptibility to frost, summer desiccation, and herbivory, the bulbs at greater depth have higher rates of survival. The trade-off for this enhanced survival at depth is a reduction in the availability of soil phosphate at deeper depths; thus the plants supported by deeper bulbs become more dependent upon their mycorrhizal fungi (Merryweather and Fitter, 1995b). In contrast, Sanders and Fitter (1992a) found that the level of arbuscular mycorrhizal colonization of roots of mixed plant assemblages in a natural grassland varied among plant species but not significantly within species over time. They could thus not come to any conclusion about the benefits of mycorrhizal associations. Sanders and Fitter (1992b ) also could not correlate plant phosphorus, heavy metal content, and biomass to the degree of root colonization by mycorrhizal structures. They thus suggest that the influence of mycorrhizae in altering plant fitness may be nonnutritional, but as yet is unspecified. The distribution of fungal species in a mixed community of arbuscular mycorrhizal plant species is not homogenous. Johnson et al. (1992) showed that the arbuscular mycorrhizal community differed among five plant species of a grassland community. In the same way, Eom et al. (2000) show ed that the different species of plants in a tallgrass community have differing arbuscular mycorrhizal fungal associates (Fig. 5.4). This information lends credence to the idea that there are feedbacks between the mycorrhizal fungal associate and TABLE 5.4 Responses of Different Plant Families to Arbuscular Mycorrhizal Infection Showing a Continuum of Responses from Positive at One End to Negative at the Other þ ve 2 ve Mutualism Commensalism Neutralism Antagonism Asteraceae Burmanniaceae Gramineae Boraginaceae Brassicaceae Ericaceae Gentinaceae Caryophyllaceae Chenopodiaceae Fabaceae Monotroaceae Resedaceae Polygonaceae Liliaceae Orchidaceae Scrophulariaceae Pinaceae Triuridaceae Plantaginaceae 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). Chapter 5252 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. [...]... allows the surviving plants to be released from intraspecific competition There thus may be a role for Copyright 2003 by Marcel Dekker, Inc All Rights Reserved 262 Chapter 5 fungal pathogens in determining interplant spacing to minimize competition and increase fitness Interactions between shade and available water levels in the competition between oak and woody shrub species in savanna ecosystems suggests... laccata Phytopthora þ Paxillus involutus Phytopthora þ Hebeloma crustuliniforme Phytopthora þ H sinapizans Source: Data from Branzanti et al (1999) Copyright 2003 by Marcel Dekker, Inc All Rights Reserved Leaf area (cm2) Plant weight (g) 21.3 15. 6 28.1 19 .5 22.0 28.1 9.3 5. 2 9.4 6.1 5. 9 10.2 270 Chapter 5 FIGURE 5. 11 Degree of cylindorcarpon root rot in peach tree seedlings inoculated with the mycorrhizal... carbohydrates in leaves, allowing a greater supply of energy to be made available to the fungus (Table 5. 14) He also suggests that the production of alkaloids is nitrogen-demanding and cites evidence to show that these fungi are capable of altering the nitrogen balance within the host plant in favor of making more Copyright 2003 by Marcel Dekker, Inc All Rights Reserved 278 Chapter 5 FIGURE 5. 15 Relative... growth-staling products on phylloplane fungi In a study of the development of the fungal pathogen Pestalotiopsis funereal on Eucalyptus globules, they found that leaf discs treated with the growth-staling products isolated from the leaf-inhabiting microfungi of E globulus resulted in a significant decrease in the number of fungal pathogens Copyright 2003 by Marcel Dekker, Inc All Rights Reserved 266 Chapter. .. effects are greater in nutrient-poor or droughty conditions, in which the fungus competes with the host plant for limited resources The level of the impact of a pathogen thus may be greater on plants growing in marginal habitats than those in optimal habitats This would certainly alter the competitive abilities of plants growing in marginal conditions This reduction in fitness of a pathogen-infected plant... the endophytic fungi Additionally, these fungi infect seeds where the pericarp is missing or damaged, in such a way that the fungus acts as an antagonist against pathogenic fungi Fitness of the host plant is also enhanced by the presence of endophytes in its seeds Clay (1990) cites a number of examples in which grass seeds were rendered ineffective in germination due to insect damage in the absence... not change under changing environmental conditions In a study of the in uence of elevated carbon dioxide on the rate of grazing of grasses by the fall armyworm Spodoptera frugiperda, Marks and Lincoln (1996) saw an increase in grazing intensity with elevated CO2, but the proportion of plant consumed by the insects was similar to that of plants grown in ambient conditions (Fig 5. 15) Indeed, Clay (1997)... the global movement of invasive plants and fungi are attracting increasing interest from researchers, farmers, and economists (Rossman, 2001) In particular, the rapid evolution of introduced plant pathogens by genetic change, induced by their new environmental conditions, is of great concern in terms of Copyright 2003 by Marcel Dekker, Inc All Rights Reserved 260 Chapter 5 devising potential control... reduces the incidence of insect herbivory (Table 5. 11), grazing by ungulates, and oviposition on the plant by insects TABLE 5. 9 Seedling Shoot Biomass of Paraberlinia bifoliolata When in Contact with or Isolated from the Root and Mycorrhizal System of Different Tropical Tree Species After 8 months Adult tree species Afzelia Brachystegia Paraberlinia Tetraberlinia Seedling shoot biomass in contact with... shown to induce disease resistance to plants (Mandeel and Baker, 1991; Martyn et al., 1991) Most of these studies, however, have been conducted in agricultural settings or in artificial conditions; the importance of these interactions in natural ecosystems and their in uence on plant fitness is largely unknown 5. 5 MYCORRHIZAL– PATHOGEN INTERACTIONS Mycorrhizal fungi have been known to be effective in the . Dekker, Inc. All Rights Reserved. fungal pathogens in determining interplant spacing to minimize competition and increase fitness. Interactions between shade and available water levels in the competition. area predict increasing rainfall in these regions, which would result in a potential increase in the rate of spread of the disease. Brasier (1996), however, suggests that the severity of cold winters in. and indirect effects of fungi can both cause changes in populations of organisms and alter community composition. The interactions considered in this chapter are summarized in Table 5. 1. 5. 1