FUNGI IN ECOSYSTEM PROCESSES - CHAPTER 3 pot

3 Fungi and Primary Productivity: Plant Growth and Carbon Fixation The role of fungi in primary production goes beyond making nutrients available to plants. There are intimate associations between the photosynthesizing components of the ecosystem and fungi, many of which are symbiotic. Such interactions between fungi and other organisms enhance nutrient availability for primary production and include mycorrhizae and associated rhizospheric microbial communities. In addition, some of these synergistic interactions between plants and fungi are involved in the prevention of plant disease and inhibiting herbivory. The latter is an important trait of endophytes, and has economic importance. In the form of lichens, the whole symbiotic association among fungi, algae, and bacteria is involved in primary production. Here, as we saw in the last chapter, the fungal partner acts as a supportive network for photosynthetically active algae and bacteria. In the mycorrhizal habit, fungi form a close association with plant roots and are physiologically and morphologically adapted to assist in the transport of nutrients into root systems. The diversity of mycorrhizal morphologies, the range of fungal taxa associated with mycorrhizal associations, and their range of degrees of dependency upon the association has led scientists to investigate their biology and ecology for more than 100 years. Indeed, Seta ¨ la ¨ et al. (1998) accumulated evidence to show that the diversity of organisms in soil has significant effects on primary production, especially when the number of trophic levels is low. They also suggest that the inclusion of ectomycorrhizae into the models of diversity and function of forested systems is of fundamental importance in understanding the mechanisms regulating primary production. As endophytes, fungi can be important in defending plants against herbivory, thus indirectly influencing primary productivity by negating or Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. minimizing plant biomass loss through grazing. In addition to these direct effects of fungi on regulation of primary production, fungi are important in regulating the individual fitness of a plant or animals, and thus can influence the standing of individual species within a community and the community composition. These indirect effects will be explored in greater depth in Chap. 5. Table 3.1 shows the ecosystem services promoted by fungi that will be discussed in this chapter. 3.1 THE ROLE OF LICHENS IN PRIMARY PRODUCTION The role of lichens in soil formation was discussed in Chap. 2. The fact that these organisms are able to access mineral nutrients from the dissolution of parent rock material and that the symbiotic bacteria and algae are able to photosynthesize make it logical to assume that lichens can be important components of total primary productivity. The importance of this process to net primary production is most important in a number of ecosystems in which lichens compose a large proportion of the plant biomass. Crustose and foliose soil lichens are major components of the plant biomass in many cold, wet environments, in which vascular plants are less able to survive. Beymer and Klopatek (1991) showed that approximately 28 kg C ha 21 was fixed by the lichen crust community in a pinyon pine and juniper forest in a semiarid environment in the Grand Canyon. Using radioactive tracer techniques, they estimated that approximately 34–36% of this fixed carbon becomes incorporated into soil organic matter. In mat-forming lichens, Crittenden et al. (1994) showed that lichen growth was limited by the availability of nitrogen in oligotrophic environments. They showed significant and positive relationships between nitrogen availability and chitin content (a measure of fungal biomass) of the lichen. Crittenden (1989) reported that there is very little nitrogen available in the substratum on which these lichens grow and that they are very dependent upon intercepting nitrogen in precipitation. The efficiency of nitrogen interception can often be close to 100% (Table 3.2), but at certain times lichens can be a source of leached nitrogen and potassium for other plants. Indeed, this form of nitrogen capture can be equivalent to the N fixation capacity of those lichens containing nitrogen-fixing bacterial phycobionts (Table 3.3). This information suggests that within limits, increased atmospheric N deposition will stimulate growth of lichens in nutrient-poor environments. Growth of mat-forming lichens can be severely limited by the availability of nitrogen. In some cases, as in the soil crust communities, bacteria, in association with lichens and fungi, may fix significant quantities of nitrogen. Belnap (2002) showed that between 1 and 13 kg N ha 21 y 21 could be fixed by crust communities in the deserts of Utah. Terricolous lichen species have been shown to have growth rates of 0.2 to 0.4 g g 21 dry weight (30 to 70 g m 22 )in Chapter 394 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. Sweden (Palmqvist and Sundberg, 2000). These authors also report that epiphytes in the same locality only produce 0.01 to 0.02 g g 21 (1 to 4 g m 22 ). The greater biomass accumulation of ground-inhabiting species is attributed to their better water-holding capacity and greater light levels than arboreal habitats. As epiphytes, lichens are able to successfully utilize the mineral nutrients that are intercepted by or leached from tree canopies and that run down the branches and trunks as stem flow. Again, the combination of fungal sequestration of mineral nutrients and photosynthesis by the symbiotic algae provides another source of carbon fixation in the tree canopy. TABLE 3.1 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 boldface. Fungal groups in parentheses are regarded as of lesser importance in that function. Fungi and Primary Production 95 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. In the Norwegian high arctic, Cooper and Wookey (2001) measured the rate of growth of the fruiticose lichens Cetraria spp., Cladonia spp., and Alectoria nigricans (Fig. 3.1) as between 2.4 and 10.6 mg g 21 per week or between 2.5–11.2% of the original lichen biomass in one season (approximately 10 weeks). Similarly, Peck et al. (2000) showed that the arctic tumbleweed lichen Masonhalea richardsonii increased in biomass by about 10% per year in Alaska. These rates of growth are similar to those reported by Ka ¨ renlampi (1971). These lichens provide a large amount of the winter feed of reindeer, and in the island of Svalbard, may become severely depleted in biomass due to the intense grazing pressure, low rates of growth, and the indirect effect of reindeer trampling on lichen survival. In temperate forest ecosystems, epiphytic lichens can form a significant proportion of the net primary production of the ecosystem. Using tethered arboreal lichens, Sillett et al. (2000) showed that the colonization of experimental branches was highest in clear-cut and old-growth Douglas fir forests and lowest in young (10-year-old, 1.5-m-tall) forests (Fig. 3.2). In general there was improved lichen colonization and growth on rough branches compared to smooth branches, TABLE 3.2 Range of Nutrient Retention by Mat-Forming Lichens from Rainfall Nutrient retention (%) Mat lichen species NO 3 -N NH 4 -N K Stereocaulon paschale 86 –100 40– 99 2 37– þ 90 Cladonia stellaris 62–99 50–97 2978– þ 65 Source: Data from Crittenden (1989). TABLE 3.3 Accumulation and Loss of N in Two Mat-Forming Lichen Species During 82 Days of Growth Stereocaulon paschale Cladonia stellaris Increment in total biomass N 758 95 Inorganic N in rainfall deposited 31 31 Inorganic N in rainfall retained 27 25 N lost as organic N 19 11 N fixation 669 0 Note: Values are expressed as mg N m 22 of pure lichen cover. Source: Data from Crittenden (1989). Chapter 396 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. but this preference was forest-dependent. For the lichen Lobaria oregana there was greater colonization of smooth bark in the clear-cuts, no difference between barks in the young forest, and a significance preference for rough bark in old- growth stands (Fig. 3.3). Differences in growth rate and colonization potential may be related to light levels. In a study of light use efficiency of five macrolichen species, Palmqvist and Sundberg (2000) showed that there was FIGURE 3.1 Relative growth rate of a range of lichen species from the article. Solid bars represent relative growth rate, hatched bars represents the relative growth rate over a 10 week interval. Data from Cooper and Wookey (2001). FIGURE 3.2 Frequency of occurrence of lichens on experimental brances located in clearout, young and old growth stands of Douglas fir forests. Data from Sillett et al. (2000). Fungi and Primary Production 97 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. a significant positive correlation between intercepted irradiance and growth when lichens were wet. They demonstrated that there was a range of between 0.5–2% of the light use efficiency per dry weight at a standard energy equivalent of light between lichens grown in low- and high-light regimes. In tropical ecosystems, the production of lichen biomass is limited by the high rates of dark respiration, leading to a low net rate of carbon accumulation. Lange et al. (2000) determined that within the genus Leptogium between 47–88% of the carbon gained during photosynthesis was lost as respiration, thus limiting productivity (Table 3.4). An important function of the fungal component of lichens is to support and protect the photosynthetic apparatus contained in the prokaryotic symbiont. Solhaug and Gauslaa (1996) showed that by extracting the lichen Xanthoria parietina with 100% acetone they were able to extract the compound parietin without damage to the lichen. At high light intensities, however, it was found that FIGURE 3. 3 Density of the lichen Lobaria oregana colonizing rough or smooth experi- mental branches located in clearcut, young and old growth Douglas fir forest stands. Data from Sillett et al. (2000). TABLE 3.4 Carbon Budget of the Lichen Leptogium spp. in the Panamanian Tropics Lichen species Net photosynthetic gain (mg C (gC) 21 d 21 ) Respiratory carbon loss (mg C (gC) 21 d 21 ) Carbon loss as of carbon gain Leptogium phyllocarpum adult 9.3 2 7.2 77.4 Leptogium phyllocarpon juvenile 15.7 2 7.4 47.1 Leptogium cyanescens 8.97 2 5.4 60.2 Leptogium azureum 6.2 2 5.5 88.7 Source: Data from Lange et al. (2000). Chapter 398 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. extracted lichens showed a reduction in photosynthet ic oxygen production, evidencing damage to the photosynthetic apparatus in the absence of the blue light filtering chemical produced by the fungus, Both the physical support provided by the fungus and its ability to produce beneficial chemicals thus aid the process of primary production in lichens. 3.2 THE ROLE OF MYCORRHIZAE IN PLANT PRIMARY PRODUCTION We saw in Chap. 2 how the saprotrophic fungal community in association with bacteria and soil fauna make mineral nutrients available for plant growth. Similar processes occur in both freshwater and marine ecosystems to provide nutrients for both pelagic and rooted vegetation. In both the terrestrial and, to a more limited extent, in freshwater and estuarine ecosystems, a symbiotic association between mycorrhizal fungi and plant roots influences the uptake of mineral nutrients from the substratum into plants for biomass production. This functional group of fungi have evolved along with their host plants and have a variety of ways in which they interact with both readily and poorly available nutrient resources to enhance plant growth. They are also important in protecting host plants against pathogens. In addition to these factors, these fungi may be more important than previously thought in influencing competition among component plant species of a plant community. This can occur by the fungal influence of host plant fitness and through the sharing of resources between plants of the same or different species within the plant community. The importance of mycorrhizal contribution to primary production in forested ecosystems was shown by Vogt et al. (1982). They showed that although the mycorrhizal fungi contributes only some 1% of total ecosystem biomass, the percentage of net primary production represented by mycorrhizal fungi was 14 –15% (or 45% in young forest stands and 75% in mature stands) when combined with the fine root biomass supporting the mycorrhizal fungal tissue (Vogt et al., 1982). Pankow et al. (1991), however, suggest that the main role of mycorrhizal symbioses is not during the early, productive stages of plant succession in ecosystems, but rather in the protective stage, during which most resources are entrained in plant biomass. Here, they suggest, mycorrhizae control the cycling of nutrients from decomposing organic matter back into plants and reduce the likelihood of nutrient loss from the ecosystem. 3.2.1 The Mycorrhizal Habit Mycorrhizae are symbiotic associations between fungi and plant roots. Their description and function have been detailed in many excellent texts, to which the reader is referred (Harley, 1969; Harley and Smith, 1983; Smith and Read, Fungi and Primary Production 99 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. 1997). The ecology and role of mycorrhizae in ecosystems has also been explored in a variety of texts (Allen, 1991; Read et al., 1992; Varma and Hock, 1995; Mukerji, 1996). In this chapter we will try to take a wider view of the impact of mycorrhizae in the ecosystem without dwelling on the minutiae of physiological and biochemical processes involved in the physiology of the mycorrhizal association. Approximately 95% of all vascular plants have a mycorrhizal association (Brundrett, 1991). Traditionally, mycorrhizal associations have been divided into a range of categories, based on the taxonomy of the fungal associate and the physical form of the interactions between the root and the fungus in the mycorrhizal structures that are produced in the symbiosis. A list of mycorrhizal forms, their plant associates, and the key features of the mycorrhizae is given in Table 3.5. Among the most common types of mycorrhizal association are the arbuscular mycorrhizal types, which are formed mainly by zygomycete fungal species. These fungi are mainly associated with herbaceous vegetation, grasses, and tropical trees, although a limited number of temperate woody plants may also associate with arbuscular mycorrhizae. The association is characterized by fungal penetration within the host root cortical cells and the development of a variously TABLE 3.5 Outline of Some of the Features of Different Types of Mycorrhizal Associations Mycorrhizal type Host plant group Characteristics Fungal associate Arbuscular mycorrhizae Herbaceous plants, grasses; some trees Formation of arbuscules within cortical cells of host root Ectomycorrhizae Coniferous and deciduous trees Formation of a sheath or mantle of fungal tissue around the root surface and a Hartig net of fungal penetration between the cortical cells to the endodermis Basidiomycetes Ascomycetes Ectendomycorrhizae Ericoid mycorrhizae Ericaceaea Hyphal coils within the host root cortical cells Arbutoid mycorrhizae Arbutus Hyphal coils within the host root cortical cells Orchidaceous mycorrhizae Orchids Fungal propagule carried in the seed of the plant Chapter 3100 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. developed, treelike branching of the hyphae between the host cell wall and plasmolemma called an arbuscule. It is here that the surface area of the interface between plant host and fungus is optimized for nutrient and carbohydrate exchange. In some instances, vesicles are formed in some cortical cells. These consist of a swollen hyphum occupying a large volume of the cell. This structure contains storage material, and its name gave rise to the vesicular-arbuscular mycorrhizal type. This name is now reserved for a limited number of associations, mainly with the fungal genus Glomus (Smith and Read, 1997). The arbuscular mycorrhizal association is formed with a large number of plant species and a relative small diversity of fungal species. Because these fungi do not produce large fruiting structures as in the Basidiomycotina, the identification of the fungal partner is by the anatomy of spores, which may be produced within or outside the host root. The ectomycorrhizal habit consists of an association between, mainly, tree species and a range of fungal taxa consisting of basidiomycetes, ascomycetes and some zygomycetes. In this type, the fungus does not penetrate into the host cortical cells, but only between them, forming a Hartig net. The Hartig net exists outside the endodermis of the root. On the surface of the root, a sheath or covering of fungal material develops. This surface structure may be of varying degrees of complexity from a loose weft of hyphae to highly organized pseudoparenchymatous structures. It is the structure of the sheath, degree of branching, (induced by change in cytokinins), and nature of emanating hyphae or hyphal strands that allow morphological identification of these mycorrhizae (Agerer, 1987–1999; Ingleby et al., 1990: Goodman et al., 1996– 2000). Ectomycorrhizal associations are formed between a limited number of plant species and a huge number of fungal species. In addition to ectomycorrhizae, ectendomycorrhizal associations also occur with tree species. These associations have both ectomycorrhizal and arbuscular mycorrhizal structural characteristics (Laiho & Mikola, 1964). Ericoid mycorrhizae are similar in structure to arbuscular mycorrhizae, but are associated solely with members of the ericales (Ericaceae, Empetraceae, Epicaridaceae, Diapensiaceae and Prionotocaceae). All of these groups are sclerophyllous evergreens and reside in habitats where both nitrogen and phosphorus are sparsely available. The root systems of these plants consist of very fine roots containing a single layer of cortical cells, which the mycorrhizal fungi penetrate to form hyphal coils, rather than arbuscules (Read, 1996). The fungi associated with this type of symbiosis are still not completely identified, but consist of a relative few genera, including Hymenoscyphus and Oidiodendron. Closely associated with these mycorrhizae are the arbutoid mycorrhizae. Orchidaceous mycorrhizae are unique in terms of the obligate nature of the association. The importance of the mycorrhizal association for seed germination and the initial establishment of the plant has been reviewed by Zettler and McInnes (1992) and Rasmussen and Wigham (1994). The fungal partner is usually ascribed Fungi and Primary Production 101 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. to the genus Rhizoctonia, and there has been such evolution of the obligatene ss of the association that the fungus is transported in the seed of the plant. Further details of the structure of all mycorrhizal associations can be found in Peterson and Farquhar (1994) and Smith and Read (1997). For the purposes of demonstrating the role in mycorrhizae in ecosystem processes, the following discussions will mainly be limited to the role of arbuscular-, ericoid-, and ectomycorrhizae. 3.2.2 The Basic Function of Mycorrhizae In the previous chapter we saw how fungi are important in a variety of ways in developing the structure of soils and regulating soil fertility by the processes of decomposition and mineralization. The major ecosystem function of mycorrhizae is to assist host plants in the acquisition of mineral nutrients from soil. In the classic elementary texts of plant physiology, the function of nutrient uptake is ascribed to the root hairs, which increase the root surface area to provide the maximal root surface to soil pore-water interface. As we have seen, however, if approximately 95% of plants are mycorrhizal and these mycorrhizal associations alter root morphology, then this picture of nutrient uptake is too simplistic. The ability to assist the host plant in obtaining nutrients has been ascribed to the fact that during mycorrhizal development, root hair development is suppressed and the function of the root hair is replaced by fungal hyphae. These hyphae have two major benefits for sequestering nutrients. They are of smaller diameter than root hairs and can penetrate more easily and to a greater distance from the root into the soil, thus exploring a greater volume of soil and presenting a greater surface area for nutrient absorption than could the root–root hair system alone (Nye and Tinker, 1977; Clarkson, 1985; Hetrick, 1991; Marschner and Dell, 1994). The energetic efficiency results in a better balance betwee n the investment of photosynthate to roots per unit nutrient absorbed (Vogt et al., 1982, Harley and Smith, 1983; Fitter, 1991). Rousseau et al. (1994) showed that for ectomycorrhizal pine seedlings the extraradical mycelium accounted for only 5% of the potential nutrient-absorbing system dry weight (fungi and roots), which represents a small investment in structural carbohydrate. The mycelium accounted for 75% of the potential absorbing area and over 99% of the absorbing length (Table 3.6), however. Similarly, Kabir et al. (1996) showed that mycelium of the arbuscular mycorrhizae colonizing roots of corn (Zea mays ) and barley (Hordeum vulgaris ) accounted for more than 83% of the soil fungal hyphae. The second benefit is that it is energetically more efficient to produce a long, thin hyphum than a root hair. The analysis of this cost-benefit equation for arbuscular mycorrhizae in natural conditions (Fitter, 1991), however, suggests that the nutritional benefit alone is not always worth the investment. Fitter (1991) suggests that the benefit is only realized at specific times in the life cycle of Chapter 3102 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. [...]... (19 93) showed that these mat-forming ectomycorrhizal communities in Douglas fir forests are important in increasingly removing organic nitrogen from the soil pool and immobilizing it into high C:N FIGURE 3. 10 Total phosphorus concentration of soil in the root layer of high density (squares) and low density (trianges) of tropical cesalps, indicating the effect of ectomycorrhizal fungi in maintaining... Proprionic Formic Pyruvic 0.4 0 .3 0 .3 0 .3 4.8 5.1 4 .3 5.9 0.4 0 .3 0.4 0.4 Malic þ Succinic 0 .3 1.4 3. 7 1 .3 Tricarboxylic Tartaric Oxalic Citric Isocitric Aconitic SUM 0.2 0.2 13. 4 0.2 1.7 3. 1 6.2 7.9 1.0 0.5 4.5 3. 8 0.2 0.2 0.2 0.2 0.2 0.2 0.2 0.9 17 .3 11.7 40.8 32 .6 Note: The role of mycorrhizal fungi is not implied, but it is probable that they could be involved in increasing the function of organic... in soil are in the inorganic phase in soil water Arbuscular mycorrhizae dominate under these conditions in temperate grasslands and in tropical forests and grasslands In these ecosystems of herbaceousdominated plant communities, decomposition is rapid and organic matter rapidly becomes incorporated into the soil mineral matrix The nutrient supply for plants is mainly through inorganic nutrients, mineralized... Hebeloma crustuliniforme Lactarius sp Scleroderma citrinum Cenococcum geophilum pNPPase Phytase P source Mycelium Soluble Mycelium Soluble 32 P uptake Pi Po Pi Po Pi Po Pi Po Pi Po Pi Po 1.8 1.1 15.6 18 .3 0.6 0.6 8.2 6 .3 3.7 4.7 0.1 0.7 60.0 45.0 77.4 41.4 4.8 11.0 Nd Nd 1.0 1.0 Nd Nd 55.2 36 .3 83. 8 60.0 2.0 2.7 265.1 198.4 74 .3 2 .3 13. 1 23. 2 0.7 0.4 0 .3 0 .3 0.0 Nd Nd Nd Nd Nd Nd Nd 17.0 5.2 136 .5 4000 —... mechanisms of acquiring both P and Fe from these soils ¨ by the production of organic acids in the rhizosphere (Strom, 1997; Lee, 1999) (Table 3. 14) Part of this ability may be linked to the arbuscular mycorrhizal FIGURE 3. 13 Rate-limiting processes in the uptake of phosphorus by plants and the role of arbusculr mycorrhizae in overcoming these limitations Thin arrows represent flows in the non-mycorrhizal... roots of bluebell increases with age During the ageing process, bluebell bulbs descend further into the soil to zones in which phosphorus becomes increasingly depleted As they do so, the roots become increasingly more colonized by mycorrhizae, and the enhanced phosphorus gained by this association allows the fecundity (measured as bulb diameter) to be maintained (Fig 3. 15) In a continuation of this... rates of mineralization) into the low-quality resource in order to effect more rapid decomposition by lowering the C:N ratio Similarly, in arctic regions, in which decomposition and nutrient mineralization is constrained by low temperatures, Tibbett et al (1998a) suggest that there has been a pre adaptation of Hebeloma Copyright 20 03 by Marcel Dekker, Inc All Rights Reserved 112 Chapter 3 species... arbuscular mycorrhizal fungi in biogeochemical cycling and the maintenance of sustainable plant-soil interactions Arbuscular mycorrhizae ¨ are of particular importance in agriculture (Gianinazzi and Schuepp, 1994), but discussion of these ecosystems is out of the scope of this book, except when specific principles relative to natural ecosystems are discussed Jeffries and Barea (1994) discuss the in uence of arbuscular... could also use bovine serum albumin, none of the mycorrhizal fungi could utilize nitrogen in the form of ethylenediamine or putrescine, suggesting that the ectomycorrhizal fungi could not compete with saprotrophic fungi for resources in decaying animal carcasses Bartlett and Lewis (19 73) demonstrated the production of surface acid phosphatases by beech mycorrhizae and suggested their potential importance.. .Fungi and Primary Production 1 03 TABLE 3. 6 Plant and Fungal Parameters for Pine Tree Seedlings Colonized by the Ectomycorrhizal Fungi Pisolithus tinctorius and Cenococcum geophilum Showing the Enhanced Nutrient Uptake Capacity of the Mycorrhizal Plants Due to Extraradical Hyphal Development Plant/fungal parameter Pisolithus Cenococcum Nonmycorrhizal plant 69.5 477 3. 72 4.02 33 .8 13. 6 47.4 6.42 0 .36 . endophytes, fungi can be important in defending plants against herbivory, thus indirectly in uencing primary productivity by negating or Copyright 20 03 by Marcel Dekker, Inc. All Rights Reserved. minimizing. (1989). TABLE 3. 3 Accumulation and Loss of N in Two Mat-Forming Lichen Species During 82 Days of Growth Stereocaulon paschale Cladonia stellaris Increment in total biomass N 758 95 Inorganic N in rainfall. can in uence the standing of individual species within a community and the community composition. These indirect effects will be explored in greater depth in Chap. 5. Table 3. 1 shows the ecosystem