FUNGI IN ECOSYSTEM PROCESSES - CHAPTER 7 (end) pot

7 Synopsis and Outlook to the Future 7.1 INTRODUCTION Previous chapters in this book have gone into some detail about the role that fungi play in specific ecosystems and in ecosystem processes in general. In Chap. 6 we encountered a number of anthropogenic impacts on ecosystems and saw how they have affected the fungal community and also how the fungi have been instrumental in moderating the effects of the perturbations on other organisms and processes. The intent of this final chapter is to step back and take a much broader and to some extent more philosophical and conceptual approach to the detail that has come before. In this chapter I will outline some areas that I believe warrant further investigation. In recent years a large number of sophisticated techniques have become available to researchers. Many of these techniques have been devised for other areas of research and have been adopted by mycologists. Because of this, we currently see from the number of articles appearing in the mycological journals a movement away from the traditional observation and ecological approach to the subject, toward detailed physiological studies and molecular-based taxonomy. This is probably a necessary evolution of our communal thought processes and I think in the near future we will see a better integration of these new tools to address some of the broader, ecosystemwide questions. My feeling is that a number of these new techniques are highly relevant to the understanding of the role of fungi in ecosystem processes, but the application of the methods to this end is far from complete. In particular, when we are discussing the role of fungi in ecosystem processes, there are orders of magnitude of difference in the scale at which an individual fungal hyphum operates and at which the processes are Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. manifest in the ecosystem. The ability to measure and understand the processes at the microscale of resolution and then to translate them to the larger scale at which plant and larger animal communities operate is one of the big challenges of the future (Friese et al., 1997; Schimel and Gulledge, 1998). Friese et al. (1997) provide us with a conceptual framework on which we can start to effect the translation of information from the microscale to the ecosystem level of the impacts of fungi (Fig. 7.1). It is here that new methods, such as remote sensing and GIS (geographic information systems), will allow us to identify fungal effects and superimpose data and information on many levels (scales). This will assist our efforts to determine the magnitude of hyphal-scale events at landscape levels (Oudemans et al., 1998). 7.2 THE ECOSYSTEM In a recent article, Pickett and Cadenasso (2002) discussed their ideas of what we think about the concept of an ecosystem. They started their discussion with the basic definition of Tansley, which states that an ecosystem consists of an assemblage of organisms (the biotic component) and the associated physical FIGURE 7.1 Concepts of hierarchy and scale in ecosystems. The relationship between scales (indicated by double-headed arrows) is important in assessing the impact of function at a lower scale on the processes at higher scales. Source: From Friese et al. (1997). Chapter 7392 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. environment in which the organisms live. They further suggest that the interaction among the component parts of an ecosystem, both among the organisms and between the organisms and the physical environment, is another important aspect of the ecosystem. These interactions provide a hierarchical structure through which material (energy and nutrients) flow. They further show that the evolution of the use of the term ecosystem incorporated the idea that ecosystems are scale-independent and are dynamic in nature (meaning that they are not static), and changes in time reflect changes in the complexity and degrees of divergence from equilibrium or stability. As an ecosystem consists of component parts that are important in the movement of materials within the ecosystem, the system is ideally suited to modeling. These models are similar to the way that an industrial process can be simplified to supply and demand functions that are rate-limiting steps governing the rate of a process—the production of an end product. As Pickett and Cadenasso (2002) readily point out, however, the complexity of ecosystems is not as easily modeled, and indeed, many models may need to be developed to understand each of a variety of complex processes that occur simultaneously in the ecosystem. The level of sophistication of the model used depends of the nature of the question being asked, and may vary from a simple word model to a complex mathematical model that attempts to incorporate as many variables as possible. A complex model will need to identify and understand the contribution of each organism and abiotic component to the process being studied. Understanding the intermediate level of organization of an ecosystem by grouping organisms into functional groups or guilds may also provide a holistic understanding of the system without knowledge of the details of each contributing entity, however. This is referred to as an “averaging engine” by Andre ´ n et al. (1999), and for a process modeler, requires only knowledge about the values of the stocks and fluxes between stocks within the ecosystem (Fig. 7.2). It is the complexity of the interaction between component organisms in an ecosystem, however, and the interaction of the organisms with changing environmental conditions that leads to the evolution of diversity of organisms. As we become increasingly aware of the effects that humans have on environmental conditions, we become increasingly aware of the diversity of the organisms within ecosystems, their potential fragility, and the possible consequences of their loss (Tilman, 2000; Adams and Wall, 2000; Schwartz et al., 2000; Wolters et al., 2000). There is a philosophy that in order to understand how an ecosystem works it should be “kicked” and the nature of the response of the ecosystem processes and organisms will give an indication of the controls and feedbacks in the system and what major organisms effect these controls. Wolters et al. (2000) discuss the variable responses of different groups of organisms in soil to global warming. Not all organisms respond to the same degree or even in the same direction, thus to be able to understand what it is that determines the overall Synopsis and Outlook 393 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. FIGURE 7.2 An ecosystem as seen from the point of view of a modeler. Here only the components of a system are necessary for explaining processes. Dots represent real or imaginary organisms. The large upward arrow represents the average activity value for all organisms in the ecosystem. Arrows from species indicate the contribution of each species to the whole ecosystem activity and represents functional groups, enzyme activity, etc. External environmental forces are represented by the box and arrow on the right. Source: Modified from Andre ´ n et al. (1999). Chapter 7394 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. response of an ecosystem, it is often useful to understand the role of individual organisms or functional groups. It is for this reason that we are attempting to understand the role of fungi in ecosystem processes. As was stated earlier in this book, however, we have limited knowledge of the taxonomic diversity of fungi in ecosystems and even less understanding of the physiology of these organisms. To give an idea of the magnitude of the problem that faces mycologists, Hawksworth (1991) estimates that we may have 3 million species of fungi on planet Earth. In their search for fungal species in tropical ecosystems for potential pharmaceutical use, Bills and Polishook (1994) made a total of 1709 fungal isolates from samples of leaf litter collected from four sites in Costa Rica. The number of isolates per sample ranged from 281 to 599, equivalent to 78 to 134 species per sample. Using rarefaction statistics, they determined that the number of species isolated per sample was considerably higher than was predicted from a random subsample of 200 isolates from each sample (Table 7.1). What is the importance of this level of diversity of fungi in the ecosystem? It is logical to think that each fungal species had a unique function. In their analysis of 40 data sets that related ecosystem function to the diversity of organisms within the ecosystem, however, Schwartz et al. (2000) suggested that the majority of studies showed a Type B relationship between diversity and ecosystem function rather than a Type A response. A Type A response (Fig. 7.3) is one in which ecosystem function continues to increase as diversity increases. In a Type B response, however, the function within the ecosystem reaches a maximum before the maximum species diversity is attained (a saturation response). In this condition, it is thought that there is duplicity of function within the members of the community, and functional redundancy occurs. In the case of a Type B response, a loss of diversity is inconsequential to the function unless diversity is reduced below a threshold level or until a “keystone species” is removed (Paine, 1966). Schwartz et al. (2000) say that the response of different ecosystem functions TABLE 7.1 Total Number of Fungal Species Isolated from Leaf Litter at Four Sites in Costa Rica in Relation to the Expected Number of Species as Determined by Rarefaction Analysis Site code Total number of fungal species Expected number of fungal species OS56 134 84 OS83 81 46 OS133 78 47 OS136 93 75 Source: Data from Bills and Polishook (1994). Synopsis and Outlook 395 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. may vary in relation to a change of diversity of a functional group of organisms. They cite the results of van der Heijden et al. (1998), in which plant shoot biomass saturated at approximately 50% of the diversity of arbuscular mycorrhizae added to the roots of an old field plant community (a Type B response), whereas root biomass continued to increase as mycorrhizal diversity increased (a Type A response). At issue, however, is how representative shoot and root biomass are indicative ecosystem processes. A more global ecosystem function that could have been measured, however, would have been net primary productivity. In terms of ecosystem component s being organized in a hierarchical structure, O’Neill et al. (1991) have shown that with respect to the organization of communities of individual organisms, the levels at which different processes occur can be used to dissect out the functional contribution of individual species or groups of species. Using hierarchy theory, they maintain, hypothesis generation can be more accurately achieved. Within ecosystems, organisms of a variety of sizes coexist. We normally identify ecosystems by macroplant community assemblages, but the processes occurring in ecosystems are frequently modified by much smaller organisms. For example, decomposition and nutrient mineralization are carried out by bacteria, fungi, and micro- and mesoarthropods. The immediate effect of any one of these organisms is at the microscale of resolution; however, the combined effects of these organisms are seen at the local, landscape, and whole ecosystem level. One of the most challenging tasks that we face is to create the ability to seamlessly transcend the scales of resolution and convert the processes we observe and measure at one scale to that of the next level up or down. Ecologists thus have taken either a top- down or bottom-up approach to try to understand the complexities of interactions between scales (Parmelee, 1995; Friese et al., 1997; Anderson, 2000). Recently, FIGURE 7.3 Hypothetical relationships between biodiversity and ecosystem function. Type A response shows a continued increase in ecosystem function as diversity increases. Type B response shows saturation of the ecosystem response before maximal species diversity is attained. Source: Adapted from Schwartz et al. (2000). Chapter 7396 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. the idea of reducing ecosystem complexity to its minimum (microcosm approach) has been aided by the development of “mesocosms” (Odum, 1984), in which the degree of complexity of a controlled and contrived ecosystem becomes more analogous to the real world. Here the number of organisms in the ecosystem is relatively large, and complex interspecific interactions are allowed to develop. Concomitant with this comes a lack of control of changes in the ecosystem, but a more realistic set of dynamics is allowed to develop (Anderson, 1995; Lawton and Jones, 1995). Studying the processes occurring in microcosms, in which almost complete control of the system can be maintained, provides us with limited information. The use of mesocosms that are a nearer facsimile of the “real world” allows us to better understand interactions between organisms and their environment and the functional significance of these interactions. Increasing the complexity of the study system in this way allows us to increase in the functional diversity of the component organisms and to better predict the rate determining factors of environmental processes. As fungal hyphae act at the micrometer scale of resolution, their species and community effects may extend to the scale of meter and tens of meters, and there is much more use that can be made of studies of the same process at multiple levels of scale. 7.3 THE FUNGAL ORGANISM The evolution of fungi in terrestrial ecosystems is still unclear. It is hypothesized that fungi were around in marine and aquatic ecosystems before plant emergence onto land; however, the fossil record for fungi is almost completely absent. It is only when plants emerged onto land that the fossil record of fungi was first noted, and here only where fungi were associated with plants and hence appeared in the plant fossils. Kidston and Lang (1921) documented the occurrence of fungi in primitive land plants, Rh ynia and Asteroxylon, in the Silurian. The association between the fungal structures with plant has been interpreted by Pirozynski and Malloch (1975) as being a primitive mycorrhizal association. According to their hypothesis, it appears that land plants only evolved in conjunction with a mycorrhizal fungal partner. The detail of the pictures and descriptions in the original Kidston and Lang (1921) publication leave much doubt as to the actual function of the fungal/plant association seen, however. Are these fungi pathogens? Are these fungi endophytes other than mycorrhizae? How much of the plant kingdom not preserved in the fossil record had emerged onto land prior to Rhynia and Asteroxylon and were being decomposed by saprotrophic fungi? Were the plant fragments seen by Kidston and Lang actually dead and being colonized by saprotrophic fungi? Whatever the outcome of this debate, it is clear that fungi have a variety of functional groups and their associations with plants, and, presumably animals, have an ancient origin. Synopsis and Outlook 397 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. As we have seen from the previous chapters, fungi constitute an important component of the ecosystem. Fungi have been found in all the major ecosystems of the world and have been seen to play a large variety of roles. We have seen how fungi may be important in soil formation, soil fertility, decomposition, primary production, secondary production, and population regulation, and how they may influence plant community composition. The processes that are mediated by fungi are mediated by environmental conditions. An example of this is the influence of C:N and lignin:N ratios within plant residues (Melillo et al., 1982). This has been a dominant concept in the understanding of fungal succession and function during leaf litter decomposition and the rates of nutrient immobilization and mineralization (Frankland, 1992; 1998; Conn and Dighton, 2000). The changes in resources of the leaf litter during decomposition and the changes in fungal assemblages that effect the decomposition results in heterogeneity of resources and species assemblages in space and time (Morris and Boerner, 1999; Morris, 1999). Miller (1995) reviewed the relationship between taxonomic fungal diversity and function. In his review he lists some 21 ecosystem functions carried out by fungi (Table 7.2). He suggests, however, that we do not always have adequate tools and expertise to link these two factors together. There are two aspects of diversity within fungi that require discussion. First, genetic diversity is important, as different fungal species may have different physiological traits. It is because of this fact that we see fungal successions on decomposing resources (Frankland, 1992; 1998; Ponge, 1990; 1991). As we saw earlier these resource successions occur where different fungal species have different enzyme capacities and thus are capable of using different components of the initial resource. At any one time, if a fungus does not possess the enzyme suite allowing resource utilization, this fungus is at a competitive disadvantage and is likely to be replaced by a species with the requisite enzyme competence. Fungi exist as a variety of functional groups (Miller, 1995), and are associated with a range of plant and animal species. They occur in a variety of environments, ranging from eutrophic agricultural and forest ecosystems, to highly oligotrophic systems in which they utilize silicon compounds as an energy source (Wainwright et al., 1997) (Fig. 7.4), to cold oligotrophic conditions in the high Arctic (Bergero et al., 1999), to man- made extreme environments, such as the former reactor room at Chernobyl, in which high levels of radiation have existed for a number of years (Zhdanova et al., 2000). Due to the number of associations between fungi and other organims, it is therefore not surprising that Hawksworth (1991) comes to estimate the potential diversity of fungi at 3 million. He came to this figure by extrapolating the number of fungi known in the United Kingdom as a percentage of the world, adding in the ratio of fungals plant associations with the predictions of the number of new plants yet to be discovered, and Chapter 7398 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. then doing the same for the number of insects likely to be found in the future (Table 7.3). Even at the more conservative estimate of 1.5 million fungal (Hawksworth, 2001) species (ignoring potential new insect species being found), Hawksworth points out that we now know about 4.6% of the fungi that could exist. “Where are the missing fungi?” asks Hyde (2001a,b). This question has triggered recent surveys to find the missing fungi in a variety of ecosystems and functional groups (Sipman and Aptroot, 2001; Watling, 2001; Zhou and Hyde, 2001; Yanna and Hyde, 2001; Dulymamode et al., 2001; Taylor, 2001; Wong and Hyde, 2001; Ho et al., 2001; Arnold, 2001; Photita et al., 2001). As fungi are nondiscrete organisms, however, they exhibit a considerable degree of phenotypic plasticity. Such plasticity exhibited by an individual fungus TABLE 7.2 Ecosystem Functions Performed by Fungi Physiological and metabolic Decomposition of organic matter, volatilization of C, H, and O Mineralization of N, P, K, S, etc. Immobilization of nutrient elements Accumulation of toxic metals Synthesis of humic materials Ecological Energy exchange between below- and above-ground system Alteration of niche development Regulation of successional trajectory and velocity Mediative and integrative Transport of elements and water from soil to plant roots Interplant movement of nutrients and carbon Regulation of water and ion movement through plants Regulation of photosynthesis Regulation of below-ground C allocation Seedling survival Protection of roots from pathogens Modify soil aggregate formation and soil permeability Modify soil ion exchange and water-holding capacity Detoxification of soils Contribution to food webs Development of parasitic and mutualistic symbioses Production of secondary metabolites Source: As presented by Miller (1995). Synopsis and Outlook 399 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. FIGURE 7.4 Effects of various silicon substrates added to Czapek Dox medium on the yield of mycelium of Aspergillus oryzae. Source: Data from Wainwright et al. (1997). TABLE 7.3 Estimates of the Total Number of Fungi in the World Estimate Basis Total number of species A British Isles 1,620,000 B U.S. plants and plant products 270,000 C Biological flora of British Isles 1,539,000 D Alpine sedge community 1,620,000 E Mean of above 1,262,250 F Unstudied substrates 1,650,000 G Anamorphs = teleomorphs 1,504,800 H Assuming 30 million insects 3,004,800 Note: Predictions are made from the number of fungi already known (A), modified by the average number of fungi known to associate with plants (B), this value extrapolated for A using the plant species in the British Isles (C), modified for a figure from alpine communities (D), and then all these values are averaged (E). Conversions and extrapolations F to H are based on predicted unknown substrates for fungi yet to be discovered, the fact that some anamorphs and teleomorphs will be found to be the same species, and extrapolating to the potential number of insects yet to be discovered that will bear fungi. Source: Data from Hawksworth (1991). Chapter 7400 Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved. [...]... fungal mycelia in the ecosystem help in maintaining ecosystem stability? 7. 6 FUNGI IN ECOSYSTEM PROCESSES: WHAT NEXT? We have seen that we need further understanding of the physiology and function of individual species of fungi We have seen too that although we are developing tools for the rapid identification of fungal species, we need to be able to do this in mixed-species assemblages in a quantitative,... stability or moving the system to a different state of equilibrium One way in which to gain insight into the role of fungi in ecosystem processes is thus to investigate fungal communities and their function in disturbed ecosystem In Chap 6, I have thus selected a few examples of perturbed ecosystems, particularly in relation to pollution and climate change We find that in these altered ecosystems, fungi are... long way since Harley (1 971 ) gave his opinion on the role of fungi in ecosystems With the new ecological, physiological, and remote sensing tools that are available to us today, I believe that our understanding of the role of these inconspicuous organisms in ecosystem processes could be enhanced at a more rapid rate than that between 1 971 and now We are aware that fungi do not work alone in the ecosystem, ... terrestrial ecosystems Their importance in aquatic and marine ecosystems is perhaps less strong, but I do not believe that these ecosystems have been thoroughly studied from a fungal perspective I hope that each chapter in this book has suggested some of the ways in which fungi are important, either as fungi alone or in their multifarious interactions with other organisms, in the processes of establishing... intervention (Marx, 1 975 ; 1980; Denny and Wilkins, 19 87; Denny and Ridge, 1995; Leyval et al., 19 97) Saprotrophic fungi are capable of changing the chemical state of some heavy metals to make them more or less toxic to other organisms in the ecosystem (Byrne, 1995; Slejkovec et al., 19 97; Morley et al., 1996; Fischer et al., 1995) The fact that fungi are capable of surviving and, indeed, thriving in. .. L (19 87) Chestnut blight: The classical problem of an introduced pathogen Mycologia 79 :23 – 37 Anderson, J M (1995) Soil organisms as engineers: Microsite modulation of macroscale processes In: Jones, C G., Lawton, J H., eds Linking Species and Ecosystems New York: Chapman & Hall, pp 94– 106 Anderson, J M (2000) Food web functioning and ecosystem processes: problems and perception of scaling In: Coleman,... Dekker, Inc All Rights Reserved Synopsis and Outlook 405 7. 5 PERTURBATIONS One of the ways in which we can understand the functioning of ecosystems, the processes that occur within them, and particularly the feedback mechanisms that regulate processes and maintain stability is to “kick” the system By effecting a perturbation, it is possible to see and measure the processes that are active in returning... our understanding of the role of fungi in ecosystem processes 7. 4 THE FUNGAL COMMUNITY How much do we know about assemblages of fungi? We have seen in earlier chapters of this book that there is replacement of fungal species by others during the colonization and utilization of specific resources in the environment Such Copyright 2003 by Marcel Dekker, Inc All Rights Reserved 404 Chapter 7 successions... disturbing in uence as other organisms, but there are examples in which the physiological plasticity of fungi allow them not only to persist, but to play a major role in returning the ecosystem back to balance For example, in the presence of heavy metal pollution, we have seen that some fungi are capable of immobilizing planttoxic heavy metals into fungal biomass (Byrne et al., 1 979 ; 19 97) In the mycorrhizal... much less in the arbuscular mycorrhizal association (Smith and Read, 19 97) ? Along with the concept of functional redundancy is the possibility of some organisms being “keystone” species (Paine, 1966) Are there examples of fungi acting as keystone species, in which their absence in the ecosystem leads to a significant decline in ecosystem properties? There are examples in which the presence of a single species . in the ecosystem help in maintaining ecosystem stability? 7. 6 FUNGI IN ECOSYSTEM PROCESSES: WHAT NEXT? We have seen that we need further understanding of the physiology and function of individual. 7 Synopsis and Outlook to the Future 7. 1 INTRODUCTION Previous chapters in this book have gone into some detail about the role that fungi play in specific ecosystems and in ecosystem processes. understanding of the role of fungi in ecosystem processes, but the application of the methods to this end is far from complete. In particular, when we are discussing the role of fungi in ecosystem processes,