FUNGI IN ECOSYSTEM PROCESSES - CHAPTER 7 (end) pot

In particular, when we are discussing the role of fungi inecosystem processes, there are orders of magnitude of difference in the scale atwhich an individual fungal hyphum operates and a

In recent years a large number of sophisticated techniques have becomeavailable to researchers Many of these techniques have been devised for otherareas of research and have been adopted by mycologists Because of this, wecurrently see from the number of articles appearing in the mycological journals amovement away from the traditional observation and ecological approach to thesubject, toward detailed physiological studies and molecular-based taxonomy.This is probably a necessary evolution of our communal thought processes and Ithink in the near future we will see a better integration of these new tools toaddress some of the broader, ecosystemwide questions My feeling is that anumber of these new techniques are highly relevant to the understanding of therole of fungi in ecosystem processes, but the application of the methods to thisend is far from complete In particular, when we are discussing the role of fungi inecosystem processes, there are orders of magnitude of difference in the scale atwhich an individual fungal hyphum operates and at which the processes are

manifest in the ecosystem The ability to measure and understand the processes atthe microscale of resolution and then to translate them to the larger scale at whichplant and larger animal communities operate is one of the big challenges of thefuture (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 thetranslation of information from the microscale to the ecosystem level of theimpacts of fungi (Fig 7.1) It is here that new methods, such as remote sensingand GIS (geographic information systems), will allow us to identify fungaleffects and superimpose data and information on many levels (scales) This willassist our efforts to determine the magnitude of hyphal-scale events at landscapelevels (Oudemans et al., 1998).

In a recent article, Pickett and Cadenasso (2002) discussed their ideas of what wethink about the concept of an ecosystem They started their discussion withthe basic definition of Tansley, which states that an ecosystem consists of anassemblage of organisms (the biotic component) and the associated physical

FIGURE7.1 Concepts of hierarchy and scale in ecosystems The relationship betweenscales (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)

environment in which the organisms live They further suggest that theinteraction among the component parts of an ecosystem, both among theorganisms and between the organisms and the physical environment, is anotherimportant aspect of the ecosystem These interactions provide a hierarchicalstructure through which material (energy and nutrients) flow They further showthat the evolution of the use of the term ecosystem incorporated the idea thatecosystems are scale-independent and are dynamic in nature (meaning that theyare 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 themovement of materials within the ecosystem, the system is ideally suited tomodeling These models are similar to the way that an industrial process can besimplified to supply and demand functions that are rate-limiting steps governingthe rate of a process—the production of an end product As Pickett andCadenasso (2002) readily point out, however, the complexity of ecosystems is not

as easily modeled, and indeed, many models may need to be developed tounderstand each of a variety of complex processes that occur simultaneously inthe ecosystem The level of sophistication of the model used depends of thenature of the question being asked, and may vary from a simple word model to acomplex mathematical model that attempts to incorporate as many variables aspossible 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 bygrouping organisms into functional groups or guilds may also provide a holisticunderstanding of the system without knowledge of the details of eachcontributing entity, however This is referred to as an “averaging engine” byAndre´n et al (1999), and for a process modeler, requires only knowledge aboutthe 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 anecosystem, however, and the interaction of the organisms with changingenvironmental conditions that leads to the evolution of diversity of organisms As

we become increasingly aware of the effects that humans have on environmentalconditions, we become increasingly aware of the diversity of the organismswithin ecosystems, their potential fragility, and the possible consequences oftheir 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 ecosystemworks it should be “kicked” and the nature of the response of the ecosystemprocesses and organisms will give an indication of the controls and feedbacks inthe system and what major organisms effect these controls Wolters et al (2000)discuss the variable responses of different groups of organisms in soil to globalwarming Not all organisms respond to the same degree or even in the samedirection, thus to be able to understand what it is that determines the overall

FIGURE7.2 An ecosystem as seen from the point of view of a modeler Here only the components of a system arenecessary for explaining processes Dots represent real or imaginary organisms The large upward arrow represents theaverage activity value for all organisms in the ecosystem Arrows from species indicate the contribution of each species tothe whole ecosystem activity and represents functional groups, enzyme activity, etc External environmental forces arerepresented by the box and arrow on the right Source: Modified from Andre´n et al (1999).

response of an ecosystem, it is often useful to understand the role of individualorganisms or functional groups.

It is for this reason that we are attempting to understand the role of fungi inecosystem processes As was stated earlier in this book, however, we have limitedknowledge of the taxonomic diversity of fungi in ecosystems and even lessunderstanding of the physiology of these organisms To give an idea of themagnitude of the problem that faces mycologists, Hawksworth (1991) estimatesthat we may have 3 million species of fungi on planet Earth In their search forfungal species in tropical ecosystems for potential pharmaceutical use, Bills andPolishook (1994) made a total of 1709 fungal isolates from samples of leaf littercollected from four sites in Costa Rica The number of isolates per sample rangedfrom 281 to 599, equivalent to 78 to 134 species per sample Using rarefactionstatistics, they determined that the number of species isolated per sample wasconsiderably higher than was predicted from a random subsample of 200 isolatesfrom 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 withinthe ecosystem, however, Schwartz et al (2000) suggested that the majority ofstudies showed a Type B relationship between diversity and ecosystem functionrather than a Type A response A Type A response(Fig 7.3) is one in whichecosystem function continues to increase as diversity increases In a Type Bresponse, however, the function within the ecosystem reaches a maximum beforethe maximum species diversity is attained (a saturation response) In thiscondition, it is thought that there is duplicity of function within the members of thecommunity, and functional redundancy occurs In the case of a Type B response, aloss of diversity is inconsequential to the function unless diversity is reducedbelow a threshold level or until a “keystone species” is removed (Paine, 1966).Schwartz et al (2000) say that the response of different ecosystem functions

TABLE7.1 Total Number of Fungal Species Isolated from LeafLitter at Four Sites in Costa Rica in Relation to the ExpectedNumber of Species as Determined by Rarefaction Analysis

Site code

Total number offungal species

Expected number offungal species

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 biomasssaturated at approximately 50% of the diversity of arbuscular mycorrhizae added

to the roots of an old field plant community (a Type B response), whereas rootbiomass continued to increase as mycorrhizal diversity increased (a Type Aresponse) At issue, however, is how representative shoot and root biomass areindicative ecosystem processes A more global ecosystem function that could havebeen measured, however, would have been net primary productivity

In terms of ecosystem components being organized in a hierarchicalstructure, O’Neill et al (1991) have shown that with respect to the organization ofcommunities of individual organisms, the levels at which different processesoccur can be used to dissect out the functional contribution of individual species

or groups of species Using hierarchy theory, they maintain, hypothesisgeneration can be more accurately achieved Within ecosystems, organisms of avariety of sizes coexist We normally identify ecosystems by macroplantcommunity assemblages, but the processes occurring in ecosystems arefrequently modified by much smaller organisms For example, decompositionand nutrient mineralization are carried out by bacteria, fungi, and micro- andmesoarthropods The immediate effect of any one of these organisms is at themicroscale of resolution; however, the combined effects of these organisms areseen at the local, landscape, and whole ecosystem level One of the mostchallenging tasks that we face is to create the ability to seamlessly transcend thescales of resolution and convert the processes we observe and measure at onescale 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 interactionsbetween scales (Parmelee, 1995; Friese et al., 1997; Anderson, 2000) Recently,

FIGURE7.3 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 speciesdiversity is attained Source: Adapted from Schwartz et al (2000)

the idea of reducing ecosystem complexity to its minimum (microcosmapproach) has been aided by the development of “mesocosms” (Odum, 1984), inwhich the degree of complexity of a controlled and contrived ecosystem becomesmore 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 amore realistic set of dynamics is allowed to develop (Anderson, 1995; Lawtonand Jones, 1995) Studying the processes occurring in microcosms, in whichalmost complete control of the system can be maintained, provides us withlimited information The use of mesocosms that are a nearer facsimile of the “realworld” allows us to better understand interactions between organisms and theirenvironment and the functional significance of these interactions Increasing thecomplexity of the study system in this way allows us to increase in the functionaldiversity of the component organisms and to better predict the rate determiningfactors of environmental processes As fungal hyphae act at the micrometer scale

of resolution, their species and community effects may extend to the scale ofmeter 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

The evolution of fungi in terrestrial ecosystems is still unclear It is hypothesizedthat fungi were around in marine and aquatic ecosystems before plant emergenceonto land; however, the fossil record for fungi is almost completely absent It isonly 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 theplant fossils Kidston and Lang (1921) documented the occurrence of fungi inprimitive land plants, Rhynia and Asteroxylon, in the Silurian The associationbetween the fungal structures with plant has been interpreted by Pirozynski andMalloch (1975) as being a primitive mycorrhizal association According to theirhypothesis, it appears that land plants only evolved in conjunction with amycorrhizal fungal partner The detail of the pictures and descriptions in theoriginal Kidston and Lang (1921) publication leave much doubt as to the actualfunction of the fungal/plant association seen, however Are these fungipathogens? Are these fungi endophytes other than mycorrhizae? How much ofthe 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 beingcolonized by saprotrophic fungi? Whatever the outcome of this debate, it is clearthat fungi have a variety of functional groups and their associations with plants,and, presumably animals, have an ancient origin

As we have seen from the previous chapters, fungi constitute an importantcomponent 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 seenhow fungi may be important in soil formation, soil fertility, decomposition,primary production, secondary production, and population regulation, and howthey may influence plant community composition The processes that aremediated 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 fungalsuccession and function during leaf litter decomposition and the rates of nutrientimmobilization and mineralization (Frankland, 1992; 1998; Conn and Dighton,2000) The changes in resources of the leaf litter during decomposition and thechanges in fungal assemblages that effect the decomposition results inheterogeneity of resources and species assemblages in space and time (Morrisand Boerner, 1999; Morris, 1999) Miller (1995) reviewed the relationshipbetween taxonomic fungal diversity and function In his review he lists some 21ecosystem 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 factorstogether

There are two aspects of diversity within fungi that require discussion.First, genetic diversity is important, as different fungal species may havedifferent physiological traits It is because of this fact that we see fungalsuccessions on decomposing resources (Frankland, 1992; 1998; Ponge, 1990;1991) As we saw earlier these resource successions occur where differentfungal species have different enzyme capacities and thus are capable of usingdifferent components of the initial resource At any one time, if a fungus doesnot possess the enzyme suite allowing resource utilization, this fungus is at acompetitive disadvantage and is likely to be replaced by a species with therequisite 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 agriculturaland forest ecosystems, to highly oligotrophic systems in which they utilizesilicon compounds as an energy source (Wainwright et al., 1997)(Fig 7.4), tocold oligotrophic conditions in the high Arctic (Bergero et al., 1999), to man-made extreme environments, such as the former reactor room at Chernobyl, inwhich high levels of radiation have existed for a number of years (Zhdanova

et al., 2000) Due to the number of associations between fungi and otherorganims, it is therefore not surprising that Hawksworth (1991) comes toestimate the potential diversity of fungi at 3 million He came to this figure byextrapolating the number of fungi known in the United Kingdom as

a percentage of the world, adding in the ratio of fungals plant associationswith the predictions of the number of new plants yet to be discovered, and

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 beingfound), Hawksworth points out that we now know about 4.6% of the fungi thatcould exist “Where are the missing fungi?” asks Hyde (2001a,b) Thisquestion has triggered recent surveys to find the missing fungi in a variety ofecosystems 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

Immobilization of nutrient elementsAccumulation of toxic metalsSynthesis of humic materialsEcological Energy exchange between below- and above-ground

systemAlteration of niche developmentRegulation of successional trajectory and velocityMediative and integrative Transport of elements and water from

soil to plant rootsInterplant movement of nutrients and carbonRegulation of water and ion movementthrough plants

Regulation of photosynthesisRegulation of below-ground C allocationSeedling survival

Protection of roots from pathogensModify soil aggregate formation and soilpermeability

Modify soil ion exchange and water-holdingcapacity

Detoxification of soilsContribution to food websDevelopment of parasitic and mutualistic symbiosesProduction of secondary metabolites

Source: As presented by Miller (1995).

FIGURE7.4 Effects of various silicon substrates added to Czapek Dox medium on theyield of mycelium of Aspergillus oryzae Source: Data from Wainwright et al (1997).

TABLE7.3 Estimates of the Total Number of Fungi in the World

B U.S plants and plant products 270,000

C Biological flora of British Isles 1,539,000

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).

can be seen in the response of the thallus of external nutrient conditions Innutrient-poor environments, fungal hyphae adopt a searching strategy, formingfast effuse growth with a low hyphal density On substrates with high nutrientavailability the same fungus adopts a slow, dense pattern of hyphal growth as thehyphae utilize the resources available These patterns of growth are highlydistinctive (Das, 1991; Rayner, 1991; Ritz, 1995), and call for significant changes

in the polarity of the hyphae and alterations of the hyphal-branching pattern AsRayner (1991) points out, these hyphal aggregates possess emergent propertiesthat provide functions of the fungi that cannot be achieved by the hyphalmycelium alone The physiological function of a fungal thallus can therefore bemarkedly different in different parts of the same organism

Differentiation of the thallus into functionally and physiologicallydiverse components (absorptive hyphae, exploratory hyphae, mycelial cordsfor water and nutrient translocation, etc.) permits multifunctionality of thesame individual The concept that “the mycelium of higher fungi is portrayed

as a developmentally versatile collective in which an initially dendriticpattern of branching is converted, by hyphal anastomosis, into acommunication network” (Rayner, 1991) highlights the role of fungi innutrient and energy transport This system of differentiated and specializedmycelia can convey “information” (nutrients and energy) at a faster rate thancan be done via hyphae (Gray et al., 1995; 1996; Wells et al., 1999; Boddy,1999) The ability to have multiple functions within the same individual ismost obvious in higher fungi, and is probably more unusual in fungi thantheir nearest morphological counterparts, clonal plants This ability of fungiprovides them with the ability to exploit patchily distributed resources andwithstand stress The challenges posed by the utilization of heterogeneouslydistributed resources in an environment can either be met by the development

of distinct microbial communities within each patch of resource (Morris andBoerner 1999; Morris, 1999), or particularly in the case of fungi, by theexploitation of all resource islands by the same species and differentiatingphysiological attributes within the same thallus in each of the resourceislands (St John et al., 1983; Andrews, 1992; Cairney, 1992; Rayner, 1991;Boddy, 1999) In either case, there is a need to be able to identify thephysiological functional differences in the communities or the individual inthe different resource units and translate that function to ecosystem-levelprocesses Using an adaptation of the BIOLOG microtitre plate enzymeanalysis system devised for bacterial community functional analysis (Tunlidand White, 1992; Winding, 1994; Dobranic et al 1999) were able toinvestigate the enzyme expression of fungal communities in a variety ofmicrohabitats, providing an index of functional diversity (Zak, 1993).Microscale changes in the carbon substrates of decomposing leaves weremeasured by infrared microspectroscopy (Mascarenhas et al., 2000; Dighton

et al, 2001), by which fungal activity could be measured at the scale seen byfungal hyphae The use of these methods is necessary to the understanding ofthe function of fungi in the ecosystem in order to identify physiologicalactivity at the mycelial level The challenge is to translate the outcome ofthese processes up to higher scales of resolution.

The potential size of fungal individuals in the ecosystem (Smith et al.1992), in which a persistent organism with different functionality linked byconductive connections may cover hectares of forest floor, leads one to regardfungi as true ecosystem engineers (Lawton and Jones, 1995), particularly in therole of plumbers (Rayner, 1998) In this way, we have seen that trees can beconnected below ground by ectomycorrhizal connections among their roots(Amaranthus and Perry, 1994; Read, 1998; Rayner, 1998) With arbuscularmycorrhizal fungi, herbaceous plants can be similarly connected (Heap andNewman, 1980; Newman and Eason, 1989; Eason et al., 1991) This allows themovement of nutrients, energy, and water between plants in relation to changes insource – sink relationships, especially when they are stressed or perturbed Themore recent finding that plants of different species can be connected by theseunderground mycelial networks (Simard et al., 1997 a,b,c) alters our conceptsregarding plant interspecific interactions In contrast to the hypothesis that plantcommunities arise from competition among members of the plant assemblage,

we must now start thinking in terms of the balance between competition andsynergism among plants of different species This ability of fungi to connectseparate parts of the ecosystem together is not restricted to soil In tree canopiesand at the soil surface mycelial cords have been shown to connect dead leavestogether and to effect decomposition (Hedger et al., 1993; Lodge and Asbury,1988)

The fact that there is a large mycelial community of fungi in soil inmany ecosystems is a benefit to both plant populations and communities Ifthe ecosystem suffers some disturbance, the continued presence of amycorrhizal mycelial network enables recruitment of replacement individualsback into the community as they readily form new mycorrhizae that benefitthe host plant growth (Amaranthus and Perry, 1989) and colonization of bareground (Jumpponen et al 1999; 2002) Indeed, Hart et al (2001) suggest that

it is fragmentation of the mycorrhizal hyphal network that facilitates invasion

by exotic species into an existing ecosystem (Fig 7.5) By the possiblesharing of resources among plant species in the community, mycorrhizalfungi are likely to be able to facilitate recruitment of species into the plantcommunity that are able to establish mycorrhizal connections with existingplants and derive carbon and nutrients from them (Simard et al., 1997b,c) Incontrast, the effect of plant pathogens may influence the plant effect on theenvironment, thus enabling community changes to take place (Anderson et al.,2001)

The concept of fungi as being major ecosystem engineers is relatively new.Rayner (1993), however, suggests that fungi are the equivalent to theinfrastructure seen in modern cities He likens fungal networks in forests to thecommunication, power supply, plumbing, and sewage systems of cities Weknow little about the actual extent of foraging of individual fungi, althoughmolecular mapping tools are allowing us to do this with greater precision(Dahlberg and Stenlid, 1994; 1995; de la Bastide et al., 1994) Molecular methodsfor the identification of fungal species have helped us to know who is in theenvironment (Gardes et al., 1991; Horton et al., 1998; Hirsch et al 2000;Pennanen et al., 2001), but we are not yet at the stage when we can easily usethese techniques to tells us how much of each species coexists at any one point inspace and time The development of tools to allow us to do this and to integratethe information on species composition and their function will help us increaseour understanding of the role of fungi in ecosystem processes.

How much do we know about assemblages of fungi? We have seen in earlierchapters of this book that there is replacement of fungal species by others duringthe colonization and utilization of specific resources in the environment Such

FIGURE7.5 A life history framework for arbuscular mycorrhizal invasion success Indisturbed systems, only fungi with high colonization potential will succeed (dashed line).Over time a sustained, intact hyphal system will develop (solid line) with superiorpersistence traits Source: From Hart et al (2001)