Chapter 13. Interspecific Interaction Terminology: From Mycology to General Ecology

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Table 13.1 Possible Outcomes from Bilateral Interactions

Effect of Species B on Species A

Effect of A on B



–



0



+



–



–/–

Synnecrosis

–/0

Amensalism

–/+

Predation



0/–

Allolimy

0/0

Neutrality

0/+

Allotrophy



+/–

Parasitism

+/0

Commensalism

+/+

Symbiosis



0

+



Adapted from Burkholder, Am. Sci., 40, 601–631, 1952.



interaction terminology, though some have been reviewed previously (Abrams, 1987).

Because terms have been applied differently in different fields, comparison of interactions

across fields in ecology is difficult. It is intended for this chapter to clarify the sources

of the inconsistencies, which are discussed in separate sections for general and fungal

ecology, and to describe particular problems with application of general ecology terminology to fungi due to their growth form and life histories. I discuss temporal dynamics

of interactions and measures best used to describe outcomes. I discriminate between

interactions involving nutrient acquisition and those not involving nutrient acquisition

and propose a revised set of terms. It is anticipated that this chapter will raise questions

and generate discussions about the best use of interspecific interaction terms. For that

reason, it is hoped that this paper will facilitate discussions among ecologists by categorizing terms according to mode of nutrient acquisition and by making terms that are

currently in use commensurate.



13.2



GENERAL ECOLOGY TERMINOLOGY



Description of interspecific interactions began when deBary (1887) first described close

relationships between two organisms as symbioses, regardless of positive or negative

outcome of interaction. He divided these symbioses into saprophytic and parasitic interactions. These categorizations were based on mode of nutrient acquisition and were

adequate descriptors because they were the only ones. Burkholder (1952) subsequently

made progress by characterizing biological interactions according to outcomes (Table

13.1), which was useful because it is practical to measure a population’s size in many

instances. However, he initiated a long history of the confusing use of the terms symbiosis

and parasitism by equating them with outcomes and by describing “symbiosis” as only a

mutually beneficial interaction. Odum (1959) modified Burkholder’s description by differentiating between the effects on organisms when they did and did not interact (Table

13.2), though this distinction is not always practical. Harper (1961), Schoener (1983), and

Hodge and Arthur (1996) have all described alternate terms for antagonistic interactions,

with Schoener dividing competition according to the particular mechanisms involved. In

the more than a century since deBary’s report of types of interactions, we have had many

contributions to the pool of terms available to describe interspecific interactions, but little

consistency across the sets of terms.



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Table 13.2 Effects on Organisms When They Are and Are Not Interacting

When Not Interacting



When Interacting



Type of Interaction



A



B



A



B



Result of Interaction



Competition

Amensalism

Neutralism

Commensalism

Protocooperation

Mutualism

Parasitism/predation



0

0

0

–

0

–

–



0

0

0

0

0

–

0



–

–

0

+

+

+

+



–

0

0

0

+

+

–



Obligatory for A

Facultative for both

Obligatory for both

Obligatory for A



Adapted from Odum, Fundamentals of Ecology, W.B. Saunders Co., Philadelphia, 1959.



13.3



FUNGAL ECOLOGY TERMINOLOGY



Mycologists have employed some terms previously used to describe interspecific interactions based on outcome (Cooke and Rayner, 1984; Rayner and Webber, 1984; Rayner and

Boddy, 1988b; Zabel and Morrell, 1992). Not all terms that are available apply to fungi,

and some definitions have to be changed slightly in order to be more accurate in their

application to fungi. In addition, terms were developed by mycologists to describe specific

mechanisms exhibited by fungi during interactions (Rayner and Boddy, 1988a, 1988b;

Table 13.3) and mechanisms for competitive or antagonistic interactions in detail (Lockwood, 1992; Wicklow, 1992; Boddy, 2000), adding to the pool of available terms. Because

mycologists have tried to use some available terms, but required additional descriptors for



Table 13.3 Descriptions of Bilateral Fungal Interactions

Interaction

Neutralistic

Mutualistic

Competitive

Primary resource capture

Combat

Defense (antagonism at a distance, hyphal interference,

mycoparasitism, gross mycelial contact, deadlock)

Secondary resource capture (replacement)



Outcome

0/0, 0/+, +/0

+/+

0/–, –/0, –/–

(Mechanism)

(Mechanism)

(Mechanism)

(Mechanism)



Note: Various outcomes may occur for interactions that are considered a subdivision of

competition. However, these terms actually describe the mechanism involved in the

interaction.

Adapted from Rayner and Boddy, Fungal Decomposition of Wood, John Wiley & Sons,

New York, 1988b, with information from Boddy, FEMS Microbiol. Ecol., 31, 185–194,

2000, added.



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specific types of fungi (e.g., wood decomposers), we now have a set of terms with slightly

different meanings in fields of ecology, plus a combination of some terms describing

outcomes and others describing mechanisms. Mycologists, in their effort to reduce the

number of new terms by borrowing some from general ecology, yet requiring additional

terms for specific circumstances particular to fungi, have compounded the confusion

arising around a clear description of interspecific interactions.



13.4



DISCUSSION OF GENERAL ECOLOGY TERMINOLOGY



While Burkholder’s (1952) characterization helped clarify ecological concepts, some of

Burkholder’s terms do not apply to fungi and some are redundant. The terms allotrophy,

defined as feeding another organism, and allolimy, defined as starving another organism,

appear to be associated with higher organisms than fungi because fungi cannot actively

feed or starve other organisms. Burkholder used symbiosis to describe only mutualistic

interactions, whereas deBary’s original use of symbiosis referred to any close relationship

between two or more organisms (deBary, 1887), whether harmful or beneficial. Burkholder

used synnecrosis to refer to interactions that are negative for both organisms, implying

that both organisms in a mutually antagonistic relationship will die; however, death is not

inevitable. Burkholder’s categorization of interactions according to outcome was useful,

but some of his terms, such as allotrophy, allolimy, symbiosis, and synnecrosis, are not

generally applicable, especially to fungi.

Odum’s modification enabled ecologists to describe interactions as facultative or

obligate. Odum also adopted some new terms for outcomes described by Burkholder and

added some categories. According to Odum, the difference between protocooperation and

mutualism is whether both organisms are not affected (0/0, protocooperation) or are

negatively affected (–/–, mutualism) in the absence of the interaction. This distinction is

difficult to assess because comparative measurements can only be made relative to the

interaction. Both the null effect and any negative effect will appear negative relative to

any positive effect of the interaction. Odum also replaced Burkholder’s term synnecrosis

with competition, which is equally misleading, because it describes only one possible

mechanism leading to an outcome in which both organisms are inhibited (–/–) (see Abrams,

1987). Other mechanisms, such as allelopathy, may also result in mutual inhibition.

Odum’s use of parasitism and predation to describe outcomes that are positive for one

organism and negative for the other (+/–) is also confusing. Parasitism and predation are

modes of nutrient acquisition, or nutritive interactions, which should be considered separately from nonnutritive interspecific interactions (see below).

Harper (1961) used the term interference rather than competition to describe antagonistic interactions in plant ecology. He maintained that this term, rather than competition,

could be applied more uniformly to all fields because of the many different connotations

that exist within different fields concerning competition. Interference was later used in

fungal ecology to describe a subdivision of competition, together with exploitation (see

below, also Tinnin, 1972; Lockwood, 1992; Wicklow, 1992). Both interference (whether

used as a synonym or as a subdivision of competition) and exploitation describe mechanisms involved in antagonistic behavior.

Schoener (1983) used a set of six terms to describe the mechanisms of competition:

consumptive, preemptive, overgrowth, chemical, territorial, and encounter. His terms may

be appropriate in some situations to describe antagonistic interactions, but they describe

only mechanisms for one type of outcome. These mechanisms of antagonism should be

treated separately from the outcomes.



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Arthur and Mitchell (1989) used similar terms: competition (–/–), amensalism (–/0),

contramensalism (+/–), commensalism (+/0), and mutualism (+/+). However, they do not

distinguish mechanism from effect, nor nutritive from nonnutritive interactions. They

suggested that mechanism should be separated from outcome, but their system is not

structured to do so.

Problems in describing interspecific interactions also arise from variability in

responses due to temporal, spatial, and environmental variability. In addition, for all of

these schemes of interactions, more than one mechanism of interaction may be occurring

simultaneously. Each of these schemes relies upon an average of outcomes to determine

the net effect, and the length of time of observation may affect the observer’s determination

of type of interaction (Arthur and Mitchell, 1989). Interactions are likely to vary spatially

and change over time (Hodge et al., 1999). These interactions are dynamic and are

conditional upon the abiotic and biotic environment in which they occur (Bronstein, 1994).

For instance, pH affected the ability of nematodes to antagonize root pathogenic fungi

(El-Borai et al., 2002). Aspergillus ochraceus was most effective at antagonizing six other

species of maize spoilage fungi under moderate water availability at 18°C (Lee and Magan,

1999, 2000). When water was freely available, Alternaria alternata and Aspergillus niger

became dominant (Lee and Magan, 1999). At 30°C and moderate water availability, A.

ochraceus was dominated by other fungi except A. alternata (Lee and Magan, 2000). So

the outcome of the interaction between A. ochraceus and A. alternata is highly dependent

upon water availability and temperature. Water potential also affected outcome of interactions between fungi colonizing ash twigs (Griffith and Boddy, 1991), and water activity

and temperature affected interactions of fungi isolated from maize (Sanchis et al., 1997).

Environmental factors affect parasites (Michalakis et al., 1992) and mycoparasitism

(reviewed in Lumsden, 1992). Nutritional differences in the environment may also regulate

outcomes. Nutritional or structural differences between agar and wood caused outcomes

of interactions between fungi grown on wood discs to be different from interactions on

nutrient agar (Holmer and Stenlid, 1993). Interactions between Ceratocystis ulmi and elm

bark saprotrophs were different on malt extract agar (MEA) in petri dishes than in elm

logs (Webber and Hedger, 1986) as well. However, outcomes of interactions between wood

decay fungi plated against Armillaria luteobubalina on MEA did correspond to interactions

in Eucalyptus wood (Pearce, 1990). For this reason, conditions in which observations of

interactions are made should be made clear along with timing of “stage-specific phenomena” (Bronstein, 1994) to more fully understand the nature of the interaction.

In addition to abiotic environmental effects, biotic components can affect interactions

between organisms. For example, Dendroctonus bark beetles do worse in the presence of

phoretic Tarsonemus mites because Ophiostoma carried as a food source by the mites

antagonizes the mycangial fungi of the bark beetle, reducing the food source of the bark

beetle (Lombardero et al., 2003). This agonistic (–/+) interaction between the beetle and

the mites is the result of indirect effects of the biotic environment, whereas the direct

effect is a commensal (0/+) relationship between the mites and the beetles. Therefore, it

should be made clear whether the results of an interaction are direct or indirect (see also

Callaway and Walker, 1997). Tritrophic interactions ultimately can affect the outcome of

interactions between organisms distantly related, such as the cereal aphid parasitoid

(Aphidius rhopalosiphi) and an entomopathogenic fungus (Erynia neoaphidis), which

utilize the same food source (the grain aphid, Sitobion avenae; Fuentes-Contreras et al.,

1998). Timing of arrival of the parasitoid relative to fungal spore arrival will affect the

outcome of the interaction. Similarly, single-genet isolates of Marasmius androsaceus

were identified in younger plots, whereas discontinuous distribution was observed in older

plots (Holmer and Stenlid, 1991). Successional changes in species distributions and abun-



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dances likely affect the interactions between species within the environment (Connell and

Slatyer, 1977). Spatial patterning of 60 taxa of mycophagous insects on 66 mushroom

taxa were more closely related to aggregates of the insect species than to species of food

source, indicating dispersal as the reason for existence on a particular fruit body, rather

than niche differentiation by food type (Wertheim et al., 2000). Insects were cohabiting

(0/0) the mushrooms rather than coantagonizing (–/–) one another and eliminating each

other from the resource. Consequently, measures of biotic environmental conditions can

be affected by the temporal and spatial scales in which measures are taken and can influence

interpretation of outcomes. Size of population is known to affect outcomes of interactions

(Holmer and Stenlid, 1993) as well as other factors inherent in measure of population

growth rate. Therefore, type of measurement taken (growth, birth rate, death rate, reproductive success) can influence conclusions from interspecific interactions (Abrams, 1987).

A comprehensive terminology should account for these variables.

13.4.1



Application of General Ecology Terminology to Fungi:

Distinguishing Features of Fungi

Fungi are sedentary microscopic organisms with an indeterminate growth form. Although

fungal hyphae are microscopic, population distribution and dispersal of spores often cover

large geographic areas (e.g., see Smith et al., 1992). Likewise, the functions performed

by fungi are often related to an ecosystem or landscape scale (e.g., see Kuyper and Bokeloh,

1994). Hence, interactions at the microscale may have broad effects. The indeterminate

growth form allows fungi to interact with different organisms at different places across a

mycelial network. Each interaction may simultaneously have different effects. This growth

form allows an individual fungus to wall off an area in the event of antagonism (–/0),

which may result in two individuals plus a senesced portion of mycelium. Hence, quantification of populations is difficult and populations may not be reduced as a result of

antagonism.

Fungi, along with many other microorganisms, are not large enough to take in many

molecules that would be valuable sources of carbon and nutrients, so they release extracellular compounds to decompose substances prior to uptake (Bruce et al., 1984; Ghisalberti and Sivasithamparam, 1991; Dandurand and Knudson, 1993; Score et al., 1997).

Production and release of oxalic acid, known to aid in weathering of minerals and thereby

increase nutrient availability, by the mycorrhizal fungus Paxillus involutus was affected

by a form of nitrogen in media and the concentration of calcium and bicarbonate ions

(Lapeyrie et al., 1987). Oxalic acid was also produced by brown-rot fungi, though not in

the same quantities by all species (Espejo and Agosin, 1991). Oxalic acid reduced pH in

brown-rot cultures (Dutton et al., 1993), consequently increasing favorable conditions for

enzyme activity. In the study by Espejo and Agosin (1991), oxalic acid that was produced

was then oxidized to CO2 during the process of cellulose depolymerization. Release of

oxalic acid by one fungus may benefit many others in the vicinity. Other extracellular

substances released by fungi (whether enzymes or waste) could be used by other microorganisms as a nutrient source or may enhance or be inhibitory to their growth (Garbaye,

1991; Score et al., 1997).

These particular features make application of some of the previously used general

ecology terminology for interspecific interactions to fungi not completely appropriate. For

instance, Burkholder’s use of allotrophy and allolimy do not apply to sedentary organisms,

and his synnecrosis has an outcome (–/–) that might occur in hyphal tips in fungi but will

not kill the organism, as implied by the term. Odum uses mechanisms for antagonism that

confuse nutrient acquisition. This distinction is particularly important for microorganisms

because nutrient acquisition occurs extracellularly, will nearly always impact other organ-



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isms, and may not always do so in a negative manner (such as in the case where one

organism releases extracellular enzymes to decompose a substrate and another organism

benefits by using the enzymes or the products of the reaction as a nutrient source; Garbaye,

1991). Consequently, mycologists have adopted slightly different terms to describe antagonistic (–/0) interactions (exploitation and interference) that begin to differentiate nutritive

from nonnutritive interactions but do not do so explicitly. General ecology terms should

be selected and applied carefully to describe microbial interspecific interactions to ensure

that the connotation is correct and that the meaning of a single term is not required to

change among fields for proper application.



13.5



DISCUSSION OF FUNGAL ECOLOGY TERMINOLOGY



Rayner and Boddy (1988a, 1988b) and Boddy (2000) modified Burkholder’s schema (Table

13.3), but included only competitive, neutralistic, and mutualistic interactions. These three

main categories are similar to previous definitions in that they are based on outcomes of

interactions. Their divisions within competition — primary resource capture, combat

(antagonism at a distance, hyphal interference, mycoparasitism, or gross mycelial contact),

defense, and secondary resource capture — however, pertain to the biology and action of

the organisms and, thus, refer to mechanisms.

In this system, the subdivisions of competition are actually mechanisms of interactions with various outcomes, some of which are not the result of competition, and therefore

should not be described as subdivisions of competition. Primary resource capture describes

colonization of a resource by one organism but may not result in competition for resources

(ruderals generally do not exhibit competition). There is no interaction in primary resource

capture, so no outcome can be identified. Combat refers to “interference competition,”

according to Rayner and Webber (1984). This is particularly confusing because their

subdivisions of combat (defense, defending a resource through interference; secondary

resource capture, replacement by competing for resources and using interference) refer

to both interference and resource competition. Additional confusion arises because defense

only describes an interaction from the perspective of one organism. The outcome of the

interaction depends on the effects of the second organism. For instance, fungus A may

defend its territory through the production of allelochemicals. However, if fungus B is

involved in secondary resource capture, and the allelochemicals produced by fungus A

did not result in complete inhibition of fungus B, then fungus A would be harmed regardless

of its defense mode (–/+) because fungus B would acquire resources from A. Alternatively,

if both fungus A and fungus B were involved in defense only, the result might be a deadlock

in which both organisms might be harmed (–/–) because they have expended resources.

Although the attempt made by Rayner and Boddy to describe fungal interactions with

underlying mechanisms is a much needed addition to fungal ecology, it is a very specific

set of terms that are mainly applicable to wood decomposer fungi. The mixture of terms

within their schema is cumbersome, and the descriptions of mechanisms are not broadly

applicable to diverse organisms in other disciplines in ecology.

Within fungal ecology, interference competition has been used to describe indirect

inhibition (e.g., allelopathy or antibiosis) (Lockwood, 1992; Wicklow, 1992). This contrasts with exploitation competition or resource competition, where organisms compete

directly for a resource such as nutrients or space (Lockwood, 1992). While some argue

that interference and exploitation do not accurately describe coantagonistic (–/–) fungal

interactions (Cooke and Rayner, 1984; Boddy, 2000), any of these terms, along with the

terms proposed by Rayner and Boddy that were discussed above, could be used to describe



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Table 13.4 Distinction between Fungal Interactions Involving Nutrient Acquisition and Those

That Do Not Involve Nutrient Acquisition

Nutritive Interactions

(Interactions between a fungus and another

organism from which the fungus receives

nutrients)



Nonnutritive Interactions

(Interactions between a fungus and another

organism from which the fungus does not

receive nutrients)



Biotrophism

Necrotrophism

Saprotrophism



Coantagonism

Antagonism

Agonism

Cohabitation

Commensalism

Mutualism



Note: Each nutritive interaction may occur simultaneously with any nonnutritive interaction in one organism,

but the interactions are distinct. Terms used for nonnutritive interactions are described in more detail in Table

13.5.



mechanisms of antagonistic or coantagonistic behavior. When mechanisms specific to a

group of organisms are used in combination with general outcome-derived terms, a more

complete description of the interspecific interaction (described further below) is possible.



13.6



PROPOSED CATEGORIZATION OF INTERSPECIFIC

INTERACTIONS



Ecological terms describing interspecific interactions incorporate a mixture of mechanisms

of interaction involving nutrient acquisition and not involving nutrient acquisition. For

instance, interactions involving organisms that feed on other organisms directly should be

separated from interactions in which organisms interact directly with one another for a

pool of nutrients that is indirectly depleted as a result of the interaction. I propose that two

types of interactions be considered: (1) interactions between an organism and any organism

from which it directly receives nutrients, nutritive interactions, and (2) interactions between

an organism and any organism from which it does not directly receive nutrients, nonnutritive interactions (Table 13.4). These interactions should be considered separately because

the underlying mechanisms are different and are not directly comparable.

13.6.1

Nutritive Interactions

Nutritive interactions were described by deBary in 1887 as saprophytic and parasitic.

Contemporary terms result from refinement of deBary’s concepts to include biotrophy

(obtaining nutrients from the living cells of the host, e.g., parasitism; Barak and Chet,

1986; Figure 13.1), necrotrophy (acquiring nutrients by killing an organism, e.g., predation), and saprotrophy (acquiring nutrients from dead material, e.g., decomposition)

(Lewis, 1973; Luttrell, 1974; Cooke and Rayner, 1984; Douglas, 1994). DeBary’s concept

of classifying organisms, and fungi in particular, according to type of nutritive interaction

persists in these schemes and in current use.



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( )



Figure 13.1 Example of potential biotrophic nutritive interactions. Fomitopsis pinicola (Swartz:

Fr.) Karst encounter with Cenococcum geophilum Fr. on modified Melin-Norkrans medium (MMN)

at 20°C.



DeBary originally suggested that the classes of nutrient acquisition that he proposed

were not mutually exclusive categories, but overlapped, and this continuum has been

suggested by others (Lewis, 1973; Harley and Smith, 1983). Under this classification, the

often cited example of mycorrhizae (see also below) would be an example of bilateral

biotrophism, not mutualism. This removes the frequently discussed problem of mycorrhizal

interactions not always having a positive outcome for both the host and the symbiont. The

cost and benefit to each organism are independent of the categorization of the interaction.

Biotrophisms may be facultative or obligate. Organisms may alternate between nutritional

modes throughout their lives (Luttrell, 1974; Cooke and Rayner, 1984; Douglas, 1994),

or among stages in their life cycles. For example, an organism may be saprotrophic in

one stage of its life cycle and become biotrophic in another (Bateman, 1978). The ability

to adjust the mode of nutrient acquisition in response to changes in resource availability

might allow organisms to avoid direct competition for a particular resource with another

organism (Cooke and Rayner, 1984). Knowing the mode of nutrient acquisition of organisms can help to predict the types of nonnutritive interspecific interactions that may occur

(e.g., two saprotrophs might be more likely to compete than would a saprotrophic and a

necrotrophic fungus).

13.6.2

Nonnutritive Interspecific Interactions

Nonnutritive interspecific interactions are abundant in nature and important to population

structure (Hairston et al., 1960). However, few nonnutritive fungal interactions have been

documented. The few investigations reported have focused on competition (Rayner and

Boddy, 1988b; Shearer and Zare-Maivan, 1988; Lockwood, 1992; Wicklow, 1992; Wardle

et al., 1993; Shearer, 1995; Holmer and Stenlid, 1997a). Dodds (1997) attributes this bias

toward reporting of competitive interactions to error in experimental design (but see Wardle

et al., 1993; Hodge et al., 1999). Even when a null hypothesis of no interaction is tested

statistically, as recommended by Dodds (1997), careful attention must still be paid to



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experimental design. Attributing colonization of a substrate to only one organism (all or

nothing) can lead to conclusions of antagonism (–/0), when cohabitation (0/0) of the

substrate may have existed (Holmer et al., 1997).

13.6.3

Symbiosis

In the sense used by deBary, symbiosis refers to any close relationship, whether positive

or negative, between two organisms, involving nutrient acquisition or not. Mycorrhizae

would be symbiotic biotrophisms — close relationships involving nutrient acquisition.

In mycorrhizae, fungi acquire carbon from and exchange nutrients with host plants

(Allen, 1991; Smith and Read, 1997). Other examples of nutritive symbioses would

include gut parasites extracting nutrients from hosts and necrotrophism of, or feeding

on, mycangial fungi by bark beetles (Lombardero et al., 2003). These would also be

biotrophic symbioses. Ant–membracid interactions would be mutualistic symbioses —

close relationships with positive effects on the population size of both organisms

involved, but not involving direct nutrient acquisition (Cushman and Whitham, 1989).

The membracid nymphs receive protection from predators by the ants and the ants use

a waste product of the membracids, not directly feeding on the membracids. Other

examples of nonnutritive symbioses include a commensal symbiosis — coprophilous

fungi that require passage of spores through an animal gut to germinate but neither

contribute to nor extract nutrients from the host. Both nutritive and nonnutritive interactions can be symbiotic, following from deBary’s (1887) definition of symbiosis, a

close relationship between two organisms.

DeBary (1887) only used symbiosis to refer to modes of nutrient acquisition.

Burkholder (1952) originated the description of interspecific interactions by outcome and

used the term symbiosis more narrowly to describe a mutually beneficial outcome in

interspecific interactions; this use continues to be popular in some countries. However,

the common use of the term mutualism synonymously with symbiosis has led to the blurring

of the nutritive and nonnutritive interactions. Because symbiosis encompasses both nutritive and nonnutritive interactions, careful attention must be made to distinguish among

them when describing a symbiosis; otherwise, more descriptive information for these

interactions may be lost. A description of the specific nature of symbioses can be more

clear by adding nutritive or nonnutritive descriptors rather than using symbiosis synonymously with one type of nonnutritive interaction (mutualism). To aid future studies, the

remainder of this discussion will focus on nonnutritive interspecific interactions because

the terminology used to describe them requires further refinement, whereas terms used to

describe nutrient acquisition interactions are adequate.



13.7



PROPOSED CLASSES OF NONNUTRITIVE

INTERSPECIFIC INTERACTIONS



Outcomes of nonnutritive interspecific interactions are more readily compared across

disciplines in ecology than are mechanisms, although both categories are necessary for

full understanding of the interaction. Information regarding mechanism can be used to

modify descriptions, but terms based on mechanism alone will not clarify terminology.

Measures taken to evaluate outcome are dependent upon the purpose of the investigation

(Figure 13.2). Definitions of nonnutritive interspecific interactions are given below with

examples from fungal ecology.



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Purpose of Investigation



1. Determine resource use

2. Predict species presence (community structure) given changes in

ecosystems

3. Determine conditional outcomes/hierarchies

4. Predict evolutionary changes in populations based on determined

pressures



Type of Analysis

Long-term analyses

(population size and measures of fitness)

Short-term +/− effects

(growth measures on individuals or populations)



Figure 13.2 Key for determination of type of measures to take to determine outcomes of interspecific interactions.



13.7.1

Coantagonism

Coantagonism refers to any interaction that results in a negative outcome for both members

(–/–; Figure 13.3a and Figure 13.4a). Mechanisms of antagonism may be different for

either fungus, however, and the outcome may not be equally strongly negative for each

fungus (Holmer and Stenlid, 1997a). It is the combination of effects, with mainly negative

effects for each, that results in coantagonism. The term coantagonism is preferable to

competition to describe bilateral mutually antagonistic interactions because competition

describes only one mechanism of antagonistic interactions. Coantagonism is more consistent with terms currently used to describe other outcomes of interspecific interactions.

In studying fungal interactions in culture, three ways to identify antagonism follow.

If fungus A is antagonized by fungus B, fungus A may respond by (1) asymmetrical

inhibition only in the direction of B; (2) general decrease in overall colony size, irrespective of direction; or (3) increased radial colony diameter, but decreased hyphal diameter

and mycelial density. The latter may not actually have a negative effect on the antagonized

fungus. In this discussion, coantagonism refers to the joint action of the first two types

of antagonism.

Examples of coantagonism are relatively abundant in the mycological literature.

Nine species of brown-rot fungi coantagonized one another in plate pairings on malt extract

agar (Owens et al., 1994), though some species combinations were likely involved in

antagonism (–/0) rather than coantagonism (–/–). The same is true for seven species of

white-rot fungi and for interactions between species of brown-rot and white-rot fungi.

These interactions are further described by the mechanisms resulting in this outcome,

replacement or deadlock (see Table 13.5 and Section 13.8). Coniophora puteana and

Scytalidium spp. produced laccase (a widespread phenol-oxidizing enzyme that can cause

mycelial morphogenesis) in the presence of one another (Score et al., 1997), as did Serpula



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(a)



(b)



−

−

Co-antagonism

(d)



(c)



−

0

Antagonism



−

+

Agonism



(e)



0

0

Co-habitation



(f)



0

+

Commensalism



+

+

Mutualism



Figure 13.3 Possible interactions between two fungal cultures on petri dishes based on measurement of radial growth. Fungus A is the shaded colony and fungus B is the white colony.



(a)



(b)



(c)



(d)



Figure 13.4 Examples of nonnutritive interspecific interactions. (a) Coantagonism (–/–) (Trametes versicolor (L.: Fr.) Pilat) + (Paxillus involutus (Fr.) Fr. on water agar at 20°C. (b) Antagonism

(–/0) (T. versicolor (L.: Fr.) Pilat + Laccaria bicolor (Maire) Pat.) on water agar at 20°C. (c) Agonism

(+/–) (Fomitopsis pinicola (Swartz: Fr.) Karst + Paxillus involutus (Fr.) Fr.) on MMN at 20°C. (d)

Cohabitation (0/0) (T. versicolor (L.: Fr.) Pilat + Thelephora americanus Lloyd) on MMN at 20°C.