Ecological Archives E091-184-A4

Otso Ovaskainen, Jenni Hottola, and Juha Siitonen. 2010. Modeling species co-occurrence by multivariate logistic regression generates new hypotheses on fungal interactions. Ecology 20:2514–2521.

Appendix D. Discussion on species-to-species interactions.

The interactive mechanisms at the mycelial stage include the use of volatile and diffusible chemicals, such as enzymes and toxins, physical interference, and physicochemical modification of the substrate (Rayner and Boddy 1988, Woodward and Boddy 2008). Competitive interactions may hinder the colonization of wood that is already occupied by another mycelium, and established mycelia combat to take over already colonized wood or to defend their territories. Mechanisms behind facilitation and mutualism include modification of the chemical composition, physical structure or moisture of the wood, and the utilization of other species’ metabolites as food or stimulators of growth or reproduction. The enzyme functions of two species can be complementary, allowing a more efficient decomposition of the wood than if each of the species would act in isolation (Rayner and Boddy 1988, Woodward and Boddy 2008). Some species are specialized to interact very closely with another particular species, generating so-called predecessor-successor species pairs (Niemelä et al. 1995, Holmer et al. 1997).

Few laboratory experiments have been conducted to study directly how wood-decaying fungal species interact with each other (Table D1). A general pattern arising from the laboratory experiments is that secondary decayers are typically better competitors than primary decayers (Holmer et al. 1997, Holmer and Stenlid 1997, Boddy 2000). As an exception, the primary decayer T. abietinum (S22) has replaced not only other primary decayers, such as F. pinicola (S7), but also many secondary decayers in laboratory conditions (Holmer et al. 1997).

In our results, the majority of the negative correlations on spruce (Fig. 2a) were estimated for species pairs in which either T. abietinum or F. pinicola was involved, whereas these two species were positively associated with each other (Fig. 2a). Possible explanations for the positive association are i) that the high competitive ability of T. abietinum may help it colonize logs that are already occupied by F. pinicola, and ii) the differential resource use of these two species. F. pinicola often colonizes the tree when it is standing or even still alive (Table A2 in Appendix A), contributes to the breaking down of the tree, and produces large decay columns extending from the heartwood (Holmer and Stenlid 1997). In contrast, T. abietinum starts its active growth only after the tree has died, and its decay extends from the sapwood. F. pinicola is a brown-rot species, decomposing cellulose and hemicellulose but leaving most of the lignin unaltered. T. abietinum is a white-rot species and thus able to decompose lignin and gain access to the energy- and nitrogen-rich polysaccharides that are unavailable to F. pinicola. As F. pinicola has large perennial fruit bodies that remain identifiable long after their death, these two species may co-occur as fruit bodies long after T. abietinum has started to invade the decay columns of F. pinicola.

Niche separation may also relate to the positive association between T. abietinum and the brown-rot species A. serialis (S2)and G. sepiarium (S9). If these two species can defend themselves against T. abietinum, they may gain an advantage from T. abietinum outcompeting several other species. Most of the associations of T. abietinum with other species (mainly white-rot species) are negative (Fig. 2a), and probably arise from the superiority of T. abietinum as a competitor. It is more difficult to find a likely explanation for why several white-rot species do not fruit on logs occupied by F. pinicola (Fig. 2). We speculate that these associations may be connected with F. pinicola capturing a large volume of the log relatively quickly after the tree death, leaving little space and degradable resources for secondary decayers, especially brown-rot species such as P. caesia (S18) (Fig. 2a). The brown-rot species A. serialis and A. sinuosa (S3) have not been included in any published interaction experiments, but their positive association with F. pinicola (Fig. 2a) would suggest that they have good competitive abilities.

We obtained several positive associations for the species A. lapponica (S1) with both brown-rot and white-rot species (Fig. 2a). This seems contradictory to the results by Holmer and Stenlid (1997), who set 12 species to compete with each other in pairwise combinations, and placed A. lapponica  at the bottom of the general competitive hierarchy F. rosea (S8) > P. ferrugineofuscus (S12) > P. viticola (S16) > F. pinicola (S7) > A. lapponica. However, this overall hierarchy is inconsistent with the results obtained for some particular species pairs, suggesting that the outcome of species-to-species interactions is not determined just by overall competitive abilities. Indeed, species-to-species interactions are affected by the specific competitive mechanisms, mediation by the abiotic environment, inoculum size (Holmer and Stenlid 1997), resource size and quality, and the presence of other fungi, invertebrates or micro-organisms (Boddy et al. 2008, Woodward and Boddy 2008). As an example, A. lapponica seems to be dependent on or favored by F. rosea (Holmer and Stenlid 1997), the strong competitive ability of which might help A. lapponica to coexist with other species.

Turning to the species community on birch (Fig. 2b), we suggest that F. pinicola‘s strength and efficiency as a decayer is a likely reason behind its negative association with the white-rot species T. ochracea (S20) and T. hymenocystis (S21). F. fomentarius (S6) is another dominating decayer of birch which co-occurs with P. betulinus (S17), probably because the latter is a superior competitor (Supplementary Table V) and thus able to establish on logs occupied by F. fomentarius. P. betulinus (a brown-rot species) may also gain advantage of F. fomentarius‘ (a white-rot species) ability to decompose lignin. The fruit bodies of P. betulinus are usually on branches or the top part of the trunk, whereas F. fomentarius typically possesses the basal and middle part of the trunk.

While it is interesting to relate our results to direct interaction experiments, we note that laboratory studies have their limitations, as their outcomes are much influenced by the chosen abiotic environment, such as substrate, gaseous conditions, water potential, pH and temperature (Boddy 2000, Woods et al. 2005). Further, most laboratory studies conducted so far have been based on only one strain per species (see Woodward and Boddy 2008). Unfortunately, interaction studies on wood-decaying fungi are difficult to conduct in the field and are thus very few (but see Woods et al. 2006). In contrast, data on species co-occurrence at the fruit-body stage can be acquired relatively easily, and these data reflect the outcome of species interactions under natural conditions.

Concerning the limitation of our results, fruit-body data fail to give information on the spatial and temporal dynamics of mycelia inside the logs, including the mechanisms behind species interactions. Further, our results may be biased by differences in the life spans of fruit bodies (Table A2 in Appendix A), as short-lived annual fruit bodies are perceivable for a shorter time than long-lived perennial fruit bodies, the latter also sometimes staying identifiable as dead even after the species has been outcompeted from the log.

TABLE D1. Species interactions based on laboratory experiments in which each species was first grown in isolation, and then pairs of species were brought into contact. A>>B means that species A always replaced species B in the experiments. A>B means that species A was typically able to invade the territory held originally by species B, but that the result depended e.g. on inoculum size. AB means that neither of the species was clearly superior in competitive effect or response.Data compiled from literature (Holmer et al. 1997, Holmer and Stenlid 1997). The column Correlation is based on Fig. 2, showing the median estimate (averaged among sites) for the model M2(R), including only cases in which the posterior probability for a positive (negative) correlation was at least 90%.

Species pair

Substrate

Correlation

A. lapponica (S1) < F. pinicola (S7)

spruce

-

A. lapponica (S1) << P. ferrugineofuscus (S12)

spruce

0.40

A. lapponica (S1) << P. viticola (S16)

spruce

0.24

F. pinicola (S7) = F. rosea (S8)

spruce

0.26

F. pinicola (S7) < P. ferrugineofuscus (S12)

spruce

-0.22

F. pinicola (S7) << P. viticola (S16)

spruce

-0.18

F. pinicola (S7) < T. abietinum (S22)

spruce

0.35

F. rosea (S8) = P. ferrugineofuscus (S12)

spruce

-

F. fomentarius (S6) << P. betulinus (S17)

birch

0.33

F. fomentarius (S6) < P. igniarius (S13)

birch

-

 

LITERATURE CITED

Boddy, L. 2000. Interspecific combative interactions between wood-decaying basidiomycetes. Fems Microbiology Ecology 31:185–194.

Boddy, L., J. C. Frankland, and P. van West, editors. 2008. Ecology of Saprotrophic Basidiomycetes. Elsevier, Amsterdam, The Netherlands.

Holmer, L., P. Renvall, and J. Stenlid. 1997. Selective replacement between species of wood-rotting basidiomycetes, a laboratory study. Mycological Research 101:714–720.

Holmer, L., and J. Stenlid. 1997. Competitive hierarchies of wood decomposing basidiomycetes in artificial systems based on variable inoculum sizes. Oikos 79:77–84.

Niemelä, T., P. Renvall, and R. Penttilä. 1995. Interactions of fungi at late stages of wood decomposition. Annales Botanici Fennici 32:141–152.

Rayner, A. D. M., and L. Boddy. 1988. Fungal decomposition of wood: its biology and ecology. John Wiley & Sons, Bath.

Woods, C. M., S. Woodward, M. A. Pinard, and D. B. Redfern. 2006. Colonization of Sitka spruce stumps by decay-causing hymenomycetes in paired inoculations. Mycological Research 110:854–868.

Woods, C. M., S. Woodward, and D. B. Redfern. 2005. In vitro interactions in artificial and wood-based media between fungi colonizing stumps of Sitka spruce. Forest Pathology 35:213–229.

Woodward, S., and L. Boddy. 2008. Interactions between saprotrophic fungi. Pages 125-141 in L. Boddy, J. C. Frankland, and P. van West, editors. Ecology of Saprotrophic Basidiomycetes. Elsevier, Amsterdam.



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