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Modelling fungal competition for space:Towards prediction of community dynamics
1. | ORCID: 0000-0003-4452-7106, Department of Mathematics, Swansea University, Bay Campus, Swansea, SA1 8EN, UK |
2. | ORCID: 0000-0003-1544-0407, Department of Biosciences, Swansea University, Singleton Park Campus, Swansea, SA2 8PP, UK |
3. | ORCID: 0000-0003-0486-5450, Department of Mathematics, Swansea University, Bay Campus, Swansea, SA1 8EN, UK |
Filamentous fungi contribute to ecosystem and human-induced processes such as primary production, bioremediation, biogeochemical cycling and biocontrol. Predicting the dynamics of fungal communities can hence improve our forecasts of ecological processes which depend on fungal community structure. In this work, we aimed to develop simple theoretical models of fungal interactions with ordinary and partial differential equations, and to validate model predictions against community dynamics of a three species empirical system. We found that space is an important factor for the prediction of community dynamics, since the performance was poor for models of ordinary differential equations assuming well-mixed nutrient substrate. The models of partial differential equations could satisfactorily predict the dynamics of a single species, but exhibited limitations which prevented the prediction of empirical community dynamics. One such limitation is the arbitrary choice of a threshold local density above which a fungal mycelium is considered present in the model. In conclusion, spatially explicit simulation models, able to incorporate different factors influencing interaction outcomes and hence dynamics, appear as a more promising direction towards prediction of fungal community dynamics.
References:
[1] |
L. Boddy,
Interspecific combative interactions between wood-decaying basidiomycetes, FEMS Microbiology Ecology, 31 (2000), 185-194.
doi: 10.1111/j.1574-6941.2000.tb00683.x. |
[2] |
L. Boddy,
Saprotrophic cord-forming fungi: Meeting the challenge of heterogeneous environments, Mycologia, 91 (1999), 13-32.
doi: 10.2307/3761190. |
[3] |
G. P. Boswell,
Modelling combat strategies in fungal mycelia, Journal of Theoretical Biology, 304 (2012), 226-234.
doi: 10.1016/j.jtbi.2012.03.036. |
[4] |
J. L. Bown, C. J. Sturrock, W. B. Samson, H. J. Staines, J. W. Palfreyman, N. A. White, K. Ritz and J. W. Crawford,
Evidence for emergent behaviour in the community-scale dynamics of a fungal microcosm, Proceedings of the Royal Society B – Biological Sciences, 266 (1999), 1947-1952.
doi: 10.1098/rspb.1999.0871. |
[5] |
R. W. Buchkowski, M. A. Bradford, A. S. Grandy, O. J. Schmitz and W. R. Wieder,
Applying population and community ecology theory to advance understanding of belowground biogeochemistry, Ecology Letters, 20 (2017), 231-245.
doi: 10.1111/ele.12712. |
[6] |
I. H. Chapela, L. Boddy and A. D. M. Rayner,
Structure and development of fungal communities in beech logs four and a half years after felling, FEMS Microbiology Ecology, 53 (1988), 59-69.
doi: 10.1111/j.1574-6968.1988.tb02648.x. |
[7] |
M. J. A. Choudhury, P. M. Trevelyan and G. P. Boswell,
A mathematical model of nutrient influence on fungal competition, Journal of Theoretical Biology, 438 (2018), 9-20.
doi: 10.1016/j.jtbi.2017.11.006. |
[8] |
D. Coates and A. D. M. Rayner,
Fungal population and community development in cut beech logs. Ⅲ. Spatial dynamics, interactions and strategies, New Phytologist, 101 (1985), 183-198.
doi: 10.1111/j.1469-8137.1985.tb02825.x. |
[9] |
F. A. Davidson, B. D. Sleeman, A. D. M. Rayner, J. W. Crawford and K. Ritz,
Context-dependent macroscopic patterns in growing and interacting mycelial networks, Proceedings of the Royal Society B – Biological Sciences, 263 (1996), 873-880.
doi: 10.1098/rspb.1996.0129. |
[10] |
R. E. Falconer, J. L. Bown, N. A. White and J. W. Crawford,
Modelling interactions in fungi, Journal of the Royal Society Interface, 5 (2008), 603-615.
doi: 10.1098/rsif.2007.1210. |
[11] |
M. D. Fricker, L. L. M. Heaton, N. S. Jones and L. Boddy,
The mycelium as a network, Microbiology Spectrum, 5 (2017), 1-32.
doi: 10.1128/microbiolspec.FUNK-0033-2017. |
[12] |
J. M. Halley, H. N. Comins, J. H. Lawton and M. P. Hassell,
Competition, succession and pattern in fungal communities: Towards a cellular automaton model, Oikos, 70 (1994), 435-442.
doi: 10.2307/3545783. |
[13] |
J. Hiscox and L. Boddy,
Armed and dangerous – chemical warfare in wood decay communities, Fungal Biology Reviews, 31 (2017), 169-184.
doi: 10.1016/j.fbr.2017.07.001. |
[14] |
J. Hiscox, M. Savoury, I. P. Vaughan, C. T. Müller and L. Boddy,
Antagonistic fungal interactions influence carbon dioxide evolution from decomposing wood, Fungal Ecology, 14 (2015), 24-32.
doi: 10.1016/j.funeco.2014.11.001. |
[15] |
L. Holmer and J. Stenlid,
The importance of inoculum size for the competitive ability of wood decomposing fungi, FEMS Microbiology Ecology, 12 (1993), 169-176.
doi: 10.1111/j.1574-6941.1993.tb00029.x. |
[16] |
P. Kennedy,
Ectomycorrhizal fungi and interspecific competition: Species interactions, community structure, coexistence mechanisms, and future research directions, New Phytologist, 187 (2010), 895-910.
doi: 10.1111/j.1469-8137.2010.03399.x. |
[17] |
D. A. Kolesidis, L. Boddy, D. C. Eastwood, C. Yuan and M. S. Fowler,
Predicting fungal community dynamics driven by competition for space, Fungal Ecology, 41 (2019), 13-22.
doi: 10.1016/j.funeco.2019.04.003. |
[18] |
K. L. McGuire and K. K. Treseder,
Microbial communities and their relevance for ecosystem models: Decomposition as a case study, Soil Biology and Biochemistry, 42 (2010), 529-535.
doi: 10.1016/j.soilbio.2009.11.016. |
[19] |
H. V. Moeller and K. G. Peay, Competition-function tradeoffs in ectomycorrhizal fungi, PeerJ, 4 (2016), e2270.
doi: 10.7717/peerj.2270. |
[20] |
J. Oliva, M. Messal, L. Wendt and M. Elfstrand,
Quantitative interactions between the biocontrol fungus Phlebiopsis gigantea, the forest pathogen Heterobasidion annosum and the fungal community inhabiting Norway spruce stumps, Forest Ecology and Management, 402 (2017), 253-264.
doi: 10.1016/j.foreco.2017.07.046. |
[21] |
N. J. B. Plomley,
Formation of the colony in the fungus Chaetomium, Australian Journal of Biological Sciences, 12 (1959), 53-64.
doi: 10.1071/BI9590053. |
[22] |
J. I. Prosser, N. A. R. Gow and G. M. Gadd (eds.), Kinetics of filamentous growth and branching, in The Growing Fungus, Springer, Dordrecht, (1995), 301–318.
doi: 10.1007/978-0-585-27576-5_14. |
[23] |
J. I. Prosser and A. P. J. Trinci,
A model for hyphal growth and branching, Microbiology, 111 (1979), 153-164.
doi: 10.1099/00221287-111-1-153. |
[24] |
W. S. Rasband, ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, available from: https://imagej.nih.gov/ij/ (cited 17 Dec 2018). Google Scholar |
[25] |
T. Stella, S. Covino, M. Čvančarová, A. Filipová, M. Petruccioli, A. D'Annibale and T. Cajthaml,
Bioremediation of long-term PCB-contaminated soil by white-rot fungi, Journal of Hazardous Materials, 324 (2017), 701-710.
doi: 10.1016/j.jhazmat.2016.11.044. |
[26] |
W. Thompson and A. D. M. Rayner,
Extent, development and function of mycelial cord systems in soil, Transactions of the British Mycological Society, 81 (1983), 333-345.
doi: 10.1016/S0007-1536(83)80085-0. |
[27] |
R. Toral and P. Colet, Introduction to master equations, in Stochastic Numerical Methods: An Introduction for Students and Scientists, Wiley-VCH, Weinheim, (2014), 235–260.
doi: 10.1002/9783527683147.ch8. |
[28] |
A. van der Wal, T. D. Geydan, T. W. Kuyper and W. de Boer,
A thready affair: Linking fungal diversity and community dynamics to terrestrial decomposition processes, FEMS Microbiology Reviews, 37 (2013), 477-494.
doi: 10.1111/1574-6976.12001. |
[29] |
V. Volpert and S. Petrovskii,
Reaction–diffusion waves in biology, Physics of Life Reviews, 6 (2009), 267-310.
doi: 10.1016/j.plrev.2009.10.002. |
show all references
References:
[1] |
L. Boddy,
Interspecific combative interactions between wood-decaying basidiomycetes, FEMS Microbiology Ecology, 31 (2000), 185-194.
doi: 10.1111/j.1574-6941.2000.tb00683.x. |
[2] |
L. Boddy,
Saprotrophic cord-forming fungi: Meeting the challenge of heterogeneous environments, Mycologia, 91 (1999), 13-32.
doi: 10.2307/3761190. |
[3] |
G. P. Boswell,
Modelling combat strategies in fungal mycelia, Journal of Theoretical Biology, 304 (2012), 226-234.
doi: 10.1016/j.jtbi.2012.03.036. |
[4] |
J. L. Bown, C. J. Sturrock, W. B. Samson, H. J. Staines, J. W. Palfreyman, N. A. White, K. Ritz and J. W. Crawford,
Evidence for emergent behaviour in the community-scale dynamics of a fungal microcosm, Proceedings of the Royal Society B – Biological Sciences, 266 (1999), 1947-1952.
doi: 10.1098/rspb.1999.0871. |
[5] |
R. W. Buchkowski, M. A. Bradford, A. S. Grandy, O. J. Schmitz and W. R. Wieder,
Applying population and community ecology theory to advance understanding of belowground biogeochemistry, Ecology Letters, 20 (2017), 231-245.
doi: 10.1111/ele.12712. |
[6] |
I. H. Chapela, L. Boddy and A. D. M. Rayner,
Structure and development of fungal communities in beech logs four and a half years after felling, FEMS Microbiology Ecology, 53 (1988), 59-69.
doi: 10.1111/j.1574-6968.1988.tb02648.x. |
[7] |
M. J. A. Choudhury, P. M. Trevelyan and G. P. Boswell,
A mathematical model of nutrient influence on fungal competition, Journal of Theoretical Biology, 438 (2018), 9-20.
doi: 10.1016/j.jtbi.2017.11.006. |
[8] |
D. Coates and A. D. M. Rayner,
Fungal population and community development in cut beech logs. Ⅲ. Spatial dynamics, interactions and strategies, New Phytologist, 101 (1985), 183-198.
doi: 10.1111/j.1469-8137.1985.tb02825.x. |
[9] |
F. A. Davidson, B. D. Sleeman, A. D. M. Rayner, J. W. Crawford and K. Ritz,
Context-dependent macroscopic patterns in growing and interacting mycelial networks, Proceedings of the Royal Society B – Biological Sciences, 263 (1996), 873-880.
doi: 10.1098/rspb.1996.0129. |
[10] |
R. E. Falconer, J. L. Bown, N. A. White and J. W. Crawford,
Modelling interactions in fungi, Journal of the Royal Society Interface, 5 (2008), 603-615.
doi: 10.1098/rsif.2007.1210. |
[11] |
M. D. Fricker, L. L. M. Heaton, N. S. Jones and L. Boddy,
The mycelium as a network, Microbiology Spectrum, 5 (2017), 1-32.
doi: 10.1128/microbiolspec.FUNK-0033-2017. |
[12] |
J. M. Halley, H. N. Comins, J. H. Lawton and M. P. Hassell,
Competition, succession and pattern in fungal communities: Towards a cellular automaton model, Oikos, 70 (1994), 435-442.
doi: 10.2307/3545783. |
[13] |
J. Hiscox and L. Boddy,
Armed and dangerous – chemical warfare in wood decay communities, Fungal Biology Reviews, 31 (2017), 169-184.
doi: 10.1016/j.fbr.2017.07.001. |
[14] |
J. Hiscox, M. Savoury, I. P. Vaughan, C. T. Müller and L. Boddy,
Antagonistic fungal interactions influence carbon dioxide evolution from decomposing wood, Fungal Ecology, 14 (2015), 24-32.
doi: 10.1016/j.funeco.2014.11.001. |
[15] |
L. Holmer and J. Stenlid,
The importance of inoculum size for the competitive ability of wood decomposing fungi, FEMS Microbiology Ecology, 12 (1993), 169-176.
doi: 10.1111/j.1574-6941.1993.tb00029.x. |
[16] |
P. Kennedy,
Ectomycorrhizal fungi and interspecific competition: Species interactions, community structure, coexistence mechanisms, and future research directions, New Phytologist, 187 (2010), 895-910.
doi: 10.1111/j.1469-8137.2010.03399.x. |
[17] |
D. A. Kolesidis, L. Boddy, D. C. Eastwood, C. Yuan and M. S. Fowler,
Predicting fungal community dynamics driven by competition for space, Fungal Ecology, 41 (2019), 13-22.
doi: 10.1016/j.funeco.2019.04.003. |
[18] |
K. L. McGuire and K. K. Treseder,
Microbial communities and their relevance for ecosystem models: Decomposition as a case study, Soil Biology and Biochemistry, 42 (2010), 529-535.
doi: 10.1016/j.soilbio.2009.11.016. |
[19] |
H. V. Moeller and K. G. Peay, Competition-function tradeoffs in ectomycorrhizal fungi, PeerJ, 4 (2016), e2270.
doi: 10.7717/peerj.2270. |
[20] |
J. Oliva, M. Messal, L. Wendt and M. Elfstrand,
Quantitative interactions between the biocontrol fungus Phlebiopsis gigantea, the forest pathogen Heterobasidion annosum and the fungal community inhabiting Norway spruce stumps, Forest Ecology and Management, 402 (2017), 253-264.
doi: 10.1016/j.foreco.2017.07.046. |
[21] |
N. J. B. Plomley,
Formation of the colony in the fungus Chaetomium, Australian Journal of Biological Sciences, 12 (1959), 53-64.
doi: 10.1071/BI9590053. |
[22] |
J. I. Prosser, N. A. R. Gow and G. M. Gadd (eds.), Kinetics of filamentous growth and branching, in The Growing Fungus, Springer, Dordrecht, (1995), 301–318.
doi: 10.1007/978-0-585-27576-5_14. |
[23] |
J. I. Prosser and A. P. J. Trinci,
A model for hyphal growth and branching, Microbiology, 111 (1979), 153-164.
doi: 10.1099/00221287-111-1-153. |
[24] |
W. S. Rasband, ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, available from: https://imagej.nih.gov/ij/ (cited 17 Dec 2018). Google Scholar |
[25] |
T. Stella, S. Covino, M. Čvančarová, A. Filipová, M. Petruccioli, A. D'Annibale and T. Cajthaml,
Bioremediation of long-term PCB-contaminated soil by white-rot fungi, Journal of Hazardous Materials, 324 (2017), 701-710.
doi: 10.1016/j.jhazmat.2016.11.044. |
[26] |
W. Thompson and A. D. M. Rayner,
Extent, development and function of mycelial cord systems in soil, Transactions of the British Mycological Society, 81 (1983), 333-345.
doi: 10.1016/S0007-1536(83)80085-0. |
[27] |
R. Toral and P. Colet, Introduction to master equations, in Stochastic Numerical Methods: An Introduction for Students and Scientists, Wiley-VCH, Weinheim, (2014), 235–260.
doi: 10.1002/9783527683147.ch8. |
[28] |
A. van der Wal, T. D. Geydan, T. W. Kuyper and W. de Boer,
A thready affair: Linking fungal diversity and community dynamics to terrestrial decomposition processes, FEMS Microbiology Reviews, 37 (2013), 477-494.
doi: 10.1111/1574-6976.12001. |
[29] |
V. Volpert and S. Petrovskii,
Reaction–diffusion waves in biology, Physics of Life Reviews, 6 (2009), 267-310.
doi: 10.1016/j.plrev.2009.10.002. |




Model | Advantages | Disadvantages | Predictability |
ODE | 1. Simplicity | 1. Non-spatial | 1. Low for even one-species |
2. Determinism | |||
3. Math. liability | |||
PDE | 1. Spatial | 1. Arbitrary mycelial presence (density threshold) 2. Challenging set-up of exact initial conditions 3. Challenging measurement-parameterisation 4. Cannot model each mycelium separately |
1. High for one-species 2. Low for three-species |
2. Determinism | |||
3. Math. liability |
Model | Advantages | Disadvantages | Predictability |
ODE | 1. Simplicity | 1. Non-spatial | 1. Low for even one-species |
2. Determinism | |||
3. Math. liability | |||
PDE | 1. Spatial | 1. Arbitrary mycelial presence (density threshold) 2. Challenging set-up of exact initial conditions 3. Challenging measurement-parameterisation 4. Cannot model each mycelium separately |
1. High for one-species 2. Low for three-species |
2. Determinism | |||
3. Math. liability |
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