Emergent Behavior of Soil Fungal Dynamics: Influence of Soil Architecture and Water Distribution

Abstract Macroscopic measurements and observations in two-dimensional soil-thin sections indicate that fungal hyphae invade preferentially the larger, air-filled pores in soils. This suggests that the architecture of soils and the microscale distribution of water are likely to influence significantly the dynamics of fungal growth. Unfortunately, techniques are lacking at present to verify this hypothesis experimentally, and as a result, factors that control fungal growth in soils remain poorly understood. Nevertheless, to design appropriate experiments later on, it is useful to indirectly obtain estimates of the effects involved. Such estimates can be obtained via simulation, based on detailed micron-scale X-ray computed tomography information about the soil pore geometry. In this context, this article reports on a series of simulations resulting from the combination of an individual-based fungal growth model, describing in detail the physiological processes involved in fungal growth, and of a Lattice Boltzmann model used to predict the distribution of air-liquid interfaces in soils. Three soil samples with contrasting properties were used as test cases. Several quantitative parameters, including Minkowski functionals, were used to characterize the geometry of pores, air-water interfaces, and fungal hyphae. Simulation results show that the water distribution in the soils is affected more by the pore size distribution than by the porosity of the soils. The presence of water decreased the colonization efficiency of the fungi, as evinced by a decline in the magnitude of all fungal biomass functional measures, in all three samples. The architecture of the soils and water distribution had an effect on the general morphology of the hyphal network, with a “looped” configuration in one soil, due to growing around water droplets. These morphologic differences are satisfactorily discriminated by the Minkowski functionals, applied to the fungal biomass.

[1]  W. Otten,et al.  Effect of bulk density on the spatial organisation of the fungus Rhizoctonia solani in soil. , 2003, FEMS microbiology ecology.

[2]  O. Alizadeh,et al.  Mycorrhizal Symbiosis , 1986, Forest Science.

[3]  Michael F. Allen,et al.  The ecology of mycorrhizae , 1990 .

[4]  M. Ginovart,et al.  Individual-Based Modeling of Carbon and Nitrogen Dynamics in Soils: Parameterization and Sensitivity Analysis of Abiotic Components , 2010 .

[5]  Phil J. Hobbs,et al.  Parasitic plants indirectly regulate below-ground properties in grassland ecosystems , 2006, Nature.

[6]  P. Lavelle,et al.  Soil Ecology , 2001, Springer Netherlands.

[7]  Peihua Qiu,et al.  Statistical Analysis of Microstructures in Materials Science , 2002, Technometrics.

[8]  Michael C. Sukop,et al.  Lattice Boltzmann Modeling: An Introduction for Geoscientists and Engineers , 2005 .

[9]  A. Ashford,et al.  The role of the motile tubular vacuole system in mycorrhizal fungi , 2002, Plant and Soil.

[10]  Shan,et al.  Lattice Boltzmann model for simulating flows with multiple phases and components. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[11]  David L. Hawksworth,et al.  The fungal dimension of biodiversity: magnitude, significance, and conservation , 1991 .

[12]  Chen,et al.  Simulation of multicomponent fluids in complex three-dimensional geometries by the lattice Boltzmann method. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[13]  W. Bowman,et al.  A temporal approach to linking aboveground and belowground ecology. , 2005, Trends in ecology & evolution.

[14]  D. Or,et al.  Invasion percolation of single component, multiphase fluids with lattice Boltzmann models , 2003 .

[15]  R. Falconer,et al.  Biomass recycling and the origin of phenotype in fungal mycelia , 2005, Proceedings of the Royal Society B: Biological Sciences.

[16]  P. Baveye Comment on “Soil structure and management: A review” by C.J. Bronick and R. Lal , 2006 .

[17]  Wei Wang,et al.  Observer-dependent variability of the thresholding step in the quantitative analysis of soil images and X-ray microtomography data , 2010 .

[18]  R. Falconer,et al.  Biomass recycling: a key to efficient foraging by fungal colonies , 2007 .

[19]  W. Otten,et al.  Continuity of air-filled pores and invasion thresholds for a soil-borne fungal plant pathogen, Rhizoctonia solani , 1999 .

[20]  Hans-Jörg Vogel,et al.  Quantification of soil structure based on Minkowski functions , 2010, Comput. Geosci..

[21]  M. Alexander,et al.  MICROBIOLOGICAL CHANGES IN FLOODED SOILS , 1962 .

[22]  N. A. White The importance of wood-decay fungi in forest ecosystems. , 2003 .

[23]  Guido Rademaker,et al.  Detection of soil water in macropores of undisturbed soil using microfocus X-ray tube computerized tomography (μCT) , 2009 .

[24]  W. Otten,et al.  Modelling and quantifying the effect of heterogeneity in soil physical conditions on fungal growth , 2010 .

[25]  J. Farley,et al.  SPECIAL ISSUE: The Dynamics and Value of Ecosystem Services: Integrating Economic and Ecological Perspectives Modeling the dynamics of the integrated earth system and the value of global ecosystem services using the GUMBO model , 2002 .

[26]  Markus Tuller,et al.  Application of Segmentation for Correction of Intensity Bias in X‐Ray Computed Tomography Images , 2010 .

[27]  Veerle Cnudde,et al.  Comparison of different nano- and micro-focus X-ray computed tomography set-ups for the visualization of the soil microstructure and soil organic matter , 2008, Comput. Geosci..

[28]  T. Hattori Soil aggregates as microhabitats of microorganisms , 1988 .

[29]  Philippe C. Baveye,et al.  Comment on “The role of scaling laws in upscaling” by B.D. Wood , 2009 .

[30]  J Letey The study of soil structure - Science or art , 1991 .

[31]  R. Falconer,et al.  Linking individual behaviour to community scale patterns in fungi , 2011 .

[32]  H. Hadwiger Vorlesungen über Inhalt, Oberfläche und Isoperimetrie , 1957 .

[33]  R. Falconer,et al.  Modelling interactions in fungi , 2008, Journal of The Royal Society Interface.

[34]  Hans-Jörg Vogel,et al.  Comparison of a Lattice‐Boltzmann Model, a Full‐Morphology Model, and a Pore Network Model for Determining Capillary Pressure–Saturation Relationships , 2005 .

[35]  David Johnson,et al.  Soil Invertebrates Disrupt Carbon Flow Through Fungal Networks , 2005, Science.

[36]  Paul D. Hallett,et al.  Distribution of soil carbon and microbial biomass in arable soils under different tillage regimes , 2010, Plant and Soil.