Interactions between soil animals and ectomycorrhizal fungal mats

doi:10.1016/0167-8809(88)90063-1

Agriculture, Ecosystems & Environment

Volume 24, Issues 1–3, November 1988, Pages 161-168

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Abstract

Estimates of microbial biomass were made for ectomycorrhizal fungal mats colonizing mineral soil in a 50–75-year-old Douglas-fir stand in western Oregon. The ectomycorrhizal fungal mats are from the basidiomycete, Hysterangium setchellii. Numbers and biomass of soil animals including microarthropods and nematodes were estimated for both fungal mat and non-mat areas. The mats generally showed a significantly greater microbial biomass and also greater numbers of soil microarthropods. Protozoans were also sampled and exhibited greater abundance in fungal mats for amoebae and ciliates, but not flagellates. We hypothesize that these mats represent a larger and more active microbial biomass, available as a soil-animal food resource. Fungal mats had greater concentrations of soil C and soil N, and soil respiration and enzyme activity rates were significantly greater in mat than non-mat soil.

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Cited by (45)

Biotic interactions with mycorrhizal systems as extended nutrient acquisition strategies shaping forest soil communities and functions

2021, Basic and Applied Ecology

Citation Excerpt :

The high bacterial to fungal biomass ratio of AM systems as well as less AM protection of roots should promote a higher density of bacterivores (primarily protists and nematodes) and herbivores (root-feeding invertebrates like nematodes), and their subsequent predators and pathogens (Antunes and Koyama, 2017; Persson, Bengtsson, Menge, and Power, 1996). The high fungal biomass of EcM systems should promote a higher density of fungivores (various invertebrates and protists), and their subsequent predators (Antunes and Koyama, 2017; Cromack, Fichter, Moldenke, Entry, and Ingham, 1988; Fitter and Garbaye, 1994). While little is known about the effect of mycorrhizal type on nematode community dynamics, evidence suggests that fungal-feeding nematodes have higher abundances under EcM trees, compared to bacterial-feeding nematodes under AM trees (Cesarz et al., 2013).

Plant nutrient acquisition strategies involving ectomycorrhizal (EcM) and arbuscular mycorrhizal (AM) associations, are key plant functional traits leading to distinct carbon (C) and nutrient dynamics in forests. Yet, little is known about how these strategies influence the structure and functioning of soil communities, and if such mycorrhizal effects may be more or less pronounced depending on the type of forest and various abiotic factors. Here we explore the potential interactions occurring between plant-EcM and plant-AM systems with the diverse soil organisms occurring in forest soils, and in the process draw attention to major issues that are worthy for future research directions. Based on these potential interactions, we suggest that EcM systems, especially those involving gymnosperms in colder climates, may select for a soil community with a narrow set of functions. These EcM systems may exhibit low functional redundancy, dominated by symbiotic interactions, where EcM fungi maintain low pH and high C/N conditions in order to tightly control nutrient cycling and maintain the dominance of EcM trees. By contrast, AM systems, particularly those involving deciduous angiosperm trees in mild and warmer climates, may facilitate a functionally more diverse and redundant soil community tending towards the dominance of competitive and antagonistic interactions, but also with a range of symbiotic interactions that together maintain diverse plant communities. We propose that the contrasting belowground interactions in AM and EcM systems act as extended nutrient acquisition traits that contribute greatly to the prevailing nutrient and C dynamics occurring in these systems.
Does the natural "microcosm" created by Tuber aestivum affect soil microarthropods? A new hypothesis based on Collembola in truffle culture

2014, Applied Soil Ecology

Citation Excerpt :

It is therefore important to investigate not only grazing pressure due to the Collembola but also the effects of other taxa, which are generally less abundant but play an important role in the soil microflora regulation. Therefore, our results only partially confirmed the initial hypothesis that T. aestivum, by altering soil biogeochemistry and vegetation cover, causes differences in soil microarthropod community, as happens with microarthropod communities in ECM-mat soils (Cromack et al., 1988). We did not in fact observe a univocal trend in the T. aestivum brûlés since some microarthropod groups were less abundant in brûlés and others more abundant.

The interactions between fungi and soil fauna are not well known. Some studies suggest that soil microarthropods play an important role in fungi dispersion, but little is still known about the interaction between truffle and soil microarthropods. The aim of this study was to investigate the ability of the truffle Tuber aestivum to modify soil biogeochemistry (i.e. create a zone of scarce vegetation around the host plant, called a burn or brûlé) and to highlight the effects of the brûlé on the soil fauna community. We compared soil microarthropod communities found in the soil inside versus outside the T. aestivum brûlé with the chemistry of soil collected inside versus outside the brûlé. The study was carried out in three Mediterranean areas, two in Italy and one in Spain. The results confirmed the ability of T. aestivum to modify soil biogeochemistry in the brûlé: pH was higher and total organic carbon tended to be lower inside the brûlé compared to outside. Soil fauna communities showed some interesting differences. Some groups, such as Symphyla and Pauropoda, adapted well to the soil; some Collembolan families, and biodiversity and soil quality indices were generally higher outside the brûlé. Folsomia sp. showed higher abundance in the soil of the brûlé compared to outside. The results suggest that some Collembola groups may be attracted by the fungal metabolites produced by T. aestivum, while other Collembola and other microarthropods may find an unfavourable environment in the soil of the brûlé. The next steps will be to confirm this hypothesis and to extend the study to other keys groups such as nematodes and earthworms and to link fluctuations of soil communities with the biological phases of truffle growth.
Microbial Mediation of Plant-Herbivore Ecology

2012, Herbivores: Their Interactions with Secondary Plant Metabolites Ecological and Evolutionary Processes: Second Edition
Ectomycorrhizal mats alter forest soil biogeochemistry

2010, Soil Biology and Biochemistry

Dense hyphal mats formed by ectomycorrhizal (EcM) fungi are prominent features in Douglas-fir forest ecosystems, and have been estimated to cover up to 40% of the soil surface in some forest stands. Two morphotypes of EcM mats have been previously described: rhizomorphic mats, which have thick hyphal rhizomorphs and are found primarily in the organic horizon, and hydrophobic mats, which occur in the mineral horizon and have an ashy appearance. This study surveyed EcM mat and non-mat soils from eight early and late seral conifer forest stands at the H.J. Andrews Experimental Forest in western Oregon. EcM mats were classified by morphology and taxonomic identities were determined by DNA sequencing. A variety of chemical and biochemical properties, including enzymes involved in C, N, and P cycling were measured. Analysis was confined to a comparison of rhizomorphic mats colonizing the organic horizon with non-mat organic soils, and hydrophobic mats with non-mat mineral soils. Both the organic and mineral horizons showed differences between mat and non-mat enzyme profiles when compared on a dry weight basis. In the organic horizon, rhizomorphic mats had greater chitinase activity than non-mat soils; and in the mineral horizon, hydrophobic mats had increased chitinase, phosphatase, and phenoloxidase activity compared to the non-mat soil. The rhizomorphic mats had 2.7 times more oxalate than the non-mats and significantly lower pH. In the mineral horizon, hydrophobic mats had 40 times more oxalate and significantly lower pH than non-mat mineral soils. Microbial biomass C was not significantly different between the rhizomorphic mat and non-mat organic soils. In the mineral horizon, however, the hydrophobic mats had greater microbial biomass C than the non-mat soils. These data demonstrate that soils densely colonized by EcM fungi create a unique soil environment with distinct microbial activities when compared to non-mat forest soils.
Soil life in reconstructed ecosystems: Initial soil food web responses after rebuilding a forest soil profile for a climate change experiment

2010, Applied Soil Ecology

Disrupting ecosystem components, while transferring and reconstructing them for experiments can produce myriad responses. Establishing the extent of these biological responses as the system approaches a new equilibrium allows us more reliably to emulate comparable native systems. That is, the sensitivity of analyzing ecosystem processes in a reconstructed system is improved by excluding the period when observed phenomena are primarily responses caused by establishing the experiment rather than effects of imposed treatments; achieved by determining the extent of any pulse of activity caused by preparatory procedures. A native forest soil was physically disrupted when it was collected, sieved, and then rebuilt in lysimeters in a controlled-environment study evaluating the influence of elevated atmospheric CO₂ concentration and elevated atmospheric temperature on the reconstructed soil that was planted with Douglas-fir (Pseudotsuga menziesii Mirb. Franco) seedlings. Generally, soil food web populations responded in two phases during the exposure as indicated by preliminary evaluation of the 4.5-year dataset. Also, previous work indicated that relatively elevated soil CO₂ effluxes occurred during the first phase, suggesting that food web populations may have responded to carbon sources made available when the soil was harvested and its profile reconstructed in the lysimeters. Results are presented for bacterial and fungal biomass, numbers of protozoa and nematodes to gain insight on whether the first phase responses are attributable to the acute stress of physically disrupting the soil. We found clear relationships between changes in predator and prey populations. A prominent spike for many of the food web populations occurred the year after the climate exposures began. Except for total bacterial biomass and total fungal-hyphae biomass, overall food web responses generally were unrelated to treatments. It appears that initial food web population responses were related to increased availability of soil carbon caused by establishing the experiment. Our results provide insights into determining the length of time to maintain reconstructed forest ecosystems before responses are observed related to experimental treatments. It appears that as long as 3 years elapsed before the soil food web appeared to recover from the acute physical disturbance; 1 year of recovery prior to commencing the climate exposures to allow the soil to rest after it was reconstructed, plus approximately the first 2 years of maintaining the climate treatments. Accounting for consequences of such periods of adjustment is critical for forecasting whether comparable natural ecosystems will be net sources or sinks of elevated concentrations of atmospheric CO₂.
Controlled ectomycorrhization of an exotic legume tree species Acacia holosericea affects the structure of root nodule bacteria community and their symbiotic effectiveness on Faidherbia albida, a native Sahelian Acacia

2009, Soil Biology and Biochemistry

Citation Excerpt :

But, it is also well known that mycorrhizas modify root functions (in particular, root exudation) and, therefore, could modify microbial communities (commonly termed the “mycorrhizosphere effect”) (Katznelson et al., 1962; Linderman, 1988). The development of a number of different organisms is influenced by the mycorrhizosphere effect, for example, protozoa (Jentschke et al., 1995; Wamberg et al., 2003), microarthropods (Cromack et al., 1988), microfungi (Neal et al., 1964) and bacteria (Andrade et al., 1997; Frey-Klett et al., 2005). Surprisingly, the influence of ectomycorrhizal symbiosis on the structure of Bradyrhizobia populations has not been studied in field conditions.

Many fast growing tree species have been introduced to promote biodiversity rehabilitation on degraded tropical lands. Although it has been shown that plant productivity and stability are dependent on the composition and functionalities of soil microbial communities, more particularly on the abundance and diversity of soil symbiotic micro-organisms (mycorrhizal fungi and rhizobia), the impact of tree introduction on soil microbiota has been scarcely studied. This research has been carried in a field plantation of Acacia holosericea (Australian Acacia species) inoculated or not with an ectomycorrhizal fungus isolate, Pisolithus albus IR100. After 7 year's plantation, the diversity and the symbiotic properties of Bradyrhizobia isolated from the plantation soil or from the surrounding area (Faidherbia albida (Del.) a. Chev. parkland) and able to nodulate F. albida, a native Sahelian Acacia species, have been studied. Results clearly showed that A. holosericea modified the structure of Bradyrhizobia populations and their effectiveness on F. albida growth. This negative effect was counterbalanced by the introduction of an ectomycorrhizal fungus, P. albus, on A. holosericea root systems.

In conclusion, this study shows that exotic plant species can drastically affect genotypic and symbiotic effectiveness of native Bradyrhizobia populations that could limit the natural regeneration of endemic plant species such as F. albida. This effect could be counterbalanced by controlled ectomycorrhization with P. albus. These results have to be considered when exotic tree species are used in afforestation programs that target preservation of native plants and soil ecosystem rehabilitation.

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Agriculture, Ecosystems & Environment

Abstract

References (29)

Interactions between bacteria and ectomycorrhizal fungi

Soil Biol. Biochem.

Biological strategies of nutrient cycling in soil systems

Adv. Ecol. Res.

Calcium oxalate accumulation and soil weathering in mats of the hypogeous fungus Hysterangium crassum

Soil Biol. Biochem.

Wetting and drying effects on animal/microbial-mediated nitrogen mineralization and mineral element losses from deciduous forest litter and raw humus

Pedobiologia

The effects of biocidal treatments on metabolism in soil. I. Fumigation with chloroform

Soil Biol. Biochem.

Decomposition of roots

Microbial activities in forest soils colonized by Hysterangium setchellii (Abstract)

Through a ped darkly: an ecological assessment of root-soil-microbial-faunal interactions

Soil nutrient transformations in the rhizosphere via animal-microbial interactions

The Formation of Vegetable Mould through the Action of Worms, with Observations on their Habits

The influence of ectomycorrhizal mats on chemistry of a coniferous forest soil

Spodosol development and nutrient distribution under Hydnaceae fungal mats

Ecological studies of hypogeous fungus. II Sporocarp phenology in a western Oregon Douglas-fir stand

Can. J. Bot.

Fungal and arboreal biomass in a western Oregon Douglas-fir ecosystem: distribution patterns and turnover

Can. J. For. Res.

Cited by (45)

Biotic interactions with mycorrhizal systems as extended nutrient acquisition strategies shaping forest soil communities and functions

Does the natural "microcosm" created by Tuber aestivum affect soil microarthropods? A new hypothesis based on Collembola in truffle culture

Microbial Mediation of Plant-Herbivore Ecology

Ectomycorrhizal mats alter forest soil biogeochemistry

Soil life in reconstructed ecosystems: Initial soil food web responses after rebuilding a forest soil profile for a climate change experiment

Controlled ectomycorrhization of an exotic legume tree species Acacia holosericea affects the structure of root nodule bacteria community and their symbiotic effectiveness on Faidherbia albida, a native Sahelian Acacia

Section 2. Interactions between invertebrates and organisms associated with plant rhizospheres Interactions between soil animals and ectomycorrhizal fungal mats

Abstract

Soil Biol. Biochem.

Adv. Ecol. Res.

Soil Biol. Biochem.

Pedobiologia

Soil Biol. Biochem.

Microbial activities in forest soils colonized by Hysterangium setchellii (Abstract)

Through a ped darkly: an ecological assessment of root-soil-microbial-faunal interactions

Soil nutrient transformations in the rhizosphere via animal-microbial interactions

The Formation of Vegetable Mould through the Action of Worms, with Observations on their Habits

The influence of ectomycorrhizal mats on chemistry of a coniferous forest soil

Spodosol development and nutrient distribution under Hydnaceae fungal mats

Ecological studies of hypogeous fungus. II Sporocarp phenology in a western Oregon Douglas-fir stand

Can. J. Bot.

Fungal and arboreal biomass in a western Oregon Douglas-fir ecosystem: distribution patterns and turnover

Can. J. For. Res.

Section 2. Interactions between invertebrates and organisms associated with plant rhizospheres
Interactions between soil animals and ectomycorrhizal fungal mats