[permaculture] Adaptation to life in soil (adapted from a book chapter titled Soil as a habitat by P. Lavelle) - posted by Joel Gruver to the sanet-mg forum.

Lawrence London lfljvenaura at gmail.com
Sun Nov 5 21:26:57 EST 2017

This document is a distillation of ideas from a book chapter titled "Soil
as a habitat" by French soil ecologist Patrick Lavelle.

On Sun, Nov 5, 2017 at 7:54 PM, Lawrence London <lfljvenaura at gmail.com>

> Introduction
> Since the early days of soil science, much has been done to characterize
> soils, including their distribution, properties and response to management.
> Specific investigation of how soil functions as a habitat is a more recent
> emphasis.
> Adaptation to living in soil has generated a wide range of life forms with
> diverse traits. Understanding the challenges experienced by organisms
> living in soil and how organisms have adapted to these challenges is
> critical to understanding opportunities for more ecological soil
> management.
> Major constraints on life in soil
> Soils are compact mixtures of mineral and organic solids interspersed with
> abundant but mostly tiny pores.  Total pore volume is large (30%-60% of
> soil volume) but movement of air, water and organisms is limited by the
> labyrinth-like nature of soil porosity and the fact that only the largest
> soil organisms are strong enough to move soil particles. The small size and
> limited connectivity of pores serves as both an opportunity and obstacle
> for life in soil. Pore space that is theoretically large enough for an
> organism may sometimes be inaccessible or inhospitable due to the
> amphibious (i.e., fluctuating between wet and dry) nature of soils.
> Another major constraint on life in soil is the low-quality of most food
> resources. The main food sources available to heterotrophic soil organisms
> are living biomass, dead but relatively fresh residues and much older and
> high transformed soil organic matter - a very diverse collection of
> materials varying widely in size, chemical composition and complexation
> with soil minerals. Most of these materials are of low nutritive quality
> and difficult to digest as they often combine stoichiometric imbalances and
> high concentrations of compounds that are resistant to enzymes. Leaf and
> root residues often have low resource quality due to secondary metabolites
> that serve as defenses against herbivory. These chemical constraints are
> often exacerbated by isolated distribution and encapsulation within the
> soil matrix.
> Dwelling and moving in soils
> Total soil porosity generally decreases with depth, from porous organic
> rich layers at the surface to increasingly consolidated mineral layers
> below. Structural porosity, i.e., porosity created by physical and
> biological processes, tends to decline with depth while textural porosity,
> the random porosity that naturally separates particles of different sizes
> and shapes becomes dominant. Structural pores tend to be larger, ranging
> from microns to hundreds of microns for large root channels or earthworm
> and termite galleries, while textural pores vary from less than a micron in
> high clay soils to tens of microns in sandy soils. Different methodologies
> are used to assess different pore size classes, and normally only parts of
> the pore size spectrum are considered. Methods of evaluating connectivity
> using modern imaging technologies similar to MRI are becoming available.
> Three classes of soil pores (micro-, meso- and macro-) are defined
> according to their size and the tension required to extract water.
> Micropores are textural pores smaller than 0.15 microns that retain water
> at tensions greater than -1.5 MPa (i.e. beyond the capacity of plants to
> extract water). These pores may comprise a large proportion of the porosity
> in fine textured soils, for example ~1/3 of total porosity in a high clay
> soil vs. almost none in a coarse sandy soil. Mesopores are the smallest
> fraction of structural porosity, ranging from 0.15 to 30 microns. They
> retain plant available water, held at tensions of -0.05 to -1.5 MPa. These
> pores consist of voids between assemblages of silt and sand particles and
> are built by the activities of soil organisms (e.g., channels occupied by
> fine roots, fungal mycelia and bacterial colonies) and by physical
> processes (e.g., cracks). Macropores comprise the structural porosity
> through which water drains, as long as the connectivity of pores allows.
> Crack formation during wet/dry and freeze/thaw cycles is a common process
> that creates macropores but in most soils the majority of macropores are
> the result of bioturbation i.e., the soil moving activities of soil
> ecosystem engineers such as earthworms, termites, ants and plant roots.
> Pore size and connectivity has a large impact on life in soil, since it
> determines the physical domain within which a given organism can move
> without having to move soil. Lack of connectivity is likely a major
> limitation on movement and dispersal of soil organisms. At the same time,
> isolation of populations can protect them from predation and competition
> and favors the vast biodiversity observed in soils.
> Respiration in soils
> During rainfall or irrigation events, soil pores may become completely
> filled with water but gravity quickly empties the macropores where water is
> retained at very low tensions, provided that there is sufficient
> connectivity to allow drainage. Evaporation and transpiration will then
> progressively remove water from mesopores, first the largest and then the
> smaller mesopores. Soil water status can increase quickly driving shifts
> from aerobic to aquatic soil conditions in a few hours but drying processes
> are usually slower. At field capacity, all pores > 10 microns are filled
> with air. At permanent wilting point, water tension is ~ -1.5 MPa and only
> pores < 0.15 microns are still completely filled with water. Soil organisms
> with aquatic respiration are more likely to survive if they are tiny and
> can fit in soil pores that remain filled with water most of the time. At
> field capacity, macropores are air filled and water films are ~10 um thick.
> This condition provides microbes and microfauna with abundant aquatic
> conditions and larger invertebrates with continuous access to moisture and
> air. When plants start to wilt, microorganisms become less active and
> larger organisms suffer water stress.
> Amphibiosis in soils imposes specific constraints on respiration
> physiology. Respiration may be either of an aquatic type, based on the use
> of dissolved oxygen with gill or direct membrane exchanges (e.g. in
> bacteria and earthworms) or of an aerial type involving air circulation
> into trachea or lung-like structures (e.g. arthropods or Gasteropoda).
> Specific physiological and behavioral adaptations allow most soil organisms
> to tolerate wide fluctuations in moisture content.
> Feeding in soils
> In natural ecosystems, ~90% of all primary production returns to soil
> after the death of plants or plant organs. This, however, does not mean
> that it is easy for soil organisms to stay well nourished. Soil food
> resources may be divided into 4 main groups with different factors limiting
> their digestion: 1) Living soil organisms, 2) plant litter (e.g., leaf,
> root, woody) 3) older soil organic matter and 4) soluble resources,
> primarily the exudates and mucus produced by plant roots and earthworms or
> leachates from plant canopies and leaf litter.
> All soil organisms serve as a food resource but bacteria and fungi
> constitute the dominant living biomass in soil and thus are the main food
> resources for soil organisms that consume living biomass. Bacteria are a
> high quality food resource with a low C:N ratio and no cell walls and are
> consumed by many soil organisms. In contrast, fungi have a higher C:N ratio
> and cell walls, and have fewer consumers.
> Plant litter is comprised of dead plant organs deposited at the surface or
> within soil and is a major flow of energy and C into soil. Many types of
> plant litter are not easy to digest because of stoichiometric limitations
> (e.g., high C:N ratio) and the prevalence of polymeric compounds that can
> only be cleaved by specific enzymes.
> Plants generally translocate a large proportion of the nutrients contained
> in leaves before abscission resulting in litter with low nutrients
> concentrations. Litter quality is also impacted by the presence of
> recalcitrant compounds like polyphenols and lignin. Following the death of
> leaves, polyphenols can combine with proteins creating highly resistant
> polyphenol:protein complexes. Polyphenols that are present in the vacuoles
> of living cells combine with cytoplasmic proteins when the tissue dies,
> binding up to 72% of the nitrogen in freshly dead leaves and 85% in roots.
> Efficient release of the nitrogen in these compounds can only be mediated
> by select organisms, principally Basidiomycete fungi known as white rot
> fungi. Bacterial activity in earthworm guts can also degrade
> polyphenol:protein complexes.
> Older soil organic matter (SOM) is the most abundant food resource in
> soil, comprising 20 to >100 Mg/ha distributed within the whole soil profile
> but at decreasing concentrations with depth. Extensive analysis reveals
> that SOM, while abundant, presents its consumers with a number of
> challenges. The most serious being that SOM is dominated by chemically
> recalcitrant compounds that are mostly complexed with clay minerals
> providing additional protection against enzyme attack. SOM is also diluted
> in large volumes of mineral materials that typically represent >> 90% of
> the soil weight. Subsistence on SOM thus requires specific enzymatic
> activities plus the ability to ingest large volumes of soil.
> Soluble resources, the most easily assimilated food resources in soil, are
> comprised mostly of root or mycorrhizal exudates and earthworm mucus, and
> constitute almost 20% of the net C fixed by plants. The main compounds are
> polysaccharides with relatively low molecular weights.
> Although many studies have focused on specific compounds that constitute a
> small fraction of root exudates (e.g., hormones), exudates as a whole,
> represent a substantial readily available C source but do pose some
> challenges for their consumers. Exudates generally are C rich but nutrient
> poor. This forces their consumers to find complementary food resources
> outside the rhizosphere and/or adapt their C metabolism. Exudates are also
> a pulsed resource produced only at specific times.
> Earthworm mucus contains glycoproteins of relatively low molecular weights
> that serve as a lubricant and microbial stimulant. Although the composition
> and quantity of earthworm mucus released into soil has been seldom
> estimated, the stimulating effect on microbial activities in earthworm
> burrows is well documented. Although largely reabsorbed in the posterior
> gut, intestinal mucus represents a rich resource that is used by intestinal
> microorganisms during the transit of soil through earthworms.
> Adaptive strategies of soil organisms
> All soil organisms have adaptive strategies to deal with the constraints
> faced when living in soil but some are better adapted to certain
> constraints than others. This has led to the development of diverse
> interactions between organisms in which complementary adaptive strategies
> are shared. An interesting consequence is that mutualistic and other types
> of non-trophic interactions seem to be more prevalent in soils than other
> ecosystems.
> Digestion and cooperation
> The ability of bacteria and fungi to produce enzymes capable of digesting
> even the most recalcitrant organic compounds is harnessed by larger
> organisms (including plants). The activities of larger organisms in soil
> select and stimulate microbial populations and transport them to new
> environment and substrates.
> There are 3 main types of digestive interactions between microorganisms
> and larger organisms.
> Microbivory is predation on bacteria and fungi and is carried out by a
> wide variety of soil organisms including earthworms but predation by
> microfauna such as protozoa and nematodes is probably most important in
> terms of regulation of microbial populations and the release of the
> nutrients immobilized in microbial biomass. Microbiviory is especially
> intensive in the rhizosphere.
> External rumen (aka exhabitational) digestion occurs when organisms
> create assemblages of plant litter external to their bodies that are
> favorable for microbial/enzyme activity. An important example is when mesofauna
> and some larger arthropods ingest plant litter, excrete largely undigested
> fecal pellets (containing shredded, mixed and moistened litter) and then
> reingest the fecal pellets after an incubation period. The second time
> around, compounds that have been pre-digested by microbial activity are
> assimilated along with potentially some of the microbial biomass. Within
> this general adaptive strategy, a large diversity of behaviours has been
> identified including the assemblage of plant litter in middens and soil
> chambers for later consumption by anecic earthworms.
> Internal rumen digestion occurs when larger organisms have improved
> digestion due to the activity of microorganisms in their digestive tract.
> The microorganisms may be obligate (such as the protozoa contained in the
> posterior pouch of lower termites) or facultative symbionts in the guts of
> earthworms and higher termites. The cellulose digesting enzymes found
> within earthworms are at least partly produced by ingested microorganisms.
> These microorganisms are selectively stimulated in the anterior part of the
> gut where water and intestinal mucus are added and energetic mixing occurs.
> Once the microorganisms are activated, they produce digestive enzymes that
> release substrates that can be assimilated by both the microorganisms and
> the worms.
> Another important form of collaborative nourishment is mycorrhizal fungi
> and host plants trading energy for increased access to soil resources.
> Mycorrhizal hyphae have more absorptive area (as a result of being longer
> and finer) and greater ability to mobilize soil minerals than plant roots.
> Mycorrhizae also help to stabilize soil structure and increase plant
> tolerance of environmental stresses and root pathogens.
> A recently discovered example of collaboration is the horizontal transfer
> of genes that code for digestive enzymes from bacteria to nematodes.
> Molecular methods have shown that plant-feeding nematodes of the sub-order
> Tylenchina contain genes that encode for endoglucanases. Endogluconases are
> cellulose digesting enzymes, a family of enzymes formerly thought to be
> restricted to bacteria. The presence of these and other bacterial genes
> within a nematode genome suggests that horizontal gene transfer has
> occurred between bacteria and nematodes. It also suggests that strategies
> for cooperation between invertebrates and microorganisms may be more
> diverse than currently imagined.
> Movements, habitat building, and bioturbation
> The ability of burrowing organisms (aka soil ecosystem engineers) to move
> and mix soil is essential to the expansion and maintenance of structural
> porosity and to the redistribution and activation of microorganisms. Roots
> perform "biological drilling'', a well-recognized but still poorly
> quantified process, but earthworms are generally considered the most active
> bioturbators, in some cases ingesting and exgesting > 1000 Mg dry soil per
> ha per year and burrowing up to 900 m per m2. Termites and ants are also
> powerful ecosystem engineers that complement or replace earthworm
> activities in some ecosystems.
> Amphibiotic conditions
> Soil organisms have different strategies for surviving extreme
> fluctuations in soil moisture, from cysts and spores to resting stages to
> the construction of protective structures. Tolerance of desiccation
> generally increases as size decreases although some relatively large
> invertebrates, like ants, may survive in extremely dry environments.
> The spatial organization of soil organisms
> The energy collected through photosynthesis and mobilized primarily
> through microbial activity is used by soil ecosystem engineers to build
> distinct habitats that they co-inhabit with many other organisms. An
> important theoretical question is whether by creating these biological hot
> spots, ecosystem engineers actually extend their phenotype and increase
> their fitness or simply have an accidental effect on other organisms.
> Conclusions
> Soils have specific characteristics that create unique challenges for
> their inhabitants. Low food resource quality and spatial/mobility
> constraints have made collaboration between larger and smaller organisms a
> central process. While the physical effects of ecosystem engineers on
> smaller organisms have been intensively explored, the activating effects of
> their energy rich secretions such as root exudates, earthworm mucus and
> termite saliva on the largely dormant microbiota in soil, need more
> comprehensive description and interpretation.
> Perhaps the most practical need is for increased understanding of how
> agricultural management positively and negatively affects soil organisms
> and associated soil processes. Successful long-term conservation oriented
> farming systems (e.g., indigenous farming systems, management intensive
> grazing and continuous no-till grain/cover cropping systems) should be
> intensively studied to identify and interpret interactions between soil
> organisms, soil properties and management practices. In addition, new
> agriculture practices/systems should be designed based on an understanding
> of the importance of collaborative adaptation in soil.
> --
> Lawrence F. London, Jr.
> lfljvenaura at gmail.com
> https://sites.google.com/site/avantgeared

Lawrence F. London, Jr.
lfljvenaura at gmail.com

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