[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 19:54:35 EST 2017


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

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

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

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.


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

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