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Earthworms and humus forms

Renée-Claire Le Bayon, Jean-François Ponge, Augusto Zanella

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Renée-Claire Le Bayon, Jean-François Ponge, Augusto Zanella. Earthworms and humus forms. Yahya Kooch, Yakov Kuzyakov. Earthworms and ecological processes, Springer Nature Switzerland, pp.189-217, 2024, 978-3-031-64509-9. 10.1007/978-3-031-64510-5_6. hal-04791232

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Submitted on 19 Nov 2024

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# Chapter 4: Earthworms and humus forms

Renée-Claire Le Bayon<fnref n="1" />, Jean-François Ponge<fnref n="2" /> and Augusto Zanella<fnref n="3" />

## 1. Exploring the underground

The world's population reached a record 8 billion people on 15 November 2022, according to the Department of Economic and Social Affairs of the United Nations (2022). Human population growth impacts the Earth's system in various ways, including the extraction of natural resources such as fossil fuels, minerals, trees, water, and wildlife. Moreover, more than half of the world's population now lives in urban areas (Ritchie and Roser 2018), and urbanisation is still in expansion. Such increased pressures endanger maintaining and expanding essential ecosystem benefits and services required for human livelihood (Larondelle et al. 2014). These latter are commonly defined as the "benefits people obtain from the ecosphere and its ecosystems" (Millennium Ecosystem Assessment 2005) and listed into four broad categories: provisioning, regulating, cultural and supporting services (Dominati et al. 2010). To preserve as best as possible ecosystems' services, the conservation and management of ecosystems appear crucial because this approach considers entire communities of species and their interactions with the physical environment.

Usually, the most common and easiest way to understand terrestrial ecosystems is to study vegetation... provided you know botany and phytosociology! Vegetation relevés allow the establishment and monitoring of plant communities' structure and composition using a percentage cover of species in each layer of phytocenosis (Braun-Blanquet's scale). This approach is beneficial for preserving and predicting the ecosystems' evolution due, for instance, to anthropic impacts such as climate change. To complement this descriptive vision, energy, water, and nutrient fluxes provide a functional approach to ecosystems. However, more than staying at the level of the upper part of plants is required: we need to follow the plants' dark side underground, which means their roots. This guides us to the most concealed part of the ecosystem, the underground black box and perhaps one of the last final frontiers of the research and knowledge: the soil (see the review in Science, Sugden et al. 2004).

As a three-dimensional effective, almost non-renewable system, soils represent the primary living matrix for many ecosystems and human activities (Dominati et al. 2010; Adhikari and Hartemink 2016; Blanchart et al. 2018; Sofo et al. 2022). They play a central role in global biogeochemical cycles and host the most extensive diversity of organisms (Smith et al. 2015). Among these organisms, plants and invertebrates are essential components of soil genesis, functions and properties. Their engineering activities mainly occur in the so-called "humipedon", corresponding to the upper soil layers particularly enriched in organic matter, which are the core of the interactions between vegetation and soil (Zanella et al. 2018a; Zanella et al. 2018b). The activity of soil organisms is exceptionally high in humipedons and intensely involved in organic matter recycling and provisioning, as well as biogenic structures such as burrows, pellets and aggregates. Earthworms and plant roots mainly govern these latter: as allogenic engineers, they are responsible for physical modifications but may also be involved in biological and

<footnote n="1">¹Université de Neuchâtel, Laboratoire d'Ecologie Fonctionnelle, Rue Emile Argand 11, 2000 Neuchâtel, Suisse</footnote>

<footnote n="2">²Museum National d'Histoire Naturelle, CNRS UMR 7179, 4 avenue du Petit Château, 91800 Brunoy, France</footnote>

<footnote n="3">³Department TESAF, University of Padua, Italy</footnote>
biochemical processes. In temperate ecosystems, they are thus the leading soil engineers creating
habitats for other organisms, such as small arthropods like springtails or mites (Eisenhauer 2010;
Cameron et al. 2013; Liu et al. 2013). Both plants and earthworms also produce chemical substances,
exudates (Bais et al. 2006) and mucus, respectively (Salmon 2001), which are enriched in water, carbon
(C) and nitrogen (N). Plant roots interact with earthworms, and their concomitant activity increases
aggregate stability (Fonte et al. 2012; Schomburg et al. 2018a; Schomburg et al. 2018b). The critical
zone where most chemical, physical and biological processes occur is the humipedon (Figure 1).

<figure><img src="image_2.png" /><figcaption>**Figure 1.** The humipedon is crucial in ecosystem services as it interfaces between vegetation and mineral soil layers. This is especially the case for the carbon cycle, the hosting of biodiversity, and the regulation of water and biomass production at the ecosystem level. The humipedon has its spatiotemporal scale of functioning. Adapted from Adhikari and Hartemink (2016).</figcaption></figure>

**2. Humipedon, humus systems, humus forms: what are we talking about**

**2.1 Vocabulary**

Since Zanella et al. (Zanella et al. 2018e), the "humipedon" represents the surface organic (O, H) and organo-mineral (A) soil layers, thus avoiding confusion with previous "topsoil", "humus" or "forest humus" definitions. In terrestrial ecosystems, the humipedon organises into five humus systems: Mull, Moder, Mor, Amphi and Tangel, which can be eventually submerged a few days per year.

Humus systems differ by morpho-functional humus *diagnostic horizons* and are generated by specific
groups of organisms. In each Humus system, the thickness of diagnostic horizons defines some (3-4)
similar *"Humus forms"*.

The humipedon is made up of organic horizons (O = organic; OL = litter; OF = fragmented/fermented litter; OH = humic = transformed in rather organic minute droppings, small particle litter) and of organo-mineral A horizon (organic derivate integrated within a mineral layer). These horizons are placed on top
of each other: OL at the surface, then OF, and OH, on A at the bottom of the humipedon. The OL layer is composed of recognisable leaves at different decomposition stages. The OF layer consists mainly of fragmented debris, and the OH layer contains a majority of holorganic droppings.

It is relatively easy to distinguish three zoogenic and one non-zoogenic types of organo-mineral A horizon:

1. Biomacrostructured A horizon (code: maA): at least 1/3 of the volume made by large (> 4 mm) organo-mineral biogenic aggregates; origin: anecic or endogeic earthworms, microorganisms.

2. Biomicrostructured A horizon (code: miA): at least 2/3 of the volume made by small (≤ 1mm) organic or organo-mineral faecal pellets; origin: arthropods, enchytraeids, microorganisms.

3. Biomesostructured A horizon (code meA): zoogenic horizon, not maA, not miA; origin: anecic or endogeic earthworms, microorganisms, insect larvae and large arthropods may also intervene in the Mediterranean environment. The appearance is that of a finer and very amalgamated maA aggregates.

4. Non-zoogenic A horizon: massive (code: msA = like clay organo-mineral blocky horizon) or single grain (code: sgA = sandy organo-mineral horizon, organic pellets ≤ 10%); origin: rather due to chemical-physical reactions, water transport of molecules and minerals, microorganisms may play an unknown role too.

For more information on diagnostic horizons and graphical illustrations, refer to (Zanella et al. 2018f)

**Table 1** is a revisited version of the synthesis made by Ponge (Ponge 2003), which has been completed with Tangel and Amphi systems. From Tangel to Mor systems, a gradient of variations occurs, especially regarding the horizon sequences relative to the activity of soil organisms. The ecosystems and soil types differ and, consequently, the recycling of organic matter and nutrient availability. At a finer level, in each humus system, diagnostic horizons' presence and thickness define several humus forms, differing slightly in between (i.e., Eumull, Mesomull, Oligomull, Dysmull; (Zanella et al. 2018g).
<table><caption>**Table 1.** Main biological features of the five humus systems at the ecosystem level. Adapted and revised from Ponge (2003).</caption><thead><tr><th></th><th>TANGEL</th><th>AMPHI</th><th>MULL</th><th>MODER</th><th>MOR</th></tr></thead><tbody><tr><th>Ecosystems</th><td>Grasslands, coniferous woodlands, alpine meadows, cold and humid conditions</td><td>Deciduous and coniferous woodlands, transitional ecosystems such as abandoned pastures</td><td>Grasslands, deciduous woodlands with rich herb layer, Mediterranean scrublands</td><td>Deciduous and coniferous woodlands with poor herb layer</td><td>Heathlands, coniferous woodlands, sphagnum bogs, alpine meadows</td></tr><tr><th>Biodiversity</th><td>Medium</td><td>High in the A, low in O layers</td><td>High</td><td>Medium</td><td>Low</td></tr><tr><th>Productivity</th><td>Medium</td><td>Medium to high</td><td>High</td><td>Medium</td><td>Medium to low, adapted to acidophilic species</td></tr><tr><th>Litter horizons</th><td>OL, OF, OH</td><td>OL, OF, OH</td><td>OL, OF</td><td>OL, OF, OH</td><td>OL, OF, OH</td></tr><tr><th>Organo-mineral horizon</th><td>nozA, meA</td><td>miA, meA, maA</td><td>meA, maA</td><td>meA, miA</td><td>When present, nozA</td></tr><tr><th>Soil type</th><td>Holorganic soils, humo-calcic soils</td><td>Brown calcic soils</td><td>Brown soils</td><td>Grey-brown podzolic soils</td><td>Leached brown soils to podzols</td></tr><tr><th>Phenolic content of litter</th><td>Medium to high</td><td>Medium</td><td>Poor</td><td>Medium</td><td>High</td></tr><tr><th>Humification</th><td>Slow</td><td>Slow to medium</td><td>Rapid</td><td>Slow</td><td>Very slow</td></tr><tr><th>Humified organic matter</th><td>Slow but continuous degradation of plant debris</td><td>Holorganic faecal pellets in the O horizons, organo-mineral aggregates in the A horizon</td><td>Organo-mineral aggregates with clay-humus complexes</td><td>Holorganic faecal pellets</td><td>Slow oxidation of plant debris</td></tr></tbody></table>
<table><thead><tr><th></th><th>TANGEL</th><th>AMPHI</th><th>MULL</th><th>MODER</th><th>MOR</th></tr></thead><tbody><tr><th>Exchange sites</th><td>Organic (rich near the rock)</td><td>Organic (rich) to mineral</td><td>Mineral</td><td>Organic (rich)</td><td>Organic (poor)</td></tr><tr><th>Mineral weathering</th><td>Poor, except in the vicinity of the rock</td><td>Medium to high</td><td>High</td><td>Medium</td><td>Poor</td></tr><tr><th>Mineral buffer type</th><td>Carbonate range</td><td>Carbonate to silicate</td><td>Carbonate to silicate range</td><td>Silicate range</td><td>Iron/aluminium range</td></tr><tr><th>Impact of fire</th><td>High</td><td>Medium to high</td><td>Low (except in Mediterranean ecosystems)</td><td>Medium</td><td>High</td></tr><tr><th>Regeneration of trees</th><td>Poor</td><td>Medium, depending on A type (mA to meA)</td><td>Easy (permanent)</td><td>Poor (cyclic processes)</td><td>Young trees may develop on local degrading stumps or surface-stripped soils</td></tr><tr><th>Dominant mycorrhizal types</th><td>Ectomycorrhizae</td><td>VA-mycorrhizae to ectomycorrhizae</td><td>VA-mycorrhizae</td><td>Ectomycorrhizae</td><td>Ericoid and arbutoid mycorrhizae</td></tr><tr><th>Mycorrhizal partners</th><td>Unknown</td><td>Basidiomycetes</td><td>Zygomycetes</td><td>Basidiomycetes</td><td>Ascomycetes</td></tr><tr><th>Nitrogen forms</th><td>Protein</td><td>Protein, ammonium, nitrate</td><td>Protein, ammonium, nitrate</td><td>Protein, ammonium</td><td>Protein</td></tr><tr><th>Nutrient availability to plants</th><td>Direct from the OH horizon</td><td>Direct to indirect</td><td>Direct (through absorbing hairs)</td><td>Indirect (through extramatrical mycelium)</td><td>Poor</td></tr><tr><th>Nutrient use efficiency</th><td>Low to medium</td><td>Medium to high</td><td>Low</td><td>Medium</td><td>High</td></tr></tbody></table>
<table><thead><tr><th></th><th>TANGEL</th><th>AMPHI</th><th>MULL</th><th>MODER</th><th>MOR</th></tr></thead><tbody><tr><th>Fauna</th><td>Mesofauna (high), microfauna (high)</td><td>Macrofauna in the A horizon, mesofauna and microfauna in O horizons</td><td>Megafauna, macrofauna, mesofauna, microfauna</td><td>Macrofauna (poor), mesofauna (rich), microfauna</td><td>Mesofauna (poor), microfauna (poor)</td></tr><tr><th>Earthworms: main ecological categories</th><td>Epigeics, some endogeics</td><td>Epigeics, endogeics, anecics</td><td>Endogeics and anecics</td><td>Epigeic, some endogeics</td><td>Some epigeics in thin mors</td></tr><tr><th>Faunal group dominant in biomass</th><td>Mites, springtails, a few earthworms, enchytraeids</td><td>Endogeic earthworms in the A horizon, macro- and microarthropods, epigeic earthworms and enchytraeids in O horizons</td><td>Earthworms</td><td>Enchytraeids, a few earthworms</td><td>Mites, springtails</td></tr><tr><th>Microbial group dominant in biomass</th><td>Fungi</td><td>Bacteria and Fungi</td><td>Bacteria</td><td>Fungi and bacteria</td><td>Fungi</td></tr><tr><th>Affinities with polluted condition</th><td>Low</td><td>Low</td><td>Low</td><td>Medium</td><td>High</td></tr></tbody></table>
In addition to plant roots, soil fauna and microorganisms (bacteria, fungi) are intensely involved and often used to discriminate the humus system at the inter- and intra-level. The same occurs for Arthropods: while springtails and mites are the most common arthropods in the humipedon, enchytraeids and earthworms are the most efficient in organic matter recycling bioturbation processes, respectively (Table 1). In addition, arthropods and enchytraeids mainly live in O layers, while earthworms can live in soil surface layers or more profoundly. Figure 2 is an updated version of Zanella et al. (Zanella et al. 2018c) an extension of the presence of earthworms to a broader range of humus forms. New in situ observations revealed that epigeics are mostly ubiquitous in humus systems, while anecics range from Eumesoamphi to Eumoder.

<figure><img src="image_3.png" /></figure>

**Figure 2.** An updated version of the simplified scheme of Terrestrial humus systems classification (updated, from Zanella et al. 2018c). The scheme shows the main climatic and parent material determinants (top of the picture), diagnostic horizons (middle) and biological actors of organic matter transformation (bottom). OL, OF, nozOF, OH, mA, miA, nozA: diagnostic horizons described in Zanella et al. (Zanella et al. 2018f) transition between OH and A horizons: dashed line = gradual, continuous line= sharp; A horizon aggregates: two lines = non zoogenic; small black circles = biomicrostructured; white small circles = biomesostructured; large white circles = biomacrostructured; lithopedon: bricks = base-rich substrate, + = base-poor substrate; Pachy: thick, Eu: typical; Dys: acid; Humi: rich in undecayed organic matter; Eumacro and Eumeso: large or medium biogenic structures in the A horizon. Humps and troughs of the continuous blue line refer to the hypothesis of humus systems as ecological attractors, with Mull as the "final" attractor.

## 2.2 The Amphi system: a historical overview

The introduction of Amphi forms in the classification of humus forms results from field observations and discussions within a consortium of researchers over the last two decades, as briefly described below.
In 1882, Peter Erasmus Müller (Müller 1887) described two humus forms in Germany: Mull (made by earthworms) and Torf (made by arthropods). In 1970, in the Austrian and Italian Alps, Franz Hartmann (Hartmann 1970) discovered that these two humus forms might overlap in what he called "Humus gemellare", literally "Twin humus". This system was composed of a grey-brown organic-mineral layer made of large earthworms' dejections, overlapped by an organic black layer made of small aggregates generated by arthropods.

In 1995, Brêthes et al. (Brêthes et al. 1995) set a similar humus form in their classification system; they called it "Amphimull" ("double Mull") and placed it in the Mull system. In 1996, Calabrese et al. (1996) revealed that such "twin humus" was relatively common in beech forests and Mediterranean ecosystems. This "Amphimull" evolved into "Amphimus" in 2009 (Jabiol et al., in Baize and Girard 2009), showing the importance of discriminating this system from the Mull one and the specificity of this particular humus form.

In 2003, 26 soil specialists met in Trento (Italy) and founded a Humus Group. After three years of exchanges, the Humus Group presented a poster at the World Congress of Soil Science in Philadelphia (USA, 2006) on which the Amphi reference was displayed aside from the well-known ones of Mull, Moder and Mor (Figure 3). To provide a complete and updated framework in this chapter dedicated to earthworms, in Figure 3, we add the Tangel system (bottom, in orange), which was not present on the drawing presented in Philadelphia because considered only in 2018.

<figure><img src="image_4.png" /><figcaption>**Figure 3.** Humus forms: integration of living ecosystems. Poster presented at the 18th World Congress of Soil Science at Philadelphia in July 2006, modified. Mull, Moder, Mor, Amphi and Tangel "humus form references" (corresponding to modern "humus systems") were represented as evolutionary holes in which the humipedon ecosystems fall driven by climatic, geological and vegetational relationships and constraints. In 2006, the Amphi "hole" was filled with two humus forms: Euamphi and Dysamphi. Since 2018, they</figcaption></figure>
became four: Leptoamphi, Eumacroamphi, Eumesoamphi and Pachyamphi. Moder did not change; Mor got a third Humimor form in 2018. In 2018, a Tangel fifth hole was added at the bottom of the picture, touching Amphi, Moder and Mor. This supplementary humus system, mostly generated by arthropods in calcareous or dolomitic high mountain environments, was first described by Walter Kubiëna in 1953 (Kubiëna 1953).

The group of *epigeic* earthworms has a habitat relegated to organic horizons (vOL, zoOF, zoOH; v = verbleit, bleached, old and packed litter; zo = zoogenic, with evident signs of the presence of animals that feed on litter, such as holes, bites, droppings ...). The epigeic earthworms produce small organic droppings (OC > 20% by weight, measured with the elemental analyzer) that remain in the organic part of the soil profile (Galvan et al. 2008). These earthworms initiate the biotransformation of litter but only indirectly participate in the genesis of organo-mineral aggregates, which are due only to endogeic and anecic groups; they are active in all humus systems presenting zoogenic organic diagnostic horizons, as in Mull, Moder, Amphi and Tangel (absent on Mor).

The *endogeic* group does not inhabit the organic horizons of the profile but prefers the superficial part of the organo-mineral horizon, feeding on organic horizons deposited above their habitat, but creating an organo-mineral horizon composed of their excrements. This also happens in environments of very superficial soils, as long as they are also covered by organic horizons, both in acidic and calcareous environments. The A horizon formed by endogeic earthworms is slightly smaller in size but very similar to that formed by anecic, made up of uniformly amalgamated organo-mineral aggregates (Zanella et al. 2018f). A transitional form of humus between Mull and Moder has been described, called Hemimoder (literally Half Moder). In it the OH horizon is discontinuous. This means that juxtaposed surfaces with and without OH are observed in the field. On a more detailed scale, these are the Mull (without OH) and Moder (with OH) systems that developed in mosaic. Endogenous earthworms have been found in these areas. They would eat up the OH horizon and turn some of the area that was in Moder to Mull. This group may be present in the organo-mineral part of a Hemimoder but not on typical Moder; never present in a Mor system.

The *aneic* earthworms occupy a key place in the functioning of the Mull and Amphi systems. They form organo-mineral aggregates that make up the A horizon (fundamental matrix for plant nutrition) of all agricultural and forest soils in mild climate areas. Absent Tangel and Mor humus system, the importance of these groups of earthworms in functioning Moder is null or marginal (transitional forms towards Mull or Amphi systems).

### 3. Earthworm engineering: opportunity or threat?

Earthworms are known for a long time for the ecosystem services they provide through their engineering activity: litter decomposition (Bocock 1964), soil structure (Oades 1993), nutrient cycling (Bohlen and Edwards 1995; Edwards and Arancon 2022), among many others, are improved under the influence of their multiple interactions with plants, microbes and other soil fauna (Brown et al. 2000), stemming in the formation of earthworm Mull (Zanella et al. 2018b) Less well-known despite of far-reaching consequences for global warming mitigation is the role played by earthworms in carbon sequestration in Mull humus systems in which organic matter is buried and mixed with mineral particles in physically and chemically stable aggregates (Zhang and Schrader 1993). Although more research on the subject is urgently needed, earthworm (macro-aggregated) Mull and Amphi thereby might contain more organic carbon (although invisible to the naked eye) over their whole thickness and thus might sequester more carbon than Moder or Mor humus systems which visibly accumulate more organic matter at the soil surface (Andreetta et al. 2011; de Nicola et al. 2014). Another example of still poorly known ecosystem services provided by earthworms is the stimulation of forest regeneration through the building of humus forms favourable to tree seedling establishment (Ponge et al. 1998). As a consequence of benefits
provided by earthworm activity, the colonization of earthworm-free land by earthworms has been shown
to favour crop production. Widely reported examples are the colonization of Dutch polders by
indigenous earthworm species and New-Zealand pastures by exotic (European) earthworm species
(Curry and Cotton 1983). In both cases earthworms were considered as an essential tool for the
successful development of agriculture.

However, and quite surprisingly, earthworm processes, e.g. casting deposition, may favour biodiversity
by increasing heterogeneity at the soil surface and creating niches for plants (Milcu et al. 2006) and
animals(Hamilton and Sillman 1989), but these same processes may also degrade the soil by favouring
erosion along slopes (Le Bayon and Binet 1999; Le Bayon et al. 2002) or creating impervious crusts on
the ground (Chauvel et al. 1999). Many reports have been done on detrimental aspects of earthworm
activity. Most threatening is the still incoming invasion of North American biomes by European (several
lumbricid species) and Asian (several pheretimoid species) earthworms introduced in the past by
European settlers (Nuzzo et al. 2009). In US northeastern forests, indigenous earthworm faunas,
restricted to a few species living in their typical thick forest floors, are now outcompeted by invasive
earthworms through changes in humus forms mediated by their mixing and digging activities, even if
some cases of resistance have been observed (Hendrix et al. 2006). Dramatic changes caused by the
establishment of exotic earthworm populations are also visible at the scale of forest vegetation (Hale et
al. 2006). It might even be postulated that in a more or less near future tree populations will be affected,
too, in particular if tree species favoured by Mull for their regeneration outcompete tree species favoured
by Moder or even Mor.

In China, the introduction of the European manure worm *Eisenia fetida*, as yet commonly used for
composting organic wastes, has been suggested as a mean to reclaim soils improper for agriculture
(Zhang et al. 2015). This voluntary introduction, beside the expected development of agriculture, might
have far-reaching detrimental consequences for the conservation of indigenous ecosystems, even if such
deleterious effects are not purported at the beginning.

The main reason for these contrasted aspects of earthworm activity, whether opportunities of threats
according to circumstances, is that earthworms, in particular those species capable of digging the soil
and mixing it with organic matter (i.e. mull-forming species) create disturbances at a scale ranging from
the drilosphere to whole forest or grassland ecosystems. These disturbances propagate themselves
through scales by self-entertained chains of action and reaction, also called positive feedback loops until
some equilibrium is reached and stabilized through negative feedbacks (Jouquet et al. 2006). Here, the
Mull humus system can be considered as the climax, generating by itself the conditions of its own
development, earthworm activity favouring the nutrient-rich vegetation favouring in turn the
development of nutrient-eager earthworm populations (Ponge 2003; Arim et al. 2006). Detrimental
effects of earthworm invasion can be alleviated only by changing the humus form, an unattainable task,
or waiting enough time for a new equilibrium once the spread of invaders arrives to completion (Arim
et al. 2006).

4. Let's go to the field

Depending on the environment in which they form, there are different types of O and A horizons. In a
mesophilic environment (plains, low mountains, rainy tropical), the O horizon last very little (animals
eat them quickly); the OH horizon is rarely present. An earthworm biomacrostructured A horizon
develops. This humipedon is said to belong to a Mull system. Anecic and endogeic earthworms make
the whole A horizon of Mull and Amphi humipedons. When all organic horizons have been integrated
in the A horizon, these animals eat their own matured in the soil droppings, living on the stock of organic
molecules they previously set into the soil. In doing so, they function as natural refills of the soil,
preventing it from being stripped and returning to an inert earth phase (Bouché 2014). It is known that
the intense exploitation of agricultural soils produces the joint loss of organic carbon and earthworm population (Pelosi et al. 2014).

## 4.1 Earthworms' horizons in grassland and forest ecosystems

Pedoclimatic conditions (temperature, humidity, acidity) regulate biological activities, especially for earthworms that are active most of the time in Spring and Autumn. Depending on the environment they form, there are thus different O and A horizons.

In a mesophilic environment (plains, hills, rainy tropical environments), the O horizon disappears quickly, the organic matter being swiftly decomposed by organisms. Moreover, the OH horizon is rare, and an earthworm biomacrostructured A horizon usually develops. The resulting humipedon ranges in the Mull system with anecic and endogeic earthworms as the main ones responsible for the A layer formation. Humus forms, following a transition from mesophilic to aridic or colder conditions, may progressively be a Eumull (OL/maA), Mesomull (OL/(vOL)/maA; vOL being an old, whitish litter; brackets mean a discontinuous layer), Oligomull (OL/(OF)/meA), and Dysmull (OL/OF/meA) (Figure 5).

<figure><img src="image_5.png" /><figcaption>**Figure 5.** Pictures from two permanent grasslands and beach forests in Switzerland. A sequence in a Mull system, from the best integration of organic matter to the lowest one: Eumull, Mesomull, Oligomull, Dysmull.</figcaption></figure>

Going from mesophilic (warm and humid climate) towards conditions less favorable to anecic and endogeic earthworms (drought, low temperature, acidity) we progressively encounter Eumull: OL, maA; Mesomull: OL, (vOL), maA; vOL is an old, whitish litter: in brackets it means that it is a discontinuous layer; Oligomull: OL, (OF), meA; Dysmull: OL, OF continuous, and meA.

If the climatic conditions become even more difficult, the genesis of humipedon knows a bifurcation:

1) on a basic substrate the evolution goes towards an Amphi system (Figure 6, right). Compared to a Mull (Figure 6, left), anecic and endogeic earthworms are living deeper into the soil and cracks of carbonate rock. Progressively, less favorable conditions for anecic and endogeic earthworms lead from Leptoamphi (OH < 1 cm or discontinuous, maA) to Eumacroamphi (OH ≥ 1 cm, maA), Eumesoamphi (OH < 3 cm, meA) and finally to Eupachy amphi (OH ≥ 3 cm, meA).
2) on an acidic substrate the evolution leads to a Moder system. An OH horizon appears above an A horizon no longer made by earthworms (Figure 7, left). The series of horizons of a Moder system is as follows: OL, OF, OH, miA from arthropods or enchytraeds (presence of small lumps, mostly < 1mm), or non-zoogenic sgA or msA. Intergrades towards Amphi system may show the presence of aggregates made by endogeic earthworms. A Mediterranean Amphi, with its typical maA horizon, is displayed (Figure 7, right) as a comparison.

If the situation becomes even more difficult (high cold mountains, coniferous forests) the system moves toward Mor (acidic environment) or Tangel (limestone) systems:

1) on acidic substrate, the sequence is OL, OF, OH, absence of A [the organic horizon lies directly on mineral horizons, generally a E horizon] (Figure 8, left). A true Mor system (with a clear break between organic and mineral horizons, with degradation of the litter due to fungi) is always devoid of any category of earthworms (or other pedofauna);

2) on limestone or dolomitic rock, OL, OF, OH and a sometime a thin clay-humic A in contact with the rock, due to endogeic earthworms' activity or by decarbonatation of the carbonatic rock. Superficial Tangel discovered at high altitude in stone pine forests (> 2000 m) were inhabited by numerous endogeic earthworms (Figure 8, right).

<figure><img src="image_6.png" /><figcaption>**Figure 6.** Mull (left) and Amphi (right) on calcareous substrate. OH horizon is present only in the Amphi humipedon. In the Amphi profile, earthworms are less active at the top, but can refuge in the cracks of the rock during dry periods.</figcaption></figure>
In Mediterranean forests (Sardinia)

<figure><img src="image_7.png" /></figure>

**Figure 7.** Moder (left) and Amphi (right) in Mediterranean ecosystems. Moder generates on acidic substrate, Amphi on calcareous one. Under a black organic OH horizon, a thin (2-4 cm) grey arthropods A horizon characterizes the Moder system; under a brown OH horizon, a thick (> 10 cm) red-brown earthworms A horizon takes place in the Amphi system.

<figure><img src="image_8.png" /></figure>

**Figure 8.** Mor (left) and Tangel (right) systems. The first lies on the acidic sand of Fontainebleau (Parisian region, France); consisting of a pack of dry moss and invaded by yellow fungal hyphae, this environment is not suitable for the development of earthworms. Although at 2000 m, on the slope facing east of the basin of Lake Misurina (Belluno, Alps, Italy), earthworms are instead numerous in the Tangel which develops in the Swiss stone pine forest; the water flows to the bottom and moistens a very organic soil; in the coldest and most unfavorable periods, earthworms are probably able to overwinter in deep shelters among the cracks in the limestone rock.

## 4.2 Pioneer ecosystems: Bryo and Rhizo biological connections

Biotic and abiotic factors condition the formation of the humipedon, review in Zanella et al. (Zanella et al. 2018a). Although at the same altitude, a southern exposure is hotter and drier than a northern one. The micromorphology plays also an important role and greatly influences the amount of water present in the soil. Earthworms in general love aerated soils that are well fed with water. It is very easy to find
earthworms in dried up anmoors, for example. Everyone knows that earthworms are plentiful in ripening manure. Anecic earthworms do not like high C/N litter. Many conifers produce such type of litter. Earthworms are numerous in pioneer environments like Bryo and Rhizo topsoils (Figure 9). These humipedons exist as single system in the high mountains, forming thin layers in contact with the rock; in forest and grasslands at lower altitude they may overlap other systems. They can also be found at low altitudes, in environments of initial soils, including anthropized ones such as t boundary walls, sidewalks edges, house roofs... A Bryo system typically develops under a carpet of mosses or lichens and shows organic horizons due the degradation of the low part of the thin leaved steams of these plants; a Rhizo system takes place under a carpet of grasses and is characterized by the dense intertwining of secondary roots of these plants. In the high mountains these systems form thin humipedons in contact with the rock; at lower altitudes they lie son on other systems (often Moder systems for Bryo, Mull systems for Rhizo), in forest and grasslands as well. Endogeic earthworms are common in Bryo systems under mosses and/or lichens between the organic rests and the fragmented rock (that may be acidic or basic). Epigeic earthworms live in thin Rhizo system at high altitude (2000-2500 m) in dolomitic and calcareous mountains. At lower altitude, numerous endogeic and anecic earthworms are found in more or less humid Rhizo Mull systems all over the world, as explained in Dominguez et al. (2018).

<figure><img src="image_9.png" /><figcaption>**Figure 9.** Top left and right: Rhizo system at 2500 m in calcareous Alpine mountains. The clod appears as it is just detached from the rock and pours out. In it you can see the roots of the plants immersed in a brownish-gray mass (bryAOH) created by the young earthworm captured and set on the hand (don't worry, we released it immediately and put it back under the clod).</figcaption></figure>

Down left and right: Bryo system, on Cambrian acid red Schists. Beneath its surface living layer, this system typically shows an organic horizon of decomposing mosses and/or lichens (bryOF and thin bryOH) which rests on this more or less fragmented rock. In this fractured rock took refuge two epigeic earthworms.
## 4.3 Earthworms and humus forms in alluvial ecosystems

In near-natural floodplains, the high turnover of habitats and ecosystems due to the alluvial dynamics leads to rapid succession and community-assembly changes compared to other ecosystems (Corenblit et al. 2009; Milner and Tockner 2010). The discharge fluctuation, the frequency and intensity of flooding events cause erosion and/or deposition of sediments with a wide texture heterogeneity. The organic matter supply is also highly variable, either from autochthonous or allochthonous origin. Consequently, a wide diversity of soil layers and types occurs. In this context, the animal and plant communities follow topographic gradients where pedological changes occur from months to several hundred years (Petts and Amoros 1996; Gurnell 2007); the parental mineral material plays a crucial role in the formation and evolution of such type of humipedon. A new Para humus system called Litho (from Greek “λίθος”, stone, rock), with a Psammolitho humus form (form “ψάμμος”, sand) are under investigation and their systematic position will soon be clarified and published. In floodplains, most of the humipedons belong to this Litho Para system, especially in the vicinity of the river bed where coarse sediments predominate (Figure 10). As for soils, the variability of terraces' topography is correlated to a gradient of humus forms. A panel of Para systems (the under process Litho, and the well-known Crusto and Bryo (Zanella et al. 2018d) and the current Mull, Moder and Amphi systems coexist in floodplains.

<figure><img src="image_10.png" /></figure>

**Figure 10.** Three soil types along an elevation gradient from the direct vicinity of the Sarine River to the mature forest situated onto a terrace at a distance of 150 m (FR, Grandvillard, Switzerland). Left: willow bushes, Litho (Psammolitho) and Leptosol (Fluvic), with a J horizon (Baize and Girard 2009); middle: alder forest, Eumull and Calcaric Fluvisol; Right: ash and beech mature forest, Oligomull and Fluvic Cambisol. Organic matter and sand particles are first juxtaposed (left), then the integration begins with the formation of aggregates (middle), and finally, resistant and stable aggregates are formed (left). The formation of aggregates and the integration of the organic matter progressively increase under the influence of earthworms. The dominant species of earthworms are : left: *L. rubellus*; middle: *O. tyrtaeum*, *A. rosea*, *A. caliginosa* and *L. terrestris*; right: *L. terrestris*, *A. longa*, *A. nocturna*, *O. cyaneum* and *O. tyrtaeum*.
In this context, earthworms and plant roots are the primary ecosystem engineers that govern the formation of aggregates (Le Bayon et al. 2017; Schomburg et al. 2018b; Schomburg et al. 2018a; Schomburg et al. 2019a; Le Bayon et al. 2021b; Le Bayon et al. 2021a). The earthworm communities' distribution and composition depend on soil organic matter content, soil texture, altitude and flooding characteristics (Emmerling 1995; Salomé et al. 2011). Habitats research projects on earthworm communities in floodplains are few. Most of them were conducted at the hill level and focused on flooded meadows in northern Germany (Plum and Filser 2005), grasslands in river valleys in Estonia (Ivask et al. 2007) or short grass and herbaceous vegetation in the Netherlands (Zorn et al. 2008). In 2013, Le Bayon et al. synthesised several studies on earthworm communities in floodplains along an altitudinal gradient from the hill (350 m) to the alpine level (2300 m). Thus, overall in several Swiss near-natural floodplains, Guenat et al. (1999), Bullinger-Weber et al. (2007, 2012), and Salomé et al. (2011) found 27 species and subspecies from subalpine to hill levels (Table 2). This record corresponds to two-thirds of all inventoried earthworm species and subspecies in Switzerland, confirming that floodplains are among the most diverse terrestrial ecosystems. The earthworm distribution was widely heterogeneous within the same floodplain (Bullinger-Weber et al. 2007) and in the same vegetation unit (Bullinger-Weber et al. 2012). The texture and the organic matter are the main drivers of the presence and activity of earthworms. Epigeics are often associated with coarse sandy texture in contrast to anecics which prefer deep soils and mature forest stages providing the highest carbon content and the finest soil texture (Salomé et al. 2011).

<table><caption>Table 2. Species and sub-species of earthworms recovered in near-natural floodplains in Switzerland at several altitudinal levels. From Le Bayon et al. 2013.</caption><thead><tr><th></th><th></th></tr></thead><tbody><tr><td>Epigeic</td><td></td></tr><tr><td>Bimastos eiseni (Levinsen, 1884)</td><td></td></tr><tr><td>Dendrobaena octaedra (Savigny, 1826)</td><td></td></tr><tr><td>Dendrobaena pygmea cognetti (Michaelsen, 1903)</td><td></td></tr><tr><td>Dendrobaena pygmea pygmea (Savigny, 1826)</td><td></td></tr><tr><td>Dendrodrilus rubidus rubidus (Savigny, 1826)</td><td></td></tr><tr><td>Dendrodrilus subrubicundus (Eisen, 1874)</td><td></td></tr><tr><td>Eiseniella tetraedra tetraedra (Savigny, 1826)</td><td></td></tr><tr><td>Eisenia andrei (Bouché, 1972)</td><td></td></tr><tr><td>Lumbricus castaneus (Savigny, 1826)</td><td></td></tr><tr><td>Lumbricus meliboeus (Rosa, 1884)</td><td></td></tr><tr><td>Lumbricus rubellus (Hoffmeister, 1843)</td><td></td></tr><tr><td>Octodrilus argoviensis (Bretscher, 1899)</td><td></td></tr><tr><td>Anecic</td><td></td></tr><tr><td>Aporrectodea caliginosa nocturna (Evans, 1946)</td><td></td></tr><tr><td>Aporrectodea giardi giardi (Ribaucourt, 1901)</td><td></td></tr><tr><td>Aporrectodea longa longa (Ude, 1885)</td><td></td></tr><tr><td>Aporrectodea longa ripicola (Bouché, 1972)</td><td></td></tr><tr><td>Aporrectodea longa ripicola viridis (Bouché, 1972)</td><td></td></tr><tr><td>Lumbricus terrestris (Linnaeus, 1758)</td><td></td></tr><tr><td>Endogeic</td><td></td></tr><tr><td>Allolobophora chlorotica chlorotica (Savigny, 1826)</td><td></td></tr><tr><td>Aporrectodea caliginosa alternitosa (Bouché, 1972)</td><td></td></tr></tbody></table>
*Aporrectodea caliginosa caliginosa* (Savigny, 1826)

*Aporrectodea handlirschi handlirschi* (Rosa, 1905)

*Aporrectodea icterica icterica* (Savigny, 1826)

*Aporrectodea rosea rosea* (Savigny, 1826)

*Octolasion cyaneum* (Savigny, 1826)

*Octolasion tyrtaeum lacteum* (Oerley, 1885)

*Octolasion tyrtaeum tyrtaeum* (Savigny, 1826)

This enormous diversity and vast abundance of earthworms in floodplains provide ideal conditions to study the very first steps of soil pedogenesis, especially aggregate formation. This is particularly the case in calcareous conditions where the presence of calcium ions enhance the binding of mineral particles to organic matter to form the clay-humus complex. At the hill and the mountain level, near the Thur river and the Sarine River, we studied the implication of vegetation and earthworms on the soil structure in the context of how soils may prevent flood events. As a result, the more the distance and the elevation from the riverbed occur, the more the earthworm activity supplants those of roots, but both of them are still involved in the structuring processes (Bullinger-Weber et al. 2007; Salomé et al. 2011; Bullinger-Weber et al. 2012; Schomburg et al. 2018a). In the presence of coarse sand, plant roots dominate the aggregate building. Still, when the texture becomes finer and in width layers of silt, anecics and endogeics activities contribute primarily to creating aggregates and burrows (Schomburg et al. 2018b; Schomburg et al. 2019a; Schomburg et al. 2019b).

At the mountain level near Grandvillard (altitude: 750 m a.s.l., FR, Switzerland), earthworms are active for more than eight months per year from March to December. The pedoclimatic conditions allow maintain their bioturbation activities: the tree canopy, leaves on the soil surface and the constant humidity in the soil create an ideal habitat for earthworms, which may explain the high diversity and abundance encountered (Figure 11).

<figure><img src="image_11.png" /></figure>
**Figure 11.** Top of the figure, several earthworms recovered in floodplains and belonging to different ecological categories: *L. rubellus* (epigeic), *A. chlorotica* (endogeic), *A. caliginosa* (endogeic), *O. cyaneum* (endogeic), *A. longa* (anecic). Bottom of the figure: earthworm surface casts that may serve as nutrient pools for plants, here a young beech sprout.

These optimal conditions favour the rapid integration of the organic matter and the formation of aggregates. Approximately every two years, we go into the field with students at the same place to monitor the evolution of vegetation, humus forms and soils. In one of our study plots, a permanent soil profile is described as a Calcaric Skeletic Pantofluvic Fluvisol (Geoabruptic) according to the IUSS Working Group WRB (IUSS Working Group WRB 2022), and the humus form is a Eumull (Zanella et al. 2018g). The A layer mainly comprises macroaggregates (mA) formed by earthworms and plant roots. In 2015, a flood occurred, and a sandy deposition of several centimetres was observed on the soil surface (Figure 12, top left). After only a few days, earthworms built up surface casts. In 2016, no trace of the flood was visible anymore, and the thickness of the A has increased by at least 1 cm. In 2020, the mA showed a high density of plant roots highlighting the richness of nutrients and the water supply in this layer due to the intensive earthworm bioturbation activities.

<figure><img src="image_12.png" /></figure>

**Figure 12.** The temporal evolution (2015-2020) of the humipedon is influenced by earthworms and deposits from the Sarine River (FR, Grandvillard, Switzerland). The sediment deposition did not alter the earthworm activity (see the surface cast). The humus form is a Eumull following the key of Zanella et al. (2018). Horizons sequence: [nOL-vOL]/mAca/Dca/IIMca-Dca/IIDca according to Baize and Girard (2009). The soil is a FLUVIOSOL TYPIQUE carbonaté, leptique, polylithique, according to the classification of Baize and Girard (2009), and a Calcaric Skeletic Pantofluvic Fluvisol (Geoabruptic), according to the IUSS Working Group WRB (2022).
The case of the Sarine River highlights how fast the formation of aggregates can be. An organo-mineral layer may be formed in only several years, and the evolution from sandy and silty raw deposits to soil macroaggregates occurs as one moves away from the influence of the river. The very first steps of aggregates' production in such a context are still under research. The X-ray micro-computed tomography helped us to show that the volume ratio of mineral grains within the aggregates is significantly different according to earthworm species (Le Bayon et al. 2021). The organic matter can also be discriminated, and we showed in controlled mesocosms that plant roots could develop in sandy layers. In contrast, earthworms preferentially selected the organic matter and the silt layers (Schomburg et al. 2019a).

In floodplains, there is obviously a step between sediment and stable biogenic aggregates. After discussions and debates with soil and humus forms specialists, the J horizon was created in the French classification (Baize and Girard 2009) to describe the initial Fluviosols better (Fluvisols, according to the IUSS Group, 2022). In a J horizon (from French “jeune”, young), biogenic aggregates are absent or very rare (Figure 10). Consequently, we can consider the J horizon as a functional soil layer which usually evolves towards a zoogenic (earthworms) A layer over time (Figure 13).

This is typically the case we observed at the Sarine floodplain with the succession of soils, from the Leptosol (Fluvic) near the river to the Fluvic Cambisol in the mature and climatic forest. As these processes occur in the humipedon, the ultimate frontier would be to integrate this J layer in the classification key of humus forms, using a specific codification for the aggregates (jA in Psammolitho ?). This would be very useful to describe better the transition between Parahumus systems and Terrestrial ones in environments containing vast amounts of sand and silt, as in floodplains. Ellen Desie (Desie 2020) encountered the same issue during her fieldwork in Belgium and the Netherlands. She found an accumulation of O layers (OL/OF/OH) directly deposited on sandy mineral layers.

<figure><img src="image_13.png" /></figure>

**Figure 13.** From left to right, progressive colonization by earthworms of the organo-mineral A horizon of a stream bank (Grandvillard, FR, Switzerland). On the left, after the part devoid of earthworms closest to the stream (previously described French J horizon, Figure 10 left), an A horizon still with few aggregates, up to its final form very rich in earthworm aggregates (right).

In less active alluvial ecosystems, earthworms are implied in the formation of the humipedon, but they can be restricted to specific areas due to the permanent presence of water. Near the lake of Neuchâtel (St Blaise, altitude 440 m a.s.l., NE, Switzerland), a transect from the forest to the lake showed the influence of the water table on the vegetation and earthworm communities (Figure 14). In the alluvial forest, all humus forms belong to the Mull system, most of them varying from Eumull to Oligomull.
The biodiversity of earthworms is noticeable, with mainly endogeics and *L. terrestris* as the dominant anecic species. Going towards the lake, the influence of water begins, the presence of *Carex flacca* being an indication. Earthworms are still numerous and active, and their casts can be easily seen in the A layer of the Hydromull. The increasing effect of water limits the presence and activity of earthworms in the third sampling point: *L. rubellus* (a pioneer species) and *O. cyaneum* (known for their affinity with humid soils) are active when the water level gets down due to the fluctuations of the lake, especially in drier periods of the year. Biogenic aggregates compose the An horizon and are especially observable in May and June. In the vicinity of the lake, no earthworms were observed because of the permanent presence of water. Such transects are pedagogic to students (and researchers!) to highlight how necessary humus forms are for explaining the complex relationships between soils and vegetation.

<figure><img src="image_14.png" /><figcaption>**Figure 14.** Transect from the forest to the lake of Neuchâtel showing the humus forms and the horizons sequences, the main earthworm species and the dominant vegetation (St Blaise, NE, Switzerland). The humus forms indicate the progressive influence of the water (total distance: 60 m). The transect was made in the Spring of 2022. Photos credit: Maeder, Bovet, Bulliard and Guerra; scheme: Le Bayon and Semeraro.</figcaption></figure>
5. Earthworm functional domains as extended phenotypes: eco-evolutionary aspects

Earthworms, as soil engineers, transform the soil within their functional domain (Lavelle 2000; Lavelle
2002), also called drilosphere (Brown et al. 2000) or in a few instances vermisphere (Hamilton and
Dindal 1983). They create galleries (Amossé et al. 2015), incorporate organic matter to mineral particles
(Stout and Goh 1980), and modify the composition of microbial (Dempsey et al. 2013), animal (Migge-
Kleian et al. 2006) and plant populations (Hale et al. 2006), favouring or disfavouring species in the
space of soil where they live as multi-species assemblages in spite of intense competition (Decaëns et
al. 2008). As such they can be considered as agents of the building of ecosystems and communities
(Ponge 2021), ensuring multiple ecosystem services far beyond their direct interactions with plants,
animals and microbes (Liu et al. 2019). Here we suggest that the concept of extended composite
phenotypes (Phillips 2009), covering the environmental properties durably modified by an organism,
could be put in synonymy with the functional domain. This has strong consequences for eco-
evolutionary issues (Bailey 2012). Considering the functional domain of an earthworm species as an
extended composite phenotype means it has evolved and may continue to evolve with it.

This is reminiscent of the concept of niche construction (Odling-Smee et al. 2013), meaning that the
niche durably created by an organism (in fact an ecosystem engineer) may, even after its death, be
considered as a driving force of evolution. Like coral reefs of the Jurassic Period, the variety of which
created various calcareous substrates influencing the composition and spatial distribution of present-day
plant communities (Ricci et al. 2018), earthworm activities modify soil properties to an extent that
survive their collapse, and even take part to global climate changes. A good example is the case of
Mollisols (highly fertile soils with a deep homogeneous mineral-organic horizon), which accompanied
the rise of Poaceae in the US Great Plains during the Neogene Period (Retallack 1997) and were thought
to be responsible for further global cooling (Retallack 2013). According to what we can deduct from the
micromorphology of mollic epipedons (Pawluk and Bal 2015), Mollisols (also called Chernozems)
result from the mixing activity of soil engineers, mainly earthworms, although the presence in North
America of digging and burying earthworm species (mostly lumbricids) before the first European
settlements is still a matter of conjecture (Hendrix et al. 2008), contrary to the European framework
(Dreibrodt et al. 2022).

The still postulated (because of the absence of fossils) coevolution of grasses with earthworms is
mirrored in the present-day rich and diversified earthworm populations prevailing in permanent
grasslands (Ponge et al. 2013). The well-known association of earthworms with the Mull humus system
and arthropods with the Moder humus systems, and the paucity of fauna in the Mor humus systems led
Ponge (2003) to hypothesize that these three main terrestrial humus systems were linked by evolutionary
relationships, from Mor (before the rise of arthropods) to Moder (before the rise of terrestrial annelids)
then to Mull. Much more research is needed on the role played by earthworms in the evolution of
terrestrial biomes, like this has been fruitfully done in the coevolution of hosts with their parasites (May
and Anderson 1990) and plants with their pollinators (Kiester et al. 1984). Here the postulated processes
resort to diffuse coevolution (Janzen 1980), including as a phenotypic set of traits the environment
modified by earthworms in addition to signalling strategies (Puga-Freitas and Blouin 2015).
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