# Response to the letter by Xiaoming Zou on
“Earthworms as mutualists rather than predators of soil
microorganisms”

Manuel Blouin, Frédérique Reverchon, Isabelle Barois, Patrick Lavelle

► To cite this version:

Manuel Blouin, Frédérique Reverchon, Isabelle Barois, Patrick Lavelle. Response to the letter by Xiaoming Zou on “Earthworms as mutualists rather than predators of soil microorganisms”. Geoderma, 2025, 458, pp.117306. 10.1016/j.geoderma.2025.117306. hal-05064882

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Submitted on 13 May 2025

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Response to the letter

Response to the letter by Xiaomiing Zou on “Earthworms as mutualists rather than predators of soil microorganisms”

Following the recent publication of the paper “Earthworms as Mu-
tualists Rather than Predators of Soil Microorganisms” (Geoderma, 452,
117238) by Blouin et al. (2025), Xiaomiing Zou submitted a letter to the
editor titled “Earthworms Are Both Predators and Mutualists of Soil
Microorganisms: A Nuanced Perspective.” In his letter, the author gently
reproaches us to “acknowledge minor losses but prioritize net gains [...],
averaging out predation’s impact”. He stresses that “This statistical focus
risks masking the ecological reality: earthworms digest microbes,
meeting the definition of predation, regardless of scale”. We contend
that a meta-analysis of community metrics—such as the abundance,
richness, and evenness of bacteria and fungi—can only reveal the net
effect of earthworms on microbial communities. Concluding a predatory
relationship would have been inconsistent given that earthworms in-
crease bacterial and fungal abundances by +16.5 % and +31.4 %,
respectively. However, we fully agree with Xiaomiing Zou that a net
effect, by definition, conceals key aspects of the earthworm-microbiota
interaction. The “ecological reality” extends far beyond the duality of
earthworms acting as both predators and mutualists of microorganisms.
Xiaoming Zou’s critique provides an opportunity to explicitly unpack
the various factors that contribute to a net effect, including: (i) a di-
versity of underlying mechanisms; (ii) sequential processes occurring
across space and time; (iii) both direct and indirect interactions.
Expanding on these considerations could be particularly valuable in
cases where interactions take place in soil, involve organisms with
differing lifespans, or where one interacting entity is inherently com-
plex—such as a community. This is especially relevant in studies of the
holobiont, a concept referring to a plant or animal and its associated
microorganisms (Zilber-Rosenberg and Rosenberg, 2008).

First, the net effect integrates a diversity of mechanisms. It represents
the outcome of the gross effects of multiple underlying processes, which
can be either trophic or non-trophic. Among non-trophic mechanisms,
we can distinguish (i) phoresy – the passive transport of one species by
another (Bartlow and Agosta, 2021); (ii) ecosystem engineering – the
physical modification of the environment, influencing resource avail-
ability (Jones et al., 1994); (iii) communication (sensu lato) – signal
exchanges between a sender and a receiver (Hasson, 1991; Schaefer
et al., 2004). In aboveground ecosystems, pairwise interactions such as
predation (+/-), parasitism (+/-), competition (-/-), mutualism
(+/+), commensalism (+/0), and amensalism (-/0) have traditionally
been characterized through a trophic lens. The gross effect of these
trophic relationships is generally well-documented, with non-trophic
mechanisms introducing variability but rarely altering the overall
outcome. As a result, in many cases, the net effect remains similar to the
gross effect of trophic interactions. In soils, however, the abiotic

environment imposes strong constraints that significantly shape in-
teractions. Solid particles limit movement, space-sharing and resource
detection. These impediments are alleviated by non-trophic mecha-
nisms. Phoresy facilitates movement, as in the case of earthworms
conveying mycorrhizal fungi (Pelosi et al., 2024). Ecosystem engineer-
ing establishes a physical structure scaffolding functional domains such
as the rhizosphere, drilosphere, litter system... where diverse organisms
can live and interact (Lavelle, 2002). Communication via signal mole-
cules produced by microorganisms, mesofauna, or macrofauna enables
plants to detect resources or triggers defense mechanisms (Puga-Freitas
and Blouin, 2015). Given the significance of non-trophic mechanisms,
the net effect of soil organism interactions often diverges from the gross
effect of trophic processes. Consequently, the classification of an inter-
action as predation, mutualism, or another type may shift depending on
the environmental context, as non-trophic mechanisms are inherently
context-dependent.

Second, the net effect integrates multiple processes occurring sequentially across space and time. In the case of earthworm-microbe interactions, the spatial and temporal focus lies in comparing microbial communities in the soil before ingestion and after gut transit, when they are deposited in casts. Since microbial communities consist of thousands of species with diverse ecophysiological requirements, each species may interact with earthworms in a unique way. At a given stage of the digestive tract, different microbial species can play distinct ecological roles: some may be prey, others competitors for nutrients, mutualists aiding in the degradation of specific compounds, or commensals. Moreover, along the successive stages of digestive tract, a single microbial species can sequentially shift roles—acting as a competitor at one stage, a mutualist at another, and a prey at yet another. Additionally, mechanisms internal to the microbial community may drive ecological succession, or at least certain stages of it, independently of earthworm’s effect. Because it is nearly impossible to track each individual microbial species throughout the entire digestive process, classifying them into functional groups (e.g. aerobes and anaerobes, as mentioned by Xiaomiing Zou) could help simplify the description of their interactions. However, since functional classifications related to the gut transit are inexistent or coarse, the net effect remains a silver lining, or a small comfort.

Third, when the microbial community is considered as a single
interacting entity, the net effect represents the integration of both direct
and indirect interactions. Microbial species interact within the com-
munity itself, making it difficult to determine whether the observed
effects of earthworms are due to direct interactions between earthworms
and microbial species or to indirect interactions among microbial

DOI of original article: https://doi.org/10.1016/j.geoderma.2025.117238.

https://doi.org/10.1016/j.geoderma.2025.117306
species modified by earthworms. For instance, if earthworms enhance the abundance of bacterial species A, it is unclear whether this is due to a direct positive effect on species A or an indirect effect, such as the suppression of bacterial species B, which otherwise competes with A. Furthermore, earthworms may drive interaction modifications (Wootton, 1994) or higher-order interactions (Sanchez, 2019), potentially shifting the interaction between A and B from negative to positive. Finally, self-organization emerges from species interactions within a microbial community. For example, some species located at a specific point in space produce molecules that diffuse in the environment, while others, present elsewhere due to heterogeneous environmental conditions, are capable of degrading them. The meeting point between substrates and enzymes create a hotspot of product concentration. Consequently, local interactions between microbial species can lead to a highly structured spatial self-organization of metabolic processes (Dal Co et al., 2023). Again, the precise assessment of direct interactions between earthworms and specific microbial species is hindered by the presence of other microbial species, indirect interactions and self-organization, which may limit the realism achievable in describing earthworm-microbiota interactions.

We hope that our meta-analysis will be a relevant contribution to the field, by showing that the overall net effect of earthworms on microorganisms before versus after ingestion is positive, justifying to call this interaction “mutualism”. In accordance with Xiaoming Zou, we recognize the interest of more detailed analyses dissecting the different mechanisms, spatio-temporal dynamics and interaction network features that can be hidden in this integrative net effect.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References

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Dal Co, A., Ackermann, M., van Vliet, S., 2023. Spatial self-organization of metabolism in microbial systems: a matter of enzymes and chemicals. Cell Syst. 14, 98–108. https://doi.org/10.1016/j.cels.2022.12.009.

Hasson, O., 1991. Pursuit-deterrent signals: communication between prey and predator. Trends Ecol. Evol. 6, 325–329. https://doi.org/10.1016/0169-5347(91)90040-5.

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Manuel Blouin*
Agroecologie, Institut Agro Dijon, INRAE, Université Bourgogne, Université Bourgogne Franche-Comté, Dijon, France

Frédérique Reverchon
Red de Diversidad Biológica del Occidente Mexicano, Centro Regional del Bajío, Instituto de Ecología, A.C., Pátzcuaro, Michoacán, Mexico

Isabelle Barois
Red de Ecología Funcional, Instituto de Ecología A. C., Xalapa Veracruz, Mexico

Patrick Lavelle
Université Paris Sorbonne, IEES, Paris, France

<footnote>* Corresponding author.
E-mail address: manuel.blouin@agrosupdijon.fr (M. Blouin).
Handling Editor: Naoise Nunan</footnote>