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\DOI{10.5802/crbiol.186}
\datereceived{2025-03-05}
\daterevised{2025-08-20}
\dateaccepted{2025-09-18}
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\begin{document}

\begin{noXML}

\CDRsetmeta{articletype}{opinion}

\title{Soil macroinvertebrates, actors and indicators of soil-based
ecosystem services}

\alttitle{Les invert\'{e}br\'{e}s, acteurs et indicateurs des services
\'{e}cosyst\'{e}miques du sol}

\author{\firstname{Patrick} \lastname{Lavelle}\CDRorcid{0000-0002-2127-1067}}
\address{IEES, Universit\'{e} Paris Sorbonne, France}
\email{plavelle48@gmail.com}

\keywords{\kwd{Soil macroinvertebrates}
\kwd{Indicators}
\kwd{Soil quality}
\kwd{Ecosystem services}}

\altkeywords{\kwd{Macroinvert\'{e}br\'{e}s du sol}
\kwd{Indicateurs}
\kwd{Qualit\'{e} du sol}
\kwd{Services \'{e}cosyst\'{e}miques}}

\begin{abstract}
Soil management practices are of particular importance, as they are the
basis of 60\% of planetary ecosystem services. Positive environmental
externalities are associated with methods inspired by agroecology,
whereas conventional methods generally have elevated indirect
environmental costs. Public policies that take this reality into
account are needed to make agriculture a solution rather than an
obstacle to the regeneration of the planetary environment. Soil-based
ecosystem services, the support for primary production, climate control
through carbon sequestration, hydrological services and the
biodiversity associated to their delivery, are usually associated in
``bundles of ecosystem services''. We propose to use communities of
soil macroinvertebrates, the ones visible at the naked eye, as
estimators of all other services to which they are strongly correlated.
Macroinvertebrates are represented by a great diversity of biological
forms, and indicator species for soil functions have been identified in
several studies by scientists. The 15 orders commonly found in most
soils are known to soil managers. Estimating their communities is easy
and inexpensive with the widely used standard ISO/TSBF method. A
numerical indicator constructed from data collected in several thousand
sites sampled by this method is proposed, which can be applied
everywhere. It allows to calculate for any site a value that has been
shown to be a reliable proxy for the global chemical, physical and
biological functions that these invertebrates stimulate in the soil, in
mutualistic associations with other soil organisms. In conclusion, we
discuss the feasibility of a generalized use of this indicator by
farmer communities as a support for public policies that will organize
the fair recognition and remuneration of positive externalities
generated by some practices.
\end{abstract}

\begin{altabstract}
Les pratiques de gestion des sols sont \`a la base de 60 \% des
services \'ecosyst\'emiques plan\'etaires. Des externalit\'es
environnementales positives sont associ\'ees aux m\'ethodes inspir\'ees
de l'agro\'ecologie alors que les m\'ethodes conventionnelles ont
g\'en\'eralement des co\^uts environnementaux \'elev\'es. Des
politiques publiques qui prennent en compte cette r\'ealit\'e sont
n\'ecessaires pour faire de l'agriculture une solution plut\^ot quun
obstacle \`a la r\'eg\'en\'eration de l'environnement plan\'etaire. Les
services \'ecosyst\'emiques li\'es aux sols, le soutien \`a la
production primaire, la r\'egulation du climat, les services
hydrologiques et la biodiversit\'e associ\'ee \`a leur fourniture
forment des ensembles li\'es de services \'ecosyst\'emiques. Nous
proposons d'utiliser les peuplements de macroinvert\'ebr\'es du sol,
ceux visibles \`a l'{\oe}il nu, comme estimateurs de tous les autres
services auxquels ils sont fortement corr\'el\'es. De nombreux
arguments soutiennent cette proposition : ils sont repr\'esent\'es par
une grande diversit\'e de formes biologiques et les 15 ordres que l'on
trouve couramment sont connus des gestionnaires de sols ; l'estimation
de leurs communaut\'es par la m\'ethode ISO/TSBF est facile et peu
co\^uteuse. Finalement, l'indicateur num\'erique construit \`a partir
de donn\'ees collect\'ees dans plusieurs milliers de sites
\'echantillonn\'es par cette m\'ethode peut \^etre appliqu\'e partout,
permettant de calculer pour n'importe quel site un indicateur des
fonctions chimiques, physiques et biologiques globales que ces
invert\'ebr\'es stimulent, en association avec les autres organismes du
sol. Nous discutons en conclusion de la faisabilit\'e d'une utilisation
g\'en\'eralis\'ee de cet indicateur par les communaut\'es paysannes
comme support aux politiques publiques qui organiseront leur juste
reconnaissance et r\'emun\'eration.
\end{altabstract}

\editornote{Article submitted by invitation}
\alteditornote{Article soumis sur invitation}

\maketitle

\vspace*{1pt}

\twocolumngrid

\end{noXML}

\defcitealias{27}{ibid.}
\defcitealias{46}{ibid.}

\section{Introduction}\label{sec1}
Soils are the basis of 16 of the 24 ecosystem services listed in the
Millennium Ecosystem  Assessment \citep{1}.  These services can be
related to three major functions of the soil: water flow management,
nutrient cycling and carbone storage with effect on climate, and
support to primary production, which depends largely on the two
previous  functions \citep{2}.  Physical characteristics of the soil
determine the service of protection against erosion, water infiltration
and retention at various potentials in pore spaces and the transfer of
rainwater  to water tables \citep{3}. The recycling of organic matter is done by two
complementary processes, mineralization and humification.
Mineralization, carried out at more than 90\% by soil microorganisms,
releases in assimilable mineral forms part of the nutrients contained
in decomposing organic matter, such as nitrates, ammonium, phosphates
or sulfates for example, and makes them available to the plant and
living organisms in the soil. The complexity of biological processes
and the diversity of organisms involved in this process allow for
synchronization between the flow of released nutrients and their use by
plants, an essential conservation 
\mbox{mechanism} compared to the mediocre
rate of use of chemical fertilizers, which often does not exceed 50\%
for \mbox{nitrogen,} as an  example  \citep{4}. The portion of organic matter
that is not mineralized is preserved in the soil by two complementary
chemical and physical protection systems. Chemical protection is
achieved through the accumulation of recalcitrant compounds,
macromolecules rich in aromatic compounds that are more difficult to
degrade than carbohydrates with smaller molecules such as cellulose or
proteins. Another part of the protection is physical in nature, when
organic matter particles, micro-fragmented largely by the action of
invertebrates, are associated with mineral particles in compact soil
aggregates and thus protected from attack by microorganisms that no
longer have physical access to them  \citep{5}. Soils also shelter a
significant proportion of global  biodiversity  \citep{6,7,8}, probably
more than half of it. 

It is known that soil management methods profoundly affect the
production of these services, with positive or negative externalities
depending on the  practices \citep{9}. The adoption of intensive
agricultural methods combining the exclusive use of synthetic chemical
fertilizers, mechanical tillage and chemical control of weeds and crop
pests has considerably reduced the provision of soil ecosystem services
to the sole benefit of production. The spectacular global increase of
250\% in 40~years in food production, accompanied by a decrease in its
price to 40\% of the initial level, has been accompanied by the
degradation of at least 1/3 of the planet's  soils  \citep{1}, the
destocking of 133~Gt of carbone equivalent to 15~years of anthropogenic
emissions \citep{10}  and a generalized decrease in diversity, with,
for example, a decrease in the density of macroinvertebrates of more
than 60\% in annual crops in temperate  regions \citep{11}. Let us add
to this assessment that, beyond the year~2000, the progressive
depletion of soils gradually erased the observed benefits, and in 2020,
the price of food returned to its 1960  value  \citep{1,12}.
\looseness=-1

Agricultural economics has, until now, paid little attention to
environmental and social externalities. The only accounting element of
a farm's operation is most often production, paid at a fixed price by
the national or international market. 
\mbox{Under} these conditions,
environmental damage associated with aggressive practices is not
penalized, and the care taken by producers who use gentle practices to
maintain good environmental quality is not\break
compensated.

The idea of such compensation is, however, widespread and even
enshrined in the constitutions of various  countries \citep{13,14,15}.
Its practical implementation is limited to a few experimental
situations, if we exclude the numerous projects aimed at remunerating
the protection of areas where water supplies for many cities or carbon
storage are generated.

\looseness=-1
A major obstacle to the implementation of targeted policies is the very
measurement of services. Payment systems, for example, for carbon
storage, are complex and require a level of expertise that makes
transaction costs high. Only a few wealthy farmers or large
agribusinesses can implement them, and small producers, who generally
manage the land more amicably, are not affected by these subsidies. 
However, we know that such policies, even when implemented at a low
subsidy level, have surprising  effects \citep{16}. 

Strongly connected
to all the microbial and faunal elements of soil biodiversity,
macroinvertebrates form an abundant community everywhere and of a great
diversity. Defined simply by the fact that they are visible to the
naked eye, they are divided into 15~major taxonomic units, between
superfamilies and orders  (Table~\ref{tab1}). They include social
insects (ants and termites), many non-social insects (Coleoptera,
Diptera, Dermaptera), Myriapoda Chilopoda, Diplopoda, several groups of
Arachnida, earthworms  (Crassiclitellata) and terrestrial Gastropoda
and a few less frequent invertebrates. These groups are found
everywhere, except for termites confined to intertropical regions, with
frequencies that vary from 9 to 71\% depending on the group. The
species, genera and even families, however, differ greatly from one
site to another, even if the functions assumed are comparable within
the same group. Rarer units are found locally: Arachnids (Solifuges,
Palpigrades, Uropyges), the very primitive Onychophora of tropical
rainforests, the Mermithidae Nematodes parasites of Orthoptera whose
cycle phase passes through the soil, the pseudo-social Embioptera,
cicada larvae and spectacular Gryllotalpidae with powerful burrowing
forelegs. The diversity and abundance of these soil inhabitants are
familiar to farmers who have names for them, whatever the region.
\looseness=-1

\begin{table*}
\fontsize{9}{10.2}\selectfont\tabcolsep4.5pt
\caption{\label{tab1}General biology and frequency of soil
macroinvertebrate taxa in 3684 sites of the Macrofauna database
\citep{11}\vspace*{-2pt}}
\begin{tabular}{ccccccc}
\thead
\parbox[t]{2cm}{\centering Common english name} & 
\parbox[t]{2cm}{\centering Taxonomic classification} &
\parbox[t]{1.5cm}{\centering Taxonomic level} & Main habitat &
\parbox[t]{2cm}{\centering Feeding habits} & Respiration &
\parbox[t]{2cm}{\centering \% frequency in DB} \vspace*{2pt}\\
\endthead

Earthworms & Crassi clitellata & Order & Litter and soil & 
\parbox[t]{2cm}{\centering Detritivores, geophagous} & Skin & 70.7
\vspace*{2pt}\\

Beetles & Coleoptera & Order & \parbox[t]{2cm}{\centering Litter Rhizosphere} & 
\parbox[t]{2cm}{\centering Predators, detritivores, fungivores} & Trachea & 65.4
\vspace*{2pt}\\

Ants & Formicidae & Family & Soil and litter & 
\parbox[t]{2cm}{\centering Predators granivores, fungivores} &  Trachea & 53.3
\vspace*{2pt}\\

Spiders & Araneae & Order & Litter and soil & Predators & Trachea & 49\\

Centipede & Chilopoda & Order & 
\parbox[t]{2cm}{\centering Leaf and woody litter} & Predators & Trachea & 35.8
\vspace*{2pt}\\

Milipede & Diplopoda & Order & 
\parbox[t]{2cm}{\centering Leaf and woody litter} & Detritivores & Trachea & 33.4
\vspace*{2pt}\\

Fly larvae & Diptera & Order & Litter and soil &
\parbox[t]{2cm}{\centering Predators, detritivores, fungivores} & Trachea & 27.2
\vspace*{2pt}\\

Termites & Termitoidea & Epifamily & 
\parbox[t]{2cm}{\centering Soil, decaying logs} &
\parbox[t]{2cm}{\centering Detritivores, herbivores, wood feeders} & Trachea & 26.6
\vspace*{2pt}\\

Woodlouse & Isopoda & Order & Litter & Saprophagous & Gills & 19.5\\

Stink bugs & 
\parbox[t]{2cm}{\centering Homoptera Hemiptera} & Order & Litter &
Phytophagous & Trachea & 19.3 \vspace*{2pt}\\

\parbox[t]{2cm}{\centering Snails and slugs} & Pulmonata & Order & Litter & 
\parbox[t]{2cm}{\centering Herbivorous, saprophagous} & Lung & 18.2
\vspace*{2pt}\\

Cockroaches & Blattaria & Order & Litter & Detritivores & Trachea & 13.8\\

Cricket & Grylloidea & Super family & Litter & Detritivores & Trachea & 12.7\\

Caterpilar & Lepidoptera & Order & Litter & Detritivorous & Trachea & 12.1\\

Earwings & Dermaptera & Order & Litter & 
\parbox[t]{2cm}{\centering Predators, saprophagous} & Trachea & 8.9
\vspace*{2pt}\\

Others & 
\parbox[t]{2.5cm}{\centering Cicadoidea, Opilionidae, Scorpions, Pseudoscorpions\ldots} &
 & & & & 15.2 \vspace*{2pt}
\botline
\end{tabular}
\vspace*{-2pt}
\end{table*}

In this review, we explain the essential role of macroinvertebrates in
the ecological functioning of the soil. We then summarize a set of
field data that demonstrate the strong link between these communities
and soil-based ecosystem services. We finally present a simple and
inexpensive method that synthesizes the state of their communities into
a single numerical indicator. We propose making this indicator
available to farmers so that they can use it as a marker of the
environmental externalities of their practices and benefit from
possible subsidies that recognize the environmental benefits produced
by their work.

These invertebrates exhibit a wide variety of feeding habits, habitat
preferences, locomotion abilities and breathing patterns in the soil,
making them excellent natural indicators of living conditions in this
environment.

\vspace*{-3pt}

\section{Living in the soil}\label{sec2}

\vspace*{-3pt}

To understand the importance of macroinvertebrate populations in soil
function, it is important to \mbox{consider} the specific conditions of the
soil as a living environment. Living in the soil means facing at least
two very strong constraints: the compact nature of this environment
that is difficult to penetrate, and the nature of the available food 
resources \citep{3}.

\subsection{Moving in a compact environment}\label{sec2.1}
Soils are compact environments, although porosity can occasionally
reach high values, of more than 50\% for example, in the upper 5 to 10~cm
of Amazonian forest soils populated by active fauna. Porosity, however,
decreases rapidly in depth as biological activity decreases, and the
installation of pastures in the same Amazonian site can make it drop to
less than 20\% in the upper first  centimeters  \citep{17}. This
porosity is however composed of a sizeable proportion of micropores
inaccessible even to soil microorganisms, and the low connectivity of
habitable pores limits the usable space and movements in the soil
matrix. In such a context, two adaptive strategies are defined: moving
by digging and thereby accessing available food resources, or entering
dormancy when available resources in contact with the organism are
exhausted, and waiting for favorable conditions to resume activity. The
first strategy is that of burrowing organisms, the engineers of the
soil ecosystem, mainly earthworms, termites and ants, which move and
arrange the soil by digging galleries and macropores. For other
organisms that inhabit the mineral soil and are unable to dig, the
option is to use the porous spaces created by the engineers. This is
the case for example of the mesofauna, 0.1 to 2~mm in size, mainly
comprised of Acari and Collembola, which take advantage of the porous
spaces created by earthworms or roots to colonize deep soil  layers 
\citep{18}. For microorganisms unable to move to new food sources, once
the one in contact with them has been exhausted, the option is dormancy
until bioturbation gives them new opportunities to resume activity and
encounter new food sources. It is thus measured that in the soil, up to
75\% of bacteria are inactive \citep{19}, and the turnover time of
bacterial biomass is measured in months and even years, when the
generation time can be less than an hour in optimal laboratory 
conditions  \citep{3}.\looseness=1

\subsection{Feed on poor or unpredictable high-quality
food}\label{sec2.2}
The second major constraint of the soil relates to the quality and
availability of food resources. We can roughly distinguish two main
types of resources: (1)~necromass of plant, animal or microbial origin
and (2)~soluble resources, i.e.\ the energy mediators produced by
engineer organisms \citep{20}.

\medskip\noindent 
(1)~Necromass. 
Plant necromass is a diverse set of leaves, stems, branches and roots.
Although this set covers a very wide diversity of compositions and
structures, two general characteristics make its digestion problematic
for most organisms. The first is the overall composition in various
elements that imposes stoichiometric limitations on the use of these
resources \citep{21}. It is frequently observed that the high value of
the C:N ratio, for example, forces the user organism to find a
complementary source of nitrogen, or to implement physiological
mechanisms for the elimination of excess carbon when simple elimination
by aerobic respiration is not sufficient \citep{22}. This constraint is
well known to farmers who bury straw at a high C:N ratio, with the
consequence of immobilizing the nitrogen available in the soil and a
temporary competition between the plant and the microflora that
decomposes the straw.

In addition to this chemical limitation, a second one is the inclusion
of nitrogen from plant cells in tannin-protein complexes that very few
organisms can digest. These tannins, whose function is to limit
herbivory when the leaf is alive, are contained in vacuoles whose
contents are released when the plant dies. It is estimated that more
than 80\% of the nitrogen in dead leaves or roots is blocked in this
form \citet{23}. Another chemical limitation is the presence of lignin,
a naturally poorly digestible compound.

There may also exist a physical limitation: the mechanical resistance
of the compounds to the processes of comminution and fragmentation
necessary for seeding the fungi that will carry out the first stages of
decomposition.

Animal necromass, which represents a relatively small proportion of
resources, presents fewer 
\mbox{limitations.}

Microbial necromass, the subject of recent abundant literature
\citep{24,25}, is characterised by chemical markers that allow it to be
identified and quantified. However, a doubt remains: are these markers
exclusive to necromass or can they also characterize living biomass
and/or microbial metabolites, such as mucilage polysaccharides and
enzymes for example? 

The fragmented, transformed necromass of any origin, associated with
mineral elements in soil aggregates, constitutes the organic matter of
the soil. This is an abundant resource, but its use is made difficult
by a highly dispersed distribution at the scale of microorganisms, or
by its low concentration in soil for invertebrates that feed on it.
Added to these disadvantages is the location in aggregates that offers
physical protection, and the chemical quality impoverished in easily
assimilated elements during the various stages of its transformation.

\medskip\noindent
(2)~Soluble resources.
The other major resource for soil organisms is the largely soluble
products secreted by roots (root exudates), earthworms (intestinal
mucus) or termites (saliva). These compounds, grouped under the term
energy mediators \citep{20}, are used by soil engineering organisms,
roots and macroinvertebrates, to stimulate the activity of soil
microorganisms by priming effects \citep{3}. Microorganisms, once taken
out of the dormancy in which they can be immersed for months or even
years, digest the compounds that neither the roots nor the
invertebrates can assimilate, in a system of mutualistic digestion
\citep{26}. These resources of very high energy value and digestibility
are abundant. Up to 20\% of the products of photosynthesis are injected
into the soil at the root tips, while earthworms add to the ingested
soil between 5 and 18\% of intestinal mucus composed of low molecular
weight glycoproteins \citep{27}. The disadvantage of these resources is
the extreme localization, both in time and space, of their production,
which makes them sporadic resources \citepalias{27}.

\subsection{Self-organized soil}\label{sec2.3}
Soil communities are thus roughly divided between microorganisms unable
to move in the compact universe of the soil, which forces them to long
periods of dormancy, and invertebrates and roots, capable of moving in
the litter layers if not in the mineral soil, and even for some of them
carrying out bioturbation, but with insufficient enzymatic equipment to
digest most of the available resources \citep{26,28}. Complementarity
and association of these two groups are the basis of the functioning of
the soil as a self-organized system in which macroinvertebrates occupy
a strategic place  \citep[Figures~\ref{fig1} and~\ref{fig2},][]{20}.

\begin{figure}
\includegraphics{fig01}
\caption{\label{fig1}Soil as a self-organized system of biological
entities. Organisms of increasing sizes, from microorganisms to micro
invertebrates (microfoodwebs), ecosystem engineers and ecosystems
(horizontal axis) create structures of different sizes (vertical axis)
and organize soil at different nested scales from 1 (microbial
aggregates inhabited by microbial communities) to 5 (landscape viewed
as a mosaic of different ecosystems). Most soil-based Ecosystem
services are perceived and delivered at the landscape (5) scale.}
\end{figure}

\begin{figure}
\includegraphics{fig02}
\vspace*{-2pt}
\caption{\label{fig2}Interactions among self-organized units across
scales and the delivery of ecosystem services. Ecosystem engineers
select and activate microbial communities in their functional  domains
(1). A mutualist digestion system (2) releases energy (3) used by
ecosystem engineers to build biogenic structures and organize soil
physical structure (4) with resulting effects on water services
(infiltration and storage) (5). The combination of mineralization
processes during the digestion process and sequestration of organic
compounds in biogenic structures affects soil organic matter dynamics
(6), and hence, nutrient cycling and climate regulation (7). Note that
additional scales such as biome and biosphere may be added when
ecosystem services are considered at a global scale.}
\end{figure}

\section{Macroinvertebrates as indicators}\label{sec3}
The role of macroinvertebrates and the characteristics of their
populations make them natural indicators with great potential. The fact
that all major groups, except for termites, are present everywhere,
even if with different species, genera and families, and are recognized
by most soil workers, will facilitate the collection of data by many
people. \mbox{Practical} tools for the quantitative analysis of populations
and the development of numerical indicators are 
\mbox{available.}

There are two ways of using them as indicators: at the species level,
with indicator species, or at the population level with synthetic
indicators.

\vspace*{-2pt}

\subsection{Indicator species}\label{sec3.1}

\vspace*{-2pt}

Healthy soils may host up to several hundred macroinvertebrate species.
Ants, Coleoptera and Arachnida are usually the most speciose groups,
but earthworms and termites may also be interesting indicators 
\citep{29,30,31,32}. The IndVal evaluation, which measures the
indicative power of species for a given ecosystem attribute, allows to
identify indicator species  \citep{32}. Several studies have
successfully tested this method, opening the way to interesting uses of
community data. For example, in a set of 75~plots distributed among
five land use types of the Colombian Eastern Plains, 91~ant species
were collected using the ISO/TSBF  \citep{33,34} hand sorting method.
Of these, 52 were found in improved pastures, 45~in semi-natural
savanna, 39 and 38 respectively in rubber and oil palm plantations, and
20 in annual crops  \citep{35}. Improved pastures had the highest
number of unique species, found only in this land use system (11),
followed by rubber plantations (10) and semi-natural savannas (9). In
the same plots, measurement of a complete set of soil physical and
chemical variables, macroinvertebrate communities, accumulation of
carbon in soils and vegetation and greenhouse gaz (GHG) emissions
allowed to elaborate synthetic indicator proxies of soil-based
ecosystem services (ES)  \citep{36}. Fifteen species showed a
significant indicator value: five as indicators of general biodiversity
(soil macroinvertebrate communities); five of macroaggregate
morphology, a proxy to water infiltration and storage in soil; one of
water regulation (negatively linked to soil compaction); three to soil
nutrient provision (based on general soil chemical properties); and one
to climate regulation as evaluated by a set of carbon concentrations in
soil and biomass and GHG emissions. Interestingly, no species appeared
to be indicative of multiple ES. 

Another similar study on termites of 38~farms, located in deforested
regions of Amazonia, in the Colombian Caqueta department and Brazilian
Para state, shows interesting results. Forty-eight species were
collected in total, 12 in Colombia and 45 in Peru. Nine species were
common to both regions. Eleven species exhibited significant indicative
power. Two species in Colombia were indicators of chemical fertility
and soil aggregate morphology. In Peru, nine species had significant
indicative power: two for 
\mbox{hydrological} functions linked to soil
physical properties; one for soil aggregate morphology; and six for
soil biodiversity as measured by macroinvertebrate community patterns.
Four species were indicative of more than one ES proxy.

Participatory workshops conducted with farmers showed some knowledge of
the species encountered and their relationship with soil ecosystem
services, hydrological functions, chemical fertility and the diversity
of macroinvertebrate populations  \citep{37}. Peruvian farmers were
able to recognize four of the seven species presented and indicate
seven relationships with soil-based ES, five of which corresponded to
significant effects recognized by the IndVal method. In Colombia, all
seven species presented were known to farmers, and three of them were
associated with chemical fertility, while the IndVal method was unable
to confirm the significance of these relationships.

\subsection{Synthetic indicators of macroinvertebrate
communities}\label{sec3.2}

Other unpublished field studies logically showed that the ability of
farmers to recognize soil invertebrates improves when considering
broader taxonomic groups like families and orders. In subsequent work,
we then tested the hypothesis that community compositions assessed at
taxonomic levels such as order, would allow the prediction of
associated ES at broad geographic scales. If this hypothesis were
verified, it would show good correspondence between scientific
knowledge and that of farmers.

A simple and inexpensive manual sorting method proposed nearly 40 years
ago has been popularized in the Tropical Soil Biology and Fertility
program  \citep{33}. It has been further adopted as a standard by 
\citet{34}. The unit sample is a block of 25~cm on each side, extended
to a depth of 30~cm. The block is extracted with a metal frame if this
facility exists, and separated into four different layers, surface
litter, 0--10, 10--20 and 20--30~cm. The recommended number of repetitions
is five, spaced 30~m apart if the terrain allows, to avoid
autocorrelation of the data. A study on sampling carried out in France
even showed that, from three repetitions, the definition is sufficient
to compare communities from contrasted land use types  \citep{38}.

This simple and inexpensive method has been adopted massively. Today,
the Macrofauna database which groups the data obtained with this method
has more than 10~000 sampled sites, distributed across more than 60
countries, covering all terrestrial biomes and ecosystems except for
cold or hot deserts  \citep{39}.

A principal component analysis (PCA) of an intermediate version of the
database, with 3694 sites, gave the following general results 
(Figure~\ref{fig3}). The ``average'' community sampled in all these
sites comprised 712~individuals per m$^{2}$ belonging to five different
orders. The first factor of the PCA ordered communities according to
the abundance of all groups, with a major effect of social insects and
litter invertebrates. The second factor opposed sites with dominant
social insect populations to other non-social taxonomic groups.
Specific tests showed significant effects of all the environmental
parameters tested: vegetation cover (11\% of the total explained
variance), latitude (8.6\%), altitude (5.2\%), soil texture (3.2\%) or
temperature (2.3\%)  \citep{11}.

\begin{figure*}
\includegraphics{fig03}
\caption{\label{fig3}Projection of  ({left}) macroinvertebrate group 
densities and community parameters in a plane defined by
factors~1 and 2 (F1 and F2) of a principal component analysis of
macroinvertebrate community data of the Macrofauna database. ANT, ants;
ARAC, Arachnida; BLA, Blattaria; CHILO, Chilopoda; COL, Coleoptera;
DEN, total density per square metre; DERM, Dermaptera; DIP, Diptera
larvae; DIPLO, Diplopoda; EWM, earthworms; GAST, Gastropoda; HEMI,
Homoptera Hemiptera; ISO, Isopoda; MYR, Myriapoda; ORTH, Orthoptera;
OTH, other; RT, taxonomic richness (number of orders found in the
sampling); TER, termites; and (right) average global mean density of
different groups and species richness. Lower box: Percentage of
variance explained by different environmental factors 
\citep[after][]{11}.}
\end{figure*}

The abundance data of macrofauna groups in the different types of land
use at a given site can be synthesized into an indicator calculated
from three metrics produced by the PCA analysis: the \% of variance
explained by each of the first two axes, correlations of the variables
(the densities of the different taxonomic groups) with the factorial
axes and coordinates of the points along these axes. This indicator is
calibrated to vary from 0.1 to 1.0 depending on whether the population
is abundant and diverse  \citep{40}. This indicator has proven to be
very sensitive to the types of cover and land use, as shown in the
example of the study carried out in the eastern llanos of  Colombia 
\citep{36}. In this site, the indicator had the highest values in
pastures that associated the African grass \textit{Brachiaria
humidicola} with the legume \textit{Centrosema}. Although having a
higher average, the difference with the natural savanna and the oil
palm plantation was not significant, unlike the rubber plantation, and
especially the transitional rice, soybean and corn cropping systems,
which showed the lowest average of 0.28 against 0.74 in the improved
pasture  (Figure~\ref{fig4}).

\begin{figure*}
\includegraphics{fig04}
\caption{\label{fig4}Macrofauna indicators in different types of land
uses in Colombian Orinoquia (left) and coefficient of matrix
correlation (Rv) among tables of data for the different indicators of
ecosystem services, and associated  $p$-values (*$p<0.05$;  **$p<0.01$;
***$p<0.001$) (right).} 
\end{figure*}

In this site, the measurement of the chemical and physical parameters
of the soil and the carbon accumulated in the soil and vegetation and
emissions of greenhouse gases has allowed the construction of synthetic
indicators, with the same methodology used for macrofauna. The matrix
correlations between the data tables thus constituted are all
significant at the p threshold value of 0.01. This result, and others
similar  \citep{41,42,43,44}, confirmed, on the one hand, the group
behavior of bundles of ecosystem services, which all vary in the same
direction  \citep{45}. On the other hand, they suggest using the
macrofauna indicator as a proxy for all the others, with the additional
advantage that it can be evaluated at a low cost by local field
operators.

\subsection{Building a global indicator}\label{sec3.3}
The numerous studies comparing macroinvertebrate populations in
different types of use of a same locality always showed a pattern similar to
the one obtained with the full set of data: axis~1 of the PCA that
compares communities of different types of local land uses
systematically classifies them according to the abundance of all groups
and taxonomic richness  \citep{46}. Axis~2 separates the sites where
social insects dominate. A global indicator was therefore created from
the 3694 sites compiled in the Macrofauna database. This indicator was
applied to communities sampled in ten regions with contrasting
characteristics: partially deforested sites in the Brazilian and
Colombian Amazon; agroecosystems and forest remnants in the Colombian
Andes; tea plantations and associated systems in China; or temperate
forests in France  \citepalias{46}. The values thus calculated were compared
to those obtained by applying the same method to local datasets. Highly
significant correlations between the two sets of indicators supported
the use of a single formula to evaluate a soil macroinvertebrate
community regardless of the site. We can thus evaluate the quality of
the macrofauna population with the formula:
\begin{eqnarray*}
\text{I macrofauna} 
&
=
& 
0.014*
\mathop{(}19.2*\mathrm{EWM} + 17.5*\mathrm{ANT}
\\&&
+\, 20.9*\mathrm{TER} +
9.8*\mathrm{BLA} + 20.4*\mathrm{COL}
\\&&
+\,17.5*\mathrm{ARAC} + 20.1*\mathrm{DIPLO}
\\&&
+\,21.8*\mathrm{CHILO} + 13.5*\mathrm{HEMI}
\\&&
+\,8.9*\mathrm{DERMA} + 15.5*\mathrm{LEPI}
\\&&
+\,16.7*\mathrm{GAST} + 21.9*\mathrm{OTR}
\\&&
+\,31.8*\mathrm{DEN} + 31.8*\mathrm{RT}
\mathop{)}+0.1,
\end{eqnarray*}
with 
EWM: log density of earthworms per m$^{2}$; 
TER: log density of termites per m$^{2}$; 
BLA: log density of Blattodea per m$^{2}$; 
COL: log density of Coleoptera, \mbox{larvae} ${+}$ adults, per m$^{2}$; 
ARAC: log density of Arachnida per m$^{2}$; 
DIPLO: log density of Diplopoda per m$^{2}$;
CHILO: log density of Chilopoda per m$^{2}$; 
HEMI: log density of Hemiptera per m$^{2}$; 
DERMA: log density of Dermaptera per m$^{2}$; 
LEPI: log density of Lepidoptera per m$^{2}$; 
GAST: log density of Gastropoda per m$^{2}$; 
OTR: log density of others per m$^{2}$; 
DEN: log total density per m$^{2}$; 
RT: log number of groups EWM to OTR represented adjusted
to the range of variations of the DEN variable.

The indicator varied greatly between and within plant cover types 
(Figure~\ref{fig5}). Tropical environments had the highest values,
between 0.61~$\pm $~0.16 and 0.55~$\pm $~0.12 in natural forests and
savannas respectively, and 0.51~$\pm $~0.19, 0.49~$\pm $~0.15 and
0.48~$\pm $~0.14 in tree-related crops, pastures and non-tree crops,
respectively. Temperate soils had their highest values in grasslands
(0.38~$\pm $~0.14) and forests (0.35~$\pm $~0.14), and lower values in
bush and dry forests (0.3~$\pm $~0.14) and annual crops (0.31~$\pm
$~0.13). However, beyond these significant differences among means,
variability within groups is very high, and minimum and maximum values
in each group are rather close, since local conditions and management
options have high impacts.

\begin{figure}
\includegraphics{fig05}
\caption{\label{fig5}Variations of the global indicator of soil
macroinvertebrate communities in tropical and temperate regions, as a
function of plant cover (source Macrofauna database,
\url{https://datadryad.org/downloads/file\_stream/1355027}). Blocks
with a different letter are different at  $p<0.05$.}
\end{figure}

\section{Conclusion}\label{sec4}
Macroinvertebrate communities are at the heart of soil processes for
their globally mutualistic \mbox{interaction} with the microflora and their
powerful physical, biochemical and community engineering effects 
\citep{20}. They have the particularity of being divided into 15 main
groups, potentially present everywhere except termites, and which
perform similar functions although represented by families, genera and
species that are sometimes very distant taxonomically.

The relatively limited number of these taxonomic units means that most
field operators recognize them and can name them. Farmers' workshops
conducted in the Amazonian regions confirmed this\break knowledge. 

In all sites where the link between this indicator and indicators of
soil ecosystem services was jointly measured, very high correlations
were noted  \citep{44}. The global indicator proposed in this study is
thus a first-rate tool available to populations far from laboratories.
They will be able to use it to assess the agroecological quality of
their land. In addition, they will be able to compare plots subjected
to various practices and measure any progress obtained from the
adoption of more environmentally friendly practices. Payment policies
for ecosystem services based on this tool for their evaluations will
have the considerable advantage of allowing all producers, especially
small producers, to value the positive externalities of practices that
respect soils and their biodiversity.

To achieve this objective, a few more steps are necessary. Firstly,
producing a practical guide and making the tool easier by automating
the calculations with a smartphone application will facilitate the
operator's work. Second, training offered by technical assistance
institutions will allow, if necessary, to issue a diploma attesting to
a correct mastery of the tool. Third, on the public policy side,
additional knowledge is needed to calibrate the progress measured with
the indicator and assess associated properties such as increased
infiltration and water storage or carbon storage in the soil.

\section*{Declaration of interests}
The author does not work for, advise, own shares in, or receive funds
from any organization that could benefit from this article, and has
declared no  \mbox{affiliations} other than their research
organization.

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