Review

Soil invertebrates as ecosystem engineers: Intended and

accidental effects on soil and feedback loops

Pascal Jouquet a,*, Jens Dauber b, Jan Lagerlof c,Patrick Lavelle d, Michel Lepage e

a Laboratoire d’Ecologie des Sols Tropicaux, IRD, 32 Avenue H. Varagnat, 93143 Bondy Cedex, Franceb Department of Animal Ecology, IFZ, Justus-Liebig University of Giessen, Heinrich-Buff-Ring 26-32, D-35392 Giessen, Germany

c Department of Ecology and Crop Production Science, P.O.Box 7043,

Swedish University of Agricultural Science (SLU), SE-750 70 Uppsala, Swedend UFRA Ciencia do, Solo, IRD, CP 917 Terra Firme, 66077-530 Belem, Para, Brazil

e IRD, 01 BP 182, Ouagadougou 01, Burkina Faso

Received 11 February 2005; received in revised form 6 July 2005; accepted 8 July 2005

Abstract

Termites, ants and earthworms are considered as soil engineers because of their effects on soil properties and their influence

on the availability of resources for other organisms, including microorganisms and plants. However, the links between their

impacts on the soil environment and the resulting modification of natural selection pressures on engineer as well as on other

organisms have received little attention.

We suggest that the strategy evolved by species, or functional groups to control their environment can explain the difference

between extended phenotype and accidental engineers. Extended phenotype engineers concentrate their activities on the

building of biogenic structures in order to maintain optimal conditions for their growth. Conversely, accidental engineers expend

energy in moving through the soil to be as close as possible to their optimal environment. We discuss in this paper why termites

and ants are best viewed as extended phenotype engineers, and particularly how their impacts on ecosystem functioning can be

considered as results of their requirements and how their activities could induce feedback loops affecting themselves. We also

focus on the engineering activities of earthworms and discuss why some species can be considered as extended phenotype while

others are more accidental engineers.

Finally, we discuss links between the strategies developed by engineers and ecosystem functioning. Although both types of

engineer create ‘‘hot-spots’’ in soil, we argue that extended phenotype engineers have a greater effect on the maintenance of

ecosystem heterogeneity since they concentrate their activities at a few points, as compared to accidental engineers which may

move through the soil and thus contribute to homogenisation of nutrient distribution throughout the whole ecosystem.

# 2005 Elsevier B.V. All rights reserved.

Keywords: Termites; Ants; Earthworms; Ecosystem engineers; Soil ecology

www.elsevier.com/locate/apsoil

Applied Soil Ecology 32 (2006) 153–164

* Corresponding author. Tel.: +33 1 48 02 59 60; fax: +33 1 48 02 59 70.

E-mail address: pascal.jouquet@bondy.ird.fr (P. Jouquet).

0929-1393/$ – see front matter # 2005 Elsevier B.V. All rights reserved.

doi:10.1016/j.apsoil.2005.07.004

P. Jouquet et al. / Applied Soil Ecology 32 (2006) 153–164154

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 154

2. Termites and ants as extended phenotype engineers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155

2.1. Direct positive effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 156

2.2. Indirect positive effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 156

2.3. Indirect negative effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158

3. Are earthworms accidental engineers? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158

4. From the engineering strategy of organisms to the functioning of ecosystems . . . . . . . . . . . . . . . . . . . . . . . . 160

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162

1. Introduction

The definition given by Jones et al. (1994) of

ecosystem engineers has deeply influenced our

assessment of the role of organisms in ecosystem

functioning. Some organisms are no longer considered

to play a role only as elements of a food web, but they

are studied from the viewpoint of being responsible for

altering ecosystem dynamics through the modifica-

tion, maintenance and/or creation of habitats for other

organisms in the ecosystem. Ecosystem engineers are

organisms that directly or indirectly modulate the

availability of resources to other species, by causing

physical state changes in biotic or abiotic materials

(Jones et al., 1994, 1997). Lavelle (2002) argues that in

soil, the relative importance of regulation imposed by

ecosystem engineering is likely to be greater than

regulation by trophic relationships because of the

specific ecological constraints observed in this

environment when compared to above-ground condi-

tions. Earthworms, termites and ants have been

identified as the most important soil engineers. At

the heart of the soil engineering concept is the ability

of these organisms to move through the soil and to

build organo-mineral structures with specific physical,

chemical and microbiological properties (Lavelle

et al., 1997). Usually called biogenic structures, these

structures can be galleries, casts, mounds, fungus-

comb chambers and so on.

However, recently, Reichman and Seabloom

(2002a), taking the example of pocket gophers,

discussed the validity of the ‘‘ecosystem engineers’’

concept and concluded that it could be considered as

trivial since almost all organisms influence their

environment in one way or another. Discussion

between these authors and Wilby (2002) led to the

conclusion that trophic interactions and ecosystem

engineering are not equivalent, the latter focussing on

the magnitude of the biotically driven physical

influences on ecological processes. Furthermore,

assessment of the engineering concept as bring trivial,

especially in regards to soil physical engineers, results

in part from the way ecosystem engineers are

considered in the context of a top-down approach from

soil engineers to subordinate organisms (Fig. 1).

Through their building activities, ecosystem engineers

have impacts on soil aggregation and porosity, and

hence associated hydraulic properties, and soil organic

matter (SOM) availability for microorganisms (Lavelle

et al., 1997, 2001; Barros et al., 2001). Therefore, these

soil structures can be considered as ‘‘islands’’ in

ecosystems where the diversity and quantity of litter

transformers, micropredators and microorganisms are

often different from those in the surrounding soil and

where nutrient release can be either enhanced or

blocked depending on the age and composition of the

structure (Lavelle et al., 1992, 1997).

A thorough understanding of why organisms can be

regarded as soil engineers requires more than this

purely hierarchical top-down approach, but rather also

the study of how the modifications they create can

influence their biology through feedback effects.

Organisms modifying their environment and control-

ling energy and matter flows are likely to modify

natural selection pressures which are present in their

own local selective environment, as well as in the

selective environments of other organisms (Odling-

Smee et al., 2003). It is therefore essential to establish

the link between the ecological requirements of

engineers and their impacts on ecosystem functioning

P. Jouquet et al. / Applied Soil Ecology 32 (2006) 153–164 155

Fig. 1. Top-down approach from soil engineers to subordinate organisms (microorganisms to plants). The effects of soil-physical engineers on

ecosystem functioning are mediated through the biogenic structures created. Extended phenotype engineers are organisms creating biogenic

structures that directly influence the engineer’s fitness while accidental engineers create structures that have no direct positive effect on

themselves. While there are many published examples showing that the built-structures of soil engineers can influence the soil quality and the

activity of microorganisms and plants, very little is available about the influence of such modifications on the biology and fitness of the engineers

themselves.

(Fig. 1). Jones et al. (1994, 1997) defined the

‘‘extended phenotype engineers’’, recalling the work

of Dawkins (1982), as organisms creating structures or

effects that directly influence the fitness of individuals,

or colonies in the case of the social insects (ants and

termites in our case). Conversely, engineers creating

biogenic structures that have no direct positive effect

on themselves are accidental engineers. According to

these definitions, termites and ants can be considered

as extended phenotype engineers because their

mounds have direct and positive feedback effects on

the colonies through the maintenance of humidity and

protection of the population from enemies (Noirot

et al., 2000; Turner, 2000). Accidental engineers, such

as many earthworms, create structures that are not

directly beneficial to the individuals through feedback

effects. Following the publications of Jones et al.

(1994, 1997), several studies have been conducted on

soil ecosystem engineering and differentiation of

extended phenotype and accidental engineers. The

aim of this paper is to discuss, based on recent studies,

the relevance of the extended phenotype engineers

concept as applied to soil invertebrates and how

engineering outcomes, subject to natural selection,

could have feedback effects on the engineer’s fitness.

2. Termites and ants as extended phenotype

engineers

Ecosystem engineers have significant impacts on

ecosystem functioning at different spatial and tem-

poral scales. Although extended phenotype engineer-

ing is defined by the creation of biogenic structures

having direct positive effects on the engineers

themselves, there may be indirect effects as well.

Two scales of interactions can thus be identified: direct

and indirect effects. However, not all of the indirect

P. Jouquet et al. / Applied Soil Ecology 32 (2006) 153–164156

effects of the biogenic structures on the engineers are

positive. Some results of the engineering activities,

which are ‘‘unintended’’ and therefore are accidental

from the engineers’ point of view, either induce

negative feedback loops on the engineers’ fitness or

are neutral at best.

2.1. Direct positive effects

In the majority of cases, soil engineering activities

of termites and ants are due to the construction of nest

structures for the development of their colonies. The

social organisation and architecture of their nest

structures allow termites and ants to regulate their

environment to some extent and thus to occupy many

different habitats (Curry, 1994). Therefore, the

influence of termites and ants on soil physical and

chemical properties can partly be explained by their

auto-ecological requirements.

Termites are very vulnerable insects that protect

their colonies by improving soil structural stability

against water flux or intrusion of soil invertebrate

predators, in particular ants, into the nests (Hansel,

1993; Noirot et al., 2000; Jouquet et al., 2003, 2004a).

Soils handled by termites are very cohesive and can

resist water disturbance (Garnier-Sillam et al., 1988;

Contour-Ansel et al., 2000; Jouquet et al., 2003, 2004a).

Jouquet et al. (2002) demonstrated that the termite

Odontotermes n. pauperans utilises soil selectively,

favouring finer particles and making structures that

match their ecological needs: to spend less energy (in

term of saliva enrichment) and to maintain a degree of

moisture sufficient for the colony. Korb and Linsenmair

(1998a,b) showed that in order to maintain an optimum

microclimate inside their nest, Macrotermes bellicosus

are able to modify the architecture of their mound nests

according to their requirements in temperature,

humidity and evacuation of CO2. That is also the case

of Kalotermitinae, which are able to build their nest

structures in order to regulate moisture (Grasse, 1984).

Many ground-dwelling ants of temperate zones

build mounds constructed from mineral and plant

materials, food remains and excreta bound together by

mandibular gland secretions. These mounds are

perforated with interconnected galleries and chambers

and the soil beneath the mound also contains chambers

and galleries built from ant-worked soil-organic

materials (Petal, 1978; Holldobler and Wilson,

1990; Curry, 1994). Ants modify the properties of

their nest structures, depending on the nest size and

density of individuals, in order to regulate the

microclimate, particularly with respect to high

temperatures needed within their nests for optimal

brood rearing (Rosengren et al., 1987; Woodell and

King, 1991). Yellow meadow ants (Lasius flavus)

respond to taller vegetation by building larger mounds

with soil excavated from deeper soil layers, thereby

changing the shape of the mound to optimise the

collection of solar radiation (Dlussky, 1981; Blomq-

vist et al., 2000). The large colonies of red wood ants

(Formica s. str.) build complex mounds (ant hills)

constructed from plant materials such as litter and

twigs, and mineral soil with an outer crust-like layer,

reducing loss of heat and moisture. Besides collecting

solar energy the wood-ant mounds store heat produced

by decaying nest materials and ant body metabolism

(see Gosswald, 1989 and Holldobler and Wilson, 1990

for overviews). Harvester ants (Pogonomyrmex spp.)

create and maintain vegetation-free zones around their

nests by removing debris and clipping the vegetation.

It is speculated that the direct positive feedback of

these vegetation-free zones on the colony is a result

of reduced transit time for foragers, decreased risk of

exposure to fire and predation, and increased exposure

to solar radiation (MacMahon et al., 2000). The nest

cones constructed by harvester ants also act as solar

collectors, increasing the time available for foraging

and brood development (Cole, 1994).

These examples show that biogenic structures can

lead to the decrease of environmental hazards and to

the optimisation of colony development. As Jones

et al. (1994) postulated, the nest structures of ants and

termites cannot be considered as accidents but as

responses to their ecological requirements. Such

biogenic structures (mounds, sheetings, galleries,

fungus-comb chambers) are thus the reflections of

the environmental properties and of the engineers’

responses to such properties at a given time. As the

needs of colonies vary with time, we can assume that

the properties of the biogenic structures change

according to the age of the colonies.

2.2. Indirect positive effects

One consequence of soil engineering by termites

and ants is the increase in microbial activities and the

P. Jouquet et al. / Applied Soil Ecology 32 (2006) 153–164 157

release of mineral nutrients such as ammonium and

nitrate (e.g., Abbadie and Lepage, 1989; Brauman

et al., 2000; Dauber and Wolters, 2000; Dauber et al.,

2001; Petal et al., 2003). Soils handled by these

engineers are often enriched in fine particles as well as

in soil organic matter and exchangeable Ca, Mg, K and

Na cations as compared to the surrounding soil (see

Lobry de Bruyn and Conacher, 1990 and Folgarait,

1998 for reviews). Through their impact on soil

fertility, biogenic structures can constitute patches in

the landscape where the availability of soil nutrients

for plants is improved (Konate et al., 1999;

MacMahon et al., 2000; Kristiansen et al., 2001;

Lafleur et al., 2002; Jouquet et al., 2004b). Compara-

tive studies of ant and termite mounds have shown that

these changes in soil properties can be responsible for

changes in morphology and performance of plants and

the composition of plant communities (King, 1977;

Woodell and King, 1991; Dean et al., 1997; Blomqvist

et al., 2000; Folgarait et al., 2002; Jouquet et al.,

2004b). The various direct and indirect interactions

between the engineers and other above- and below-

ground biota are powerful factors in creating spatial

and temporal heterogeneity. As heterogeneity is

thought to be positively correlated with diversity

(Vivian-Smith, 1997), soil engineers could play a key

role in increasing plant species richness or modifying

the plant–community structure of ecosystems.

It has been shown that termite–nest structures are

partially responsible for tree, palm tree and grass

patterns in the Lamto savanna ecosystem (Cote

d’Ivoire) (Mordelet et al., 1996; Barot et al., 1999;

Jouquet et al., 2004b). One can ask if these effects on

vegetation are positive or not for these engineers.

Jouquet et al. (2004b) found that the mounds created

by the fungus-growing termite species, Odontotermes

nr pauperans, influence the grass pattern in a shrubby

savannah of Cote d’Ivoire. They found that a grass

species, Imperata cylindrica, substantially increased

on mounds compared to the surrounding soil. On the

other hand, the grass Andropogon schirensis, very rare

on mounds, was common in the surroundings. As

mounds constitute 9% of the land cover in this

ecosystem, they can be considered as islands where I.

cylindrica is concentrated. Food choice experiments

made by Konate (1998) showed strong termite

preferences in favour of I. cylindrica, as compared

to A. schirensis. Therefore, there is a clear agreement

between plant preferences for soil altered by termite

activity and termite preferences for plant species

growing on their own nests. In this situation, one can

hypothesize that termites indirectly increase their own

food availability. This increasing quantity and quality

of food is probably beneficial to the termites as an

indirect effect, through the increase in colony fitness

(i.e. better nourishment of nymphs, higher alate

production and survival). A comparable example can

be described for harvester ant species. Pogonomyrmex

spp. in the Great Basin and Intermountain Region

shrub-steppe of the western United States commonly

have a perennial bunchgrass, rice grass (Oryzopsis

hymenoides), growing in the cleared areas surrounding

their nests (T.O. Crist personal communication). The

ants seem to selectively retain this grass species on an

area that is otherwise cleared of vegetation (Nowak

et al., 1990). The seeds of the rice grass are highly

preferred by the harvester ants as shown in seed

preference trials (T.O. Crist personal communication).

Nowak et al. (1990) suggest that there is a degree of

indirect facilitation that occurs between the ants and

plants, with the rice grass benefiting from the absence

of neighbouring plant competitors. However, their

study does not complete the linkage in terms of how

ants benefit from the seeds as food. Yet, one can

suggest that they should benefit or otherwise they

would not retain rice grass on their clearings. Other

studies on harvester ants have shown that plants

growing on mounds may benefit from increased seed

production (Brown and Human, 1997). As the

diversity and biomass of harvester ants are suggested

to be food limited (MacMahon et al., 2000), this too

may have a positive feedback on the colonies fitness.

But again, studies documenting such interrelation-

ships are missing.

Very special biogenic structures created by ants are

the so-called ant gardens. These are mutualistic

interactions between specialized epiphytic plants

and ants, mostly in tropical America (Jolivet, 1996).

The ants build nests of carton material constructed

around epiphytic roots, thereby developing aggrega-

tions of artificial soil. The incorporation of epiphyte

seeds into the carton material by ants has been

suggested (Buckley, 1982; Jolivet, 1996; Orivel and

Dejean, 1999). These ant gardens, including sus-

pended soils and epiphytic associations, are habitat for

a multitude of plant species and an associated fauna

P. Jouquet et al. / Applied Soil Ecology 32 (2006) 153–164158

(Jolivet, 1996). A direct positive effect of the

engineering activity lies in the development of a

mutualistic relationships between the ants and the

epiphytes, whereby the ants profit from the roots

forming an integral part of the nest and increasing its

structural stability and an abundant food source close

to the nest such as extrafloral nectar (Buckley, 1982).

Indirect feedback effects on the ants can be either

positive, e.g. the establishment of parabiosis between

different ant species inhabiting the ant gardens, or

negative if ant species are parasitic on ant gardens

(Jolivet, 1996; Orivel et al., 1997).

These examples demonstrate that in some cases,

biogenic structures could also have indirect positive

effects on the fitness of the engineers. It is therefore

probable that the relations between the trophically

subordinate organisms (plants or aphids) and the

engineers are influenced by natural selection. Conse-

quently, in contrast to Jones et al. (1994, 1997), we think

that indirect positive effects must also be considered as

expression of the phenotype of engineers.

2.3. Indirect negative effects

Engineers equally need adaptive reactions to

negative feedbacks. One example of a negative

feedback and the adaptive mechanism evolved was

explored in a study of collective ‘medication’ in red

wood ants (Christe et al., 2003). Nest mounds of red

wood ants (Formica s. str.) are long-lived, consider-

ably warmer than other habitats close to the nest,

stable with respect to the internal temperature and

humidity and rich in organic material (Pokarzhevskij,

1981; Rosengren et al., 1987; Lenoir et al., 2001). The

high temperature and constant moisture in the nest

surface facilitates the development of an abundant and

functionally specialised decomposer community, with

a large biomass concentrated at the lower trophic

positions (Laakso and Setala, 1998). The high-energy

input by the ants favours the growth of heterotrophic

decomposer microbes but might also increase expo-

sure to pathogens (Laakso and Setala, 1998; Schmid-

Hempel, 1998; Christe et al., 2003). Christe et al.

(2003) showed that the three most frequent bacteria

found in nest mounds of Formica paralugubris were

opportunistic pathogens of a variety of organisms. It is

possible that this outcome of the ants engineering

activity can indirectly affect ant performance and can

act as a selective feedback mechanism, which

modifies ant behaviour. Indeed wood ants actively

bring solidified resin into their nests (Lenoir et al.,

1999; Christe et al., 2003). The amount of resin found

in ant-hills of the Formica rufa group can range

between 1 and 44% of the nest material by weight

(Lenoir et al., 2003). Resin, consisting of a mixture of

terpenes and esters, is known to have antibacterial and

antifungal properties. Christe et al. (2003) concluded

from the data obtained in their study, that together, the

finding of common pathogenic bacteria, the general

inhibition of microorganisms by resin, and the specific

inhibition of one potentially detrimental bacterium

suggests that the active incorporating of resin into the

nest mounds is an adaptive mechanism of defence

against pathogens. It might additionally be part of

the price a colony has to pay for creating favourable

conditions for a highly active decomposer community

affecting the physical structure of the nest mound

(Laakso and Setala, 1998; Lenoir et al., 1999).

3. Are earthworms accidental engineers?

Earthworms have been described as being one of

the main groups of soil engineers in tropical and

temperate ecosystems because they change the

structural properties of soil and thus influence soil

microorganisms, SOM regulation and plant growth

(Lavelle et al., 1992; Lavelle, 1997). They act on soil

structures through (i) the creation of burrows which

facilitate water and gas transport, (ii) the incorporation

of litter into the soil, the mixing of soil minerals and

organic material and the breaking down of SOM and

(iii) the ejection of surface and/or subsurface casts

(Brown et al., 2000). Earthworms also have a strong

effect on SOM regulation at four scales of time and

space (Lavelle, 1997):

1. S

hort-term digestion-associated processes: Diges-

tion occurs in the immediate vicinity of micro-

organisms where exoenzymes are active, in the guts

of invertebrates or in the rhizosphere soil close to

active root tips. These microsites are a few cubic

microns to millimetres in volume and processes

develop during periods of hours to a few days.

2. I

ntermediate phase in fresh biogenic structures:

Microbial activation triggered during gut transit or

P. Jouquet et al. / Applied Soil Ecology 32 (2006) 153–164 159

mechanical mixing of organic materials with soil

culminates in fresh biogenic structures, such as

fresh earthworm casts (equivalent to termite faecal

pellets). Activity then progressively decreases

during the few days or weeks following deposition.

3. L

onger term of stabilized biogenic structures:

Some structures created by invertebrates or roots

are highly compact. These structures are the

components of stable macroaggregate structures

that determine soil hydraulic properties and

resistance to erosion (Blanchart et al., 1999;

Chauvel et al., 1999). Their life span may extend

over periods of months to years depending on their

composition and the dynamics of soil structural

features (Decaens, 2000).

4. S

oil profiles: Biogenic structures combine with

other structures of soil to form soil horizons. In

some cases, creeping of soil along slopes may be

triggered by accumulation of surface deposits by

soil invertebrates. As long-term plant successional

processes and pedogenesis operate, changes occur

in soil organism communities and their effects on

soil structure over whole watersheds and time-

scales of years to centuries.

Earthworm activity is also an important factor in

vegetation dynamics and diversity. Brown et al. (2000)

differentiated five different mechanisms by which

earthworms may enhance plant performance: (i)

nutrient release in the rhizosphere, (ii) changes in

soil hydraulic properties, (iii) pest control, (iv)

enhancement of mutualistic microorganisms and

(iv) hormone-like effects. Although all these impacts

of earthworms on soil organisms and plants confirm

the engineering capacity of earthworms (sensu Jones

et al., 1994), one may question whether their

engineering may be favourable to themselves either

directly or indirectly in a feedback effect.

Earthworms can create either permanent or ephem-

eral burrows according to their feeding preferences

(Lee, 1985). Epi-anecic species consume mostly plant

litter and create more or less permanent burrows that are

formed as shelters from unfavourable environmental

conditions, such as dryness or high temperatures. The

main effect of epi-anecic earthworms is to place the

litter within the soil, in their permanent burrows and

casts which can be considered as ‘external rumens’

(comparable in their function to the fungus of exo-

symbiotic ants and termites), in which microbes

multiply and to where other fauna are attracted. This

activity enhances the degradation of uningested litter

and organic fragments in and around the casts resulting

in an increase in the palatability of SOM, which is then

reingested by earthworms (see Brown et al., 2000 for a

review). Consequently, the creation of burrows and

casts by epi-anecic earthworms can be considered as an

efficient feeding strategy, and in this case we can

assume that the fitness of these engineers depends on

the properties of the structures they build (casts and

burrows). From this viewpoint, biogenic structures may

be considered as responses to their ecological require-

ments and thus epi-anecic species are extended

phenotype engineers (sensu Jones et al., 1994).

Conversely, geophagous species move through the soil

in order to live as close as possible to their thermal,

moisture and feeding optima. Therefore, we assume

that they depend more on the environmental conditions

than epi-anecic earthworms, which are able to control

their environment by living in their structures. The

engineering of geophagous species might thus be

considered as accidental, since they do not directly

influence the fitness of earthworms. However, one may

argue that geophagous earthworms are also able to

change the environmental conditions of a whole

ecosystem due to their high mobility and biomass

and thereby create environmental conditions that might

positively or negatively influence their fitness in a

feedback effect.

Blanchart et al. (1999) distinguished two functional

groups according to the casts of geophagous earth-

worms. Castings are egested in two main forms:

globular and granular. Globular casts are large and

produced by ‘compacting’ earthworm species, and

therefore tend to be more stable and longer lasting than

the granular casts produced by ‘de-compacting’

species. There can be interesting interactions between

these structures in that de-compacting species do not

seem to be able to feed on their own casts but may

ingest casts of compacting species and vice versa

(Blanchart et al., 1999). Consequently, we assume that

feedback effects of geophagous earthworm engineer-

ing could be initially negative for their own fitness. A

spectacular example of a negative feedback engineer-

ing effect is the overdominance of Pontoscolex

corethrurus (Glossoscolecidae, Oligochaeta) in pas-

ture soils. This species reduces the soil macroporosity

P. Jouquet et al. / Applied Soil Ecology 32 (2006) 153–164160

and creates a crust at the soil surface, made of a

continuous layer of compact casts upon which they

cannot feed (Chauvel et al., 1999). Through its

dramatic effect on soil properties, it also decreases the

biomass of plants and then the SOM content.

However, the effects of de-compacting species usually

counterbalance those of compacting species in the

field. Thus, in a second step, the casts produced by one

functional group would have positive effects for the

opposite functional group, which in turn produces

casts that are fed on by the species of the first

functional group. This mutualistic interaction between

both functional groups has raised questions about the

evolutionary significance of this relationship and

further studies have to determine whether the

palatability of the food for de-compacting species is

improved in the casts of compacting species, and vice

versa. In either case, this illustrates that the engineer-

ing of geophagous earthworms may also have positive

indirect effects for themselves if both functional

groups are present in the field.

4. From the engineering strategy of organisms

to the functioning of ecosystems

This review stresses the complexity and the

multiplicity of the scales of interactions between

the impacts of the engineers on ecosystem functioning

and their ecological requirements. We tried to

demonstrate that impacts of soil engineers can be

either direct or indirect responses of their biological

requirements and that biogenic structures are dynamic

and adaptive depending on the species studied. In the

case of ants and termites, such structures can be

considered as expressions of their requirements, and

more precisely as a trade-off between growth and

protection of the colony against predators, water flux

and drought and the energetic cost for their construc-

tion. The biogenic structures are therefore necessary

for termites and ants and their fitness will depend on

the efficiency of the structures they build. In the case

of epi-anecic earthworms, biogenic structures can be

considered as direct responses of their ecological

requirements and the species are extended phenotype

engineers (sensu Jones et al., 1994). Conversely,

geophagous species are accidental engineers since the

physical structures they create are not for their own

direct benefit, i.e., they do not directly increase the

organisms fitness, although these structures can be

advantageous or dis-advantageous in a longer time

scale, depending upon whether both functional groups

(compacting versus de-compacting species) are pre-

sent.

The differentiation amongst extended phenotypic

and accidental engineers may be an interesting

concept for thoroughly understanding the impact of

soil engineers on ecosystem functioning. The produc-

tion of biogenic structures is the most important

parameter that differentiates soil engineers from other

soil organisms. From this point of view, and unlike

Reichman and Seabloom (2002b), we assume that in

soil, the concept of ecosystem engineering is not

trivial because it allows quantification of the nature

and scope of the influences of different kinds of

engineering activities. Furthermore it draws attention

to the evolution (and co-evolution) of soil engineering

strategies, which, when affecting multiple genera-

tions, introduces a second general inheritance system

in evolution that is working via environments (Odling-

Smee et al., 2003).

One important difference between both types of

engineers is the amplitude of their influence on soil

spatial and temporal heterogeneity (Fig. 2). Soil

engineers affect soil processes and heterogeneity at

widely different scales, ranging from soil aggregates

and SOM dynamics to vegetation patterns and land-

scapes (Jones et al., 1997; Wilby et al., 2001). Primary

soil heterogeneity is affected at the scale of aggregates.

However, the lifespan and size of their sphere of

influence, or functional domain (i.e., drilosphere,

termitosphere and myrmecosphere, sensu Lavelle,

2002) greatly depend on the functional groups

considered. Earthworms have an aggregated distribu-

tion in soil. In the drilosphere, earthworms particularly

influence crumb structure, particle aggregation and

SOM dynamic, resulting in horizontal mixing and then

homogeneization of soil. As a consequence, the activity

of earthworms appears to be uniformly distributed in a

horizontal dimension in the upper 20 cm of soil. While

earthworms appear to contribute a lot in terms of

heterogeneity at a lansdscape scale, they contribute

little within their own functional domain. In contrast,

termite and ant activities are mainly concentrated in

their nests and galleries and they tend to increase lateral

patch scale heterogeneity with more or less long-term

P. Jouquet et al. / Applied Soil Ecology 32 (2006) 153–164 161

Fig. 2. Link between the biology of ecosystem engineers and ecosystem functioning within their sphere of influence. Ecosystem engineers can

be considered as both extended phenotype and accidental engineers depending on their life strategy and mobility. The more species can move

through the soil, the less they are able (or need) to control their environment and the more they can be considered as accidental engineers. The

more engineers are of the ‘‘extended phenotype’’ type, the more impact they have on soil heterogeneity and the more they create long lasting

structures where the nutrients available for the subordinate organisms (microbes and plants) are concentrated.

consequences for vegetation and pedogenesis (Lavelle

et al., 1992). In this case, we argue that the sphere of

influence of accidental soil engineers, i.e. most of the

earthworm species, encompasses extensive spatial

areas due to the burrows and macroaggregates they

create through their movement for foraging in soil.

Thus, they may contribute to the homogenisation of the

soil physical and chemical properties in the whole

ecosystem (Kretzschmar, 1989). Extended phenotype

engineers in contrast have spheres of influence, which

are more limited in spatial extent by creating more

permanent structures such as nests of ants and termites.

It is therefore important to realise that in addition to the

biogenic structures, the size and the lifespan of the

functional domains of soil engineers are responses to

their auto-ecological requirements.

We have tried in this review to illustrate that

distinguishing between accidental and extended

phenotype engineering can be rather difficult. This

distinction is not only semantic but also makes it

possible to better appreciate the functioning of

ecosystems. In modifying the distribution and avail-

ability of soil nutrients, soil engineers influence

ecosystem services such as maintenance of biodiver-

sity, stability, nutrient cycling and biomass production

(http://www.milleniumassessment.org) since all of

these are directly linked to heterogeneity. Strategies

of engineers, and thus their functional domains,

influence the scale at which soil engineers affect

heterogeneity in ecosystems. It is therefore necessary

to study the links between their impact on ecosystem

functioning and their ecological requirements, their

P. Jouquet et al. / Applied Soil Ecology 32 (2006) 153–164162

ability to respond to their environment, as well as their

relationships with other soil engineers in order to

understand the structure of heterogeneity and then the

functioning of ecosystems. This viewpoint offers

many interesting challenges for the future, particularly

in agro-ecosystems where soil engineers play roles in

nutrient cycling that are often underestimated.

Acknowledgements

We are also grateful to Pradeep Panigrahi, Francoise

Binet, Daniel Cluzeau, Paul Leadley and Franck

Courchamp for valuable discussions. This work was

supported by the IRD and Paris XI University (France).

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