Termites: The Neglected Soil Engineers of Tropical Soils

Abstract

Termites are undoubtedly key soil organisms in tropical and subtropical soils. They are soil engineers in influencing the physical, chemical, and biological properties of soils and, consequently, water dynamics in tropical and subtropical ecosystems. To appreciate the effect of termites on soil, there is a need for a thorough understanding of the ecological needs and building strategies of termites and the mechanisms regulating termite diversity at local and regional scales. Termite impacts on soil properties and water dynamics can be differentiated at four different scales: (i) at the landscape scale, where termites act as heterogeneity drivers; (ii) at the soil profile scale, where termites act as soil bioturbators; (iii) at the aggregate scale, where they act as aggregate reorganizers; (iv) and last, at the clay mineral scale, where they can act as weathering agents. Last, we discuss recent literature on termite engineering published in the last 10 years in the major journals of soil science and suggest new research topics that could contribute to improved knowledge of the impact of termites on soil properties and water dynamics.

Full text

Termites: The Neglected Soil Engineers of Tropical Soils
Pasc a l Jouque t ,
1,2
Nicolas Bottinelli,
1
Rashmi R. Shanbhag,
3
Thomas Bourguignon,
4
Saran Traoré,
5
and Shahid Abbas Abbasi
6
Abstract: Termites are undoubtedly key soil organisms in tropical and
subtropical soils. They aresoil engineers in influencing the physical, chem-
ical, and biological properties of soils and, consequently, water dynamics
in tropicaland subtropical ecosystems. To appreciate the effect of termites
on soil, there is a need for a thorough understanding of the ecological needs
and building strategies of termites and the mechanisms regulating termite
diversity at local and regional scales. Termite impacts on soil properties
and water dynamics can be differentiated at four different scales: (i) at the
landscape scale, where termites act as heterogeneity drivers; (ii) at the soil
profile scale, where termites act as soil bioturbators; (iii) at the aggregate
scale, where they act as aggregate reorganizers; (iv) and last, at the clay
mineral scale, where they can act as weathering agents. Last, we discuss
recent literature on termite engineering published in the last 10 years in
the major journals of soil science and suggest new research topics that
could contribute to improved knowledge of the impact of termites on soil
properties and water dynamics.
Key Words: Termites, soil engineers, spatial and temporal scales,
water dynamics
(Soil Sci 2016;181: 157–165)
In the tropics, arthropods, particularly insects, make up the ma-
jority of known biodiversity. In these environments, termites
(Isoptera) are arguably among the most dominant and important
soil organisms (Black and Okwakol, 1997). Subjective assess-
ments of the importance of termites, based on observations of
their very high population densities, are now supported by a num-
ber of thorough studies that suggest that they may represent 40%
to 65% of the overall soil macrofaunal biomass in some biotopes,
with values comparable to the biomass of ungulate and megaher-
bivores (Loveridge and Moe, 2004). Studies in Africa, and to a
lesser extent in Australia, Southeast Asia, and South America,
focusing on savannah, bushlands, and rain forests suggest that
termites are involved in many essential ecological processes. They
play an important role in the decomposition of litter on the ground,
the regulation of soil structure, soil organic matter (SOM) and
nutrient cycling, water dynamics, soil erosion, plant growth, and
overall biodiversity (see Holt and Lepage, 2000; Jouquet et al.,
2011; Bottinelli et al., 2015, for reviews). Thus, because of their
abundance and impact on a large number of ecosystem functions,
the role of termites in most tropical and subtropical ecosystems
is considered to be similar or even more important than that of
earthworms. For the same reason, they are called “keystone spe-
cies”or “soil engineers”(Black and Okwakol, 1997; Jouquet
et al., 2006). However, in contrast to the large body of knowledge
that has been acquired on the impact of earthworms on soil porosity
and water dynamics in temperate ecosystems (i.e., Bottinelli et al.,
2015; Capowiez et al., 2014; Lévêque et al., 2015; Pagenkemper
et al., 2015), there is a paucity of information on the influence of
termites in most tropical ecosystems and, in most cases, any com-
parison between earthworms and termites remains speculative.
The aims of this review are to (i) discuss the major impacts
of termites on soil structure and water dynamics in tropical soils
and (ii) suggest new research topics that could help reduce the
gap between our knowledge on earthworm bioturbation and that
of termites.
WHY ARE TERMITES BIOTURBATORS?
Termite ecology and soil functioning are two closely related
concepts. Termites use soil from various soil depths or specifically
select soil particles of small sizes for the construction of their
aboveground and belowground nests (Jouquet et al., 2011). They
also build galleries for foragingbelowground and translocate large
quantities of soil on the ground for harvesting litter (leaves, wood,
and herbivore dung), so-called termite sheetings. In doing so, they
substantially modify the physical, chemical, and biological prop-
erties of the soils (Holt and Lepage, 2000; Jouquet et al., 2011,
2015; Bottinelli et al., 2015). Although understanding how ter-
mites act as soil bioturbators seems to be a simple question, it is
far from being trivial. Earthworms modify soil properties because
they partially or exclusively feed on soil. This feeding strategy
might in itself justify the fact that they live in soil and conse-
quently have a significant impact onits propertieswhen ingesting
and egesting it (the formation of casts) and moving in it (the for-
mation of galleries). This, however, is not the case for termites
that feed on aboveground litter, with the exception of soil feeding
termite species. From an ecological point of view, the transloca-
tion of soil and the formation of galleries by termites can be seen
as a huge investment in terms of energy. In this context, why
should termites spend so much energy living belowground and
modifying the physical and chemical properties of soils? It seems
that termites are weak and relatively fragile invertebrates and use
soil bioturbation as a strategy for protecting themselves against
vertebrate and invertebrate predators and sunlight as well as to
control their environment (Korb and Linsenmair, 1998, 2000).
This close dependence between termite fitness and soil properties
is stressed by the “extended phenotype engineering”concept
(Jones et al., 1994) that states that termites are “intended engi-
neers”(in contrast to “accidental engineers”) that modify the soil
properties with purposes according to their ecological needs
(Turner, 2004; Jouquet et al., 2006). For example, several studies
showed that termites modify their long-lasting and robust de-
signed structures more than short-lived and less important ones
(Jouquet et al., 2005a; Abe and Wakatsuki, 2010). This has direct
1
Institute of Ecology and Environmental Sciences (UMR 242 iEES Paris), Insti-
tute of Research forDevelopment, Bondy, France.E-mail: pascal.jouquet@ird.fr
2
Indo-French Cell for Water Science, Civil Engineering Department, Indian In-
stitute of Science, Bangalore, Karnataka, India.
3
Institute of Wood Science and Technology, Bangalore, Karnataka, India.
4
School of Biological Sciences, University of Sydney, Sydney, New South
Wales, Australia.
5
UFR/ST, Université Polytechnique de Bobo, Burkina Faso.
6
Centre for Pollution Control and Environmental Engineering, Pondicherry
University, Puducherry, India.
Address for correspondence: Dr. Pascal Jouquet, Institute of Ecology and Envi-
ronmental Sciences (UMR 242 iEES Paris), Institute of Research for Develop-
ment, 32 av. H. Varagnat, 93143 Bondy, France.
Financial Disclosures/Conflicts of Interest: This project was supported by the
French National Program EC2CO-Biohefect “MACROFLUX.”T. Bourguignon
was supported by a Sydney Postdoctoral fellowship.
Received May 9, 2015.
Accepted for publication July 21, 2015.
Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.
ISSN: 0038-075X
DOI: 10.1097/SS.0000000000000119
TECHNICAL ARTICLE
Soil Science •Volume 181, Number 3/4, March/April 2016 www.soilsci.com 157
Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.

positive impacts in terms of resistance and maintenance of humid-
ity and temperature and indirect positive impact by increasing the
amount of food available on some occasions (Jouquet et al., 2006).
Furthermore, the impact of termites on soil functioning is also
dependant on their construction strategies. Termites are highly euso-
cial with a clear hierarchy and sharp division of labor across the
hierarchy. They live in colonies with either single nests or several
interconnected nests. The concentration of termite activity into
one single location increases heterogeneity in the landscape, with
termite nests acting as resource or activity hotspots. They become
patches or “islands”in the landscapes where different rates and/or
nature of ecological processes occur than in the bulk soil (Jouquet
et al., 2005b; Bonachela et al., 2015). Once the colony at the ori-
gin of the patch dies, other termite colonies and inquilines species,
soil invertebrates, and specific plant species colonize the nest
structure and continue to maintain it, increasing spatial heteroge-
neity of that specific biotope for a long period, from years to cen-
turies (e.g., Traoré et al., 2008, 2015; Rückamp et al., 2012; de
Oliveira et al., 2014; Erens et al., 2015). This is, for example,
the case for Macrotermes subhyalinus or Trinervitermes species
members that are observed in mounds built and abandoned by
Macrotermes bellicosus in West Africa (Traoré, personal obser-
vation). This is also the case of heuweltjies mounds in South Africa
that are thought to be built by the harvester termite Microhodotermes
viator and that have been present in the landscape for at least
the last 36,000 years (Potts et al., 2009 from Francis et al.,
2013). On the other hand, the division of termite colonies into
small, and sometimes short-lived, structures tends to increase
heterogeneity at a small (i.e., from micrometers to centimeters)
and sometimes short scale (i.e., several months) and with a low
intensity but leads to the homogenization of the soil physical
and chemical properties in the whole ecosystem during a long
period (Jouquet et al., 2006). Consequently, it seems that termites
are not passive bioturbators and that understanding their influence
on soil functioning requires knowledge of their ecological needs
and nest-building strategies.
THE INFLUENCE OF TERMITES ON SOIL
STRUCTURE: A FUNCTIONAL,
PHYLOGEOGRAPHIC, HIERARCHICAL,
AND DYNAMIC APPROACH
Three functional groups are usually recognized to differenti-
ate the impact of termites on nutrient cycling and soil functioning:
the soil feeders, the grass/litter feeders (except fungus-growing
termites), and the fungus-growing termites (Termitidae, subfamily
Macrotermitinae). The first two groups consume organic matter
(e.g., humus, ingested with variable amounts of mineral material,
standing, or lying dead wood, grassy litter, herbivore dung) and
build their nests and line their galleries with soil particles glued
together with fecal matter. In contrast, fungus-growing termites
do not incorporate feces into their constructions, or do so only
rarely, and use saliva as a “binding agent”(Garnier-Sillam and
Harry, 1995). Consequently, the soil worked by soil and litter feeders
contains more SOM than the surrounding soil environment,
whereas the soil worked by fungus-growing termites usually con-
tains less SOM (Jouquet et al., 2011). Obviously, this difference in
SOM content influences a large number of soil properties such
as the stability of soil aggregates, their water-holding and cation
exchange capacities, sorption and availability of nutrients, soil
microbial communities, and so on (e.g., Duponnois et al., 2005;
Jouquet et al., 2005c; Lopez-Hernandez et al., 2006; Rückamp
et al., 2010).
Termites are classically separated into the paraphyletic
“lower”termites and the monophyletic “higher”termites. Lower
termites include Mastotermitidae, Kalotermitidae, Hodotermitidae,
Archotermopsidae, Termopsidae, Stylotermitidae, Rhinotermitidae,
and Serritermitidae. Higher termites are gathered into a single
family, the Termitidae, which comprises approximately 75% of
all modern termite species (Krishna et al., 2013). All lower ter-
mites feed on wood, whereas the diet of higher termites is highly
diversified, with species feeding on a gradient of organic matter
ranging from wood to soil (Donovan et al., 2001; Bourguignon
et al., 2011). There seems to be imbalances in taxonomic studies
on termite diversity around the world because the termite fauna
of America, Asia, and Australia have been little documented com-
pared with that of Africa. In addition, termites are unequally distrib-
uted between continents, and their abundance follows the sequence
Africa > South America > Southeast Asia > Australia (Davies et al.,
2003). The primary cause of this pattern is historical, and the higher
termites likely originated 50 million years ago in Africa and dis-
persed worldwide after the Gondwana broke up (Eggleton, 2000;
Bourguignon et al., 2015). As a consequence, wood feeders are
present worldwide, soil feeders are absent in Australia and are most
abundant in Africa followed by South America and Southeast Asia,
and the fungus-growing termites are present in Africa and South-
east Asia only. At a local scale, any change in land use or modifica-
tion of natural habitats as a consequence of global change (e.g.,
forest logging and global warming) also affects termite diversity.
Evidence of reduced termite diversity or modification after ecosys-
tem perturbation has been reported on several occasions. For in-
stance, wood-feeding termites are considered to be more resilient
to perturbation than soil-feeding termites, which are particularly
vulnerable to disturbances (Jones et al., 2003). In specific conditions,
wood- and litter-feeding termites, especially the fungus growers
Macrotermitiane, may even show positive responses and increase
in abundance because of the accumulation of litter, dead wood
biomass, or crop residues (Attignon et al., 2005). These global
patterns of termite distribution at local or regional scales undoubt-
edly create differences in bioturbation rates and processes.
The influence of termites on soil structure is dynamic and, in
a recent review, Bottinelli et al. (2015) differentiated three scales
at which termites can have an impact on soil structure. First, at
the scale of clay mineral particles, some specific termite species,
mainly fungus-growing termite species from the Macrotermitinae
subfamily, act as “mineral-weathering agents”by hastening the
weathering of clay minerals (Jouquet et al., 2002, 2007b; Mujinya
et al., 2011) or altering iron sesquioxides (Abe and Wakatsuki,
2010). However, as highlighted by Bottinelli et al. (2015), very little
information is available on this topic, and further studies are
required to determine if these examples can be generalized. Ter-
mites can also be considered as “soil aggregate reorganizers”at
the scale of soil aggregates, modifying their internal organization
and chemical properties for the production of their nest structures
(Jungerius et al., 1999). For example, termites play an important
role in the dynamics of soil aggregation in Brazilian Ferralsols. In
this soil, termite bioturbation is responsible for the specific granular
properties of soil microaggregates (50–250 μm in diameter),
whereas macroaggregate (500–1,000 μm in diameter) formation
is attributed to earthworm activity (Balbino et al., 2001, 2002;
Schaefer, 2001; Reatto et al., 2009). Last, termites can also play
the role of “bioturbators”at the profile scale with the translocation
of soil particles (mainly clay), soil aggregates (e.g., for the produc-
tion of termite sheetings covering the litter they consume), the pro-
duction of galleries, and the construction of epigeous mounds and
subterranean nests with specific chemical and physical properties
(Jouquet et al., 2011). Although the properties of these above-
ground nests are variable and depend on the termite feeding
group, they generally contain increased amounts of clay and cat-
ion contents. More SOM is also usually measured in termite nests,
Jouquet et al. Soil Science •Volume 181, Number 3/4, March/April 2016
158 www.soilsci.com © 2016 Wolters Kluwer Health, Inc. All rights reserved.
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except in the case of the fungus-growing termite nests that display
variable, but generally lower, SOM content compared with the
surrounding soil environment (Contour-Ansel et al., 2000; Fall
et al., 2001; Jouquet et al., 2004).
In addition to the classification of Bottinelli et al. (2015),
several studies suggested that termites can also act as “ecosystem
heterogeneity drivers”through the creation of “patches”or “high-
lands”of fertility that impact the functioning of the entire landscape
for a long period in some situations (Fig. 1) (Jouquet et al., 2007).
This effect of termites has mainly been highlighted in Africa
where termites produce epigeous mounds or termitaria with spe-
cific chemical properties (e.g., Muvengwi et al., 2013; Seymour
et al., 2014) and in Asia where they are conspicuous features in
paddy fields (Choosai et al., 2009). Although large mounds only
represent a minor proportion of landscapes (2–10/ha on average),
these patches of high-quality resources can be particularly im-
portant in nutrient-poor ecosystems, influencing mineral composi-
tion, nutrient cycling, topography, and fluxes in landscapes (Konaté
et al., 1999; Mills et al., 2009; Sileshi et al., 2010, from Seymour
et al., 2014). The concentration of clay, SOM, macronutrients, and
micronutrients in termite nest structures are also “fertile islands”
or “nutrient hotspots”for plants, other soil invertebrates, and large
herbivores (Mwabvu, 2005; Traoré et al., 2008, 2015; Choosai
et al., 2009; Erpenbach et al., 2013; Muvengwi et al., 2013,
2014; Van der Plas et al., 2013; Seymour et al., 2014). Termite
mounds have also been considered as focal points for tree regen-
eration within savannahs (Moe et al., 2009; Traoré et al., 2008,
2015) and can influence the productivity of the entire biome in
some circumstances (Pringle et al., 2010; Erpenbach et al.,
2013; Seymour et al., 2014; Muvengwi et al., 2014). They also
provide a hedge against drought, thereby increasing the level of
landscape resistance (Bonachela et al., 2015).
IMPACT OF TERMITES ON WATER
DYNAMICS AND RESISTANCE OF SOIL
TO WATER DEGRADATION
Termite bioturbation can influence water dynamics at the
same four scales of observation as above (Fig. 1).
At a small scale, any changes in clay and SOM contents and
quality, as well as in soil porosity, are likely to influence the soil
water-holding capacity and resistance to degradation by water.
The positive influence of termites on soil water-holding capacity
is widely recognized and has been highlighted on several occasions
for several trophic groups (Wood and Sand, 1978; Dangerfield
et al., 1998; Konaté et al., 1999; Jouquet et al., 2004; Dawes,
2010). Quantitative information on the effects of termites on soil
aggregate dynamics remains sparse at this scale of observation
and is mainly limited to comparisons between the soil aggregate sta-
bility of termite-worked soils (usually termite mounds) and that of
the surrounding soil environment. The influence of termites on soil
aggregate stability is directly linked to the specific dietary habits of
termites, the soil material used for nest making, and the ecological
importance of the termite structures (Jouquet et al., 2006, 2011).
FIG. 1. How termites influence soil structure and water dynamics depends on their capacity to produce galleries and modify soil
aggregates and mineral properties. Four groups can be differentiated: (i) the ecosystem heterogeneity drivers impacting heterogeneity and
hydrology at the landscape scal e; (ii) the sensu stricto bioturbators influencing soil dynamics at the profile scale, leading to modification inwater
infiltration; and (iii) the soil aggregate reorganizers and (iv) mineral-weathering agents influencing clay properties and water-holding
capacity at the soil aggregate and clay scales. Figure modified from Bottinelli et al. (2015).
Soil Science •Volume 181, Number 3/4, March/April 2016 Termites as Neglected Soil Engineers
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TABLE 1. Articles Referenced in the Web of Science Database From 2005 to 2015 in Selected Journals in Soil Science and Biology With High-Impact Factors†and Reporting Direct
Evidence of the Impact of Termites on Soil Physical, Chemical, and Biological Properties and Water Dynamics
Scale
Journals and Articles Clay Aggregate Profile Landscape Country
Applied Soil Ecology
Moura et al. 2015 Water infiltration Brazil
Jouquet et al. 2012 Dynamics of aggregates Soil erosion Vietnam
Rückamp et al. 2009 Chemical properties Brazil
Ayuke et al. 2011 Dynamics of aggregates Kenya
Bezerra-Gusmao et al. 2011 C cycling Brazil
Rückamp et al. 2009 Nitrate and DOC leaching Brazil
Jimenez et al. 2008 Chemical properties Colombia
Ackerman et al. 2007 Chemical, physical, and
hydraulic properties Brazil
Biology and Fertility of Soils
Costa et al. 2013 Microbial properties Brazil
Brossard et al. 2007 Chemical properties Stocks of nutrients Burkina Faso
Lopez-Hernandez et al. 2006 Chemical properties Venezuela, Côte d'Ivoire
Jouquet et al. 2005a Clay mineralogy Chemical and physical
properties Côte d'Ivoire
Catena
Mujinya et al. 2014 Physical properties Chemical and physical
properties Spatial distribution Congo
Francis et al. 2013 Clay mineralogy Soil properties Water infiltration in mound South Africa
Sarcinelli et al. 2009 Physical, chemical, and
micromorphological
properties
Termite mound distribution
along a toposequence Brazil
Reatto et al. 2009 Microaggregate properties Chemical and physical
properties Brazil
European Journal of Soil Biology
Diouf et al. 2006 Microbial properties Senegal
Jimenez and Decaens. 2006 Chemical properties Spatial variability Colombia
Mora et al. 2006 Spatial and temporal
variability Senegal
Jouquet et al. Soil Science •Volume 181, Number 3/4, March/April 2016
160 www.soilsci.com © 2016 Wolters Kluwer Health, Inc. All rights reserved.
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European Journal of Soil Science
Geoderma
De Oliveira et al. 2014 Clay mineralogy Microstructural
transformation Chemical and physical
properties Brazil
Mujinya et al. 2013 Clay and oxides properties Clays and oxides properties Congo
Rückamp et al. 2012 Chemical properties Soil genesis Brazil
Mujinya et al. 2011 Origin of carbonate Chemical and physical
properties Congo
Mujinya et al. 2010 Soil properties Congo
Rückamp et al. 2010 Chemical properties Brazil
Sako et al. 2009 Clay mineralogy Chemical properties Namibia
Obi and Ogunkunle. 2009 Soil spatial variability Nigeria
Cosarinsky and Roces. 2007 Micromorphology Soil properties Argentina
Breuning-Madsen et al. 2007 Soil translocation Soil translocation Ghana
Jouquet et al. 2007a Clay mineralogy Côte d'Ivoire
Pedobiologia
Abe and Wakatsuki. 2010 Sesquioxide alteration Nigeria
Villenave et al. 2009 Biological properties Senegal
Soil Biology and Biochemistry
Dahlsjo et al. 2014 Chemical properties Peru
Seymour et al. 2014 Spatial variability Zimbabwe
Renard et al. 2014 Dynamic of aggregates French Guiana
Griffiths et al. 2013 Chemical properties Kenya
Dawes. 2010 Soil porosity, penetration
resistance, and water storage Australia
Bandowe et al. 2009 Chemical properties Brazil
Jimenez et al. 2006 Chemical properties Spatial heterogeneity Colombia
Jouquet et al. 2005c Microbial properties Côte d'Ivoire
Roose-Amsaleg et al. 2005 Physical and biological
properties Gabon
Mora et al. 2005 Biological activity Colombia
Soil Science
Soil and Tillage Research
Articles are classified according to country study and scale of observation where main functions measured are listed. Review articles and articles focused on termite diversity were not considered.
†In alphabetic order: Applied Soil Ecology,Biology and Fertility of Soils,Catena,European Journal of Soil Biology,European Journal of Soil Science,Geoderma,Pedobiologia,Soil Biology and Biochemistry,
Soil Science,Soil and Tillage Research.
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For example, fungus-growing termites enrich their nests in clay
but tend to reduce their SOM content, whereas soil-feeding ter-
mites always increase the SOM content of their nest structures
(Jouquet et al., 2011).As a consequence, fungus-growing termites
usually have a negative impact on soil aggregate resistance to
water, whereas soil-feeding termites have a positive one (Contour-
Ansel et al., 2000; Jouquet et al., 2004).
At a medium (i.e., soil profile) scale, the production of a
dense network of foraging galleries connected to the soil surface
also usually improves water infiltration (Mando et al., 1996; Léonard
and Rajot,2001; Léonard et al., 2004). However, the translocation
of hundreds of kilograms to tons of soil per hectare on the ground
for harvesting leaves, wood, and herbivore dung (termite sheet-
ings) (Wood and Sand, 1978; Bagine, 1984) can rapidly generate
structural crusts that foster water runoff and soil detachment
(Jouquet et al., 2012; Bargués Tobella et al., 2014). The degrada-
tion of termite mound nests by rain or organisms (i.e., termitophilous
vertebrates and mammals feeding on termite-worked soils) can
also form seals that locally reduce water infiltration (Janeau and
Valentin, 1987). Therefore,the final impact of termites on soil hy-
drological properties results from the balance between processes
favoring soil infiltrability (i.e., the formation of open galleries
on the soil surface) and those fostering the formationof imperme-
able erosion crusts and the detachment of soil aggregates (i.e.,the
degradation of soil sheetings).
Last, at a larger scale, the concentration of nutrients and the
presence of specific vegetation on termite mounds can also have
an impact on the hydrological characteristics of watersheds in cer-
tain situations. Using rainfall simulations, Bargués Tobella et al.
(2014) measured the highest preferential flow under trees asso-
ciated with termite mounds in agroforestry systems in Burkina
Faso. Intermediate results were obtained under single trees, and
the lowest values were obtained in the open areas. Thus, the increas-
ing organic matter and better microclimate beneath trees enhance
termite activity, which in turn contributes to better preferential
flow (but not infiltrability) and groundwater recharge (Bargués
Tobella et al., 2014). Similar results were observed in the Amazon
where the water-holding capacity was reduced but water infiltra-
tion increased in termite mound soil (Ackerman et al., 2007). A re-
cent study (Bonachela et al., 2015) even suggested that termite
mound nests may increase the robustness or resilience of African
dryland ecosystems against water shortage and desertification.
HOW DO WE FILL IN THE GAP?
Compared with earthworms, little is known about the influ-
ence of termites on soil functioning. For example, approximately
10 times more articles on earthworms than on termites are refer-
enced in the Web of Science database (7,464 and 767 articles,
respectively, using the key words “soil”and either “earthworms”
or “termites”from 2005 to 2015). Furthermore, whereas the en-
gineering effects of earthworms were studied across several coun-
tries from five continents (Blouin et al., 2013), studies on termites
as soil engineers have been mainly confined to sites in Africa and
South America. Only 44 recent research articles (reviews were not
included)in the top 10 soil science journals (Table 1) investigated
the direct influence of termites on these four scale processes (key
word search “soil”and “termites”) in the last 10 years (2005–2015).
From this list, 21 studies were carried out in Africa (mainly in West
Africa and in particular in the Côte d'Ivoire, Burkina Faso, Senegal,
and Nigeria) and 20 in South America (mainly in Brazil), with only
one study each in Asia (Vietnam) and Oceania (Australia). Thus,
it seems that more research is needed in the Asia-Pacific region,
which has been neglected so far. Table 1 also shows that most
(n= 28) of the referenced articles focused on the influence of
termites on soil properties at the soil aggregate scale, often by
comparing soil properties (collected from the aboveground mounds
or soil sheetings) with the surrounding soil environment. In con-
trast, less has been done at the smallest (eight articles) and largest
scales (11 articles), highlighting the need for studies at additional
levels of complexity and scales of time and space.Information about
the properties of subterranean termite nests is also scarce, although
the density and abundance of these belowground soil structures often
exceed that of those observed aboveground (Jouquet et al., 2004).
From this list of articles, it also seems that more research is needed
on the impact of termite bioturbation activity on water dynamics.
This question has mainly been developed in studies of soil aggregate
stability of termite mound soils and water infiltration on these struc-
tures. In contrast, very little information is available on the influence
of termite foraging activity on soil porosity and water dynamics.
Last, another knowledge gap is the predominance of research
on natural or seminatural habitats, with much less focus on culti-
vated lands—either agricultural or agroforestry systems. This is
perhaps caused by the fact that researchers have focused on ter-
mites as pests in agroecosystemsand that tillage or land clearance
usually has a negative impact on termite abundance and diversity
(Black and Okwakol, 1997). Hence, a key challenge is to consi-
der the crucial roles played by termites in natural systems and
to promote their activities to improve agroecosystem function-
ing. Unfortunately, very little is known about the potential of
using termite activity to restore or improve ecosystem functioning
(20 articles for termites compared with 85 and 6,358 articles, for
earthworms and plants, respectively, as referenced by Jouquet
et al., 2014). Most of these articles were limited to demonstrating
that the application of mulch stimulates termite activity in semi-
arid environments (e.g., Mando et al., 1996; Dawes, 2010), then
highlighting the fact that termites improve soil porosity, water in-
filtration, and sometimes plant diversity and productivity. The
usefulness and efficiency of this approach in other environments
and climates, however, remain unknown. For example, the stimu-
lation of termite activity by mulch application has been proposed
for improving soil fertility in the subarid environments of India,
which are similar to those observed in West African sub-Sahelian
and Australian environments, but this approach has not been
tested so far (Pardeshi and Prusty, 2010).
CONCLUSIONS
Our knowledge of the impact of termites on soil properties
remains mainly limited to studies carried out in West Africa and
Brazil with a few species and generally under natural conditions.
Studies have mainly focused on the soil aggregate scale, over-
shadowing the impact of termites on soil functioning at larger
and smaller scales. As a consequence, many questions that have
been addressed for earthworms remain unstudied with termites,
and we are still far from developing approaches to use termites
as naturalresources to improve ecosystem functioning. For exam-
ple, whereas increased earthworm production and diversity are
now perceived as indicators and targets of sustainable agricultural
practicesin temperate regions, termite eradication is still the main
goal in tropical agroecosystems. Only increased knowledge of the
influence of termites on soil structure and water dynamics can
change this trend and explore the potential use of termites for ef-
ficient management of natural resources in tropical ecosystems.
ACKNOWLEDGMENTS
As in any review, the concepts and ideas formulated in this
article result from dialogs with many colleagues and peers,
who are all acknowledged. We are grateful to Zhang Dexin for
her illustrations.
Jouquet et al. Soil Science •Volume 181, Number 3/4, March/April 2016
162 www.soilsci.com © 2016 Wolters Kluwer Health, Inc. All rights reserved.
Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.

REFERENCES
Abe S. S., and T. Wakatsuki. 2010. Possible influence of termites (Macrotermes
bellicosus) on forms and composition of freesesquioxides in tropical soils.
Pedobiologia. 53:301–306.
Ackerman I. L., W. G. Teixeira, S. J. Riha, J. Lehmann, and E. C. M. Fernandes.
2007. The impact of mound-building termites on surface soil properties
in a secondary forest of Central Amazonia. Appl. Soil Ecol. 37:267–276.
Attignon S. E., T. Lachat, B. Sinsin, P. Nagel, and R. Peveling. 2005. Termite
assemblage in a West-African semi-deciduous forest and teak plantations.
Agric. Ecosyst. Environ. 110:318–326.
Balbino L. C., A. Bruand, M. Brossard, and M. de Fatima Guimaraes. 2001.
Comportement de la phase argileuse lors de la dessication dans les Ferralsols
miroagrégés du Brésil: Rôle de la microstructure et de la matière organique.
C. R. Acad. Sci. Paris, Sciences de la Terre et des Planètes. 332:673–680.
Balbino L. C., A. Bruand, M. Brossard, M. Grimaldi, M. Hajnos, and M. F.
Guimarães. 2002. Changes in porosity and microaggregation in clayey
Ferralsols of the Brazilian Cerrado on clearing for pasture. Eur. J. Soil
Sci. 53:219–230.
Bagine R. K. N. 1984. Soil translocation by termites of the genus Odontotermes
(Holmgren) (Isoptera: Macrotermitinae) in an arid areaof Northern Kenya.
Oecologia. 64:263–266.
Bargués Tobella A., H. Reese,A. Almaw, J. Bayala, A. Malmer, H. Laudon, and
U. Ilstedt. 2014. The effect of trees on preferential flowand soil infiltrability
in an agroforestry parkland in semiarid Burkina Faso. Water Resour. Res.
50:3342–3354.
Black H. I. J., and M. J. N. Okwakol. 1997. Agricultural intensification, soilbio-
diversity and agroecosystem function in the tropics: The role of termites.
Appl. Soil Ecol. 6:37–53.
Blouin M., N. Sery, D. Cluzeau, J.- J. Brun, and A. Bédécarrats. 2013. Balkan-
ized research in ecological engineering revealed by a bibliometric analysis
of earthworms and ecosystem services. Environ. Manage. 52:309–320.
BonachelaJ. A., R.M. Pringle, E. Sheffer, T. C. Coverdale, J. A.Guyton, K. K.
Caylor, S. A. Levin, and C. E.Tarnita. 2015. Ecological feedbacks. Termite
mounds can increase the robustness of dryland ecosystems to climatic
change. Science. 347:651–655.
BottinelliN., P. Jouquet, P. Podwojewski, M. Grimaldi, and X. Peng.2015. Why
is the influence of soil macrofauna onsoil structure only considered by soil
ecologists? Soil Till. Res. 146:118–124.
Bourguignon T., J. A. N. ŠobotnÍk, G. Lepoint, J.- M. Martin, O. J. Hardy, A.
Dejean, and Y. Roisin. 2011. Feeding ecology and phylogenetic structure
of a complex neotropical termite assemblage, revealed by nitrogen stable
isotope ratios. Ecol. Entomol. 36:261–269.
Bourguignon T., N. Lo, S. L. Cameron, J. Šobotník, Y. Hayashi, S. Shigenobu,
D. Watanabe, Y. Roisin, T. Miura, and T. A. Evans. 2015. The evolutionary
history of termites as inferred from 66 mitochondrial genomes. Mol. Biol.
Evol. 32:406–421.
Capowiez Y., N. Bottinelli, and P. Jouquet.2014. Quantitative estimates of bur-
row construction and destruction by anecic and endogeic earthworms in
repacked soil cores. Appl. Soil Ecol. 74:46–50.
Choosai C.,J. Mathieu, Y. Hanboonsong,and P. Jouquet.2009. Termite mounds
and dykes are biodiversity refuges in paddy fields in north-eastern
Thailand. Environ. Conserv. 36(1):71–79.
Contour-Ansel D., E. Garnier-Sillam, M. Lachaux, and V. Croci. 2000. High
performance liquid chromatography studies on the polysaccharides in the
walls of the mounds of two species of termite in Senegal, Cubitermes
oculatus and Macrotermes subhyalinus: Their origin and contribution to
structural stability. Biol. Fertil. Soils. 31:508–516.
Dangerfield J. M., T. S. Mc Carthy, and W. N. Ellery. 1998. The mound-building
termites Macrotermes michaelseni as an ecosystem engineer. J. Trop. Ecol.
14:507–520.
Davies R. G., P. Eggleton, D. T. Jones, F. J. Gathorne-Hardy, and L. M.
Hernández. 2003. Evolution of termite functional diversity: Analysis and
synthesis of local ecological and regional influences on local species rich-
ness. J. Biogeogr. 30:847–877.
Dawes T. Z. 2010. Reestablishment of ecological functioning by mulching and
termite invasion in a degraded soil in an Australian savanna. Soil Biol.
Biochem. 42:1825–1834.
Donovan S. E., P. Eggleton, and D. E. Bignell. 2001. Gut content analysis
and a new feeding group classification of termites. Ecol. Entomol. 26:
356–366.
Duponnois R., M. Paugy, J. Thioulouse, D. Masse, and M. Lepage. 2005. Func-
tional diversity of soil microbial community, rock phosphate dissolution
and growth of Acacia seyal as influenced by grass-, litter- and soil-
feeding termite nest structure amendments. Geoderma. 124:349–361.
de Oliveira F. S., A. F.D. C. Varajão, C. A. C.Varajão, C. E. G. R. Schaefer, and
B. Boulange. 2014. The role of biological agents in the microstructural and
mineralogical transformations in aluminium lateritic deposit in Central
Brazil. Geoderma. 226:250–259.
Eggleton P. 2000. Global patterns of termite diversity. In: Termites: Evolution,
Sociality, Symbioses, Ecology. Abe T., D. E. Bignell, and M. Higashi
(eds). Kluwer: Dordrecht, pp. 25–51.
Erens H., B. B. Mujinya, F. Mees, G. Baert, P. Boeckx, F. Malaisse, and E. Van
Ranst. 2015. The origin and implications of variations in soil-related prop-
erties within Macrotermes falciger mounds. Geoderma. 249–250:40–50.
Erpenbach A., M. Bernhardt-Römermann, R. Wittig, A. Thiombiano, and K.
Hahn. 2013. The influence of termite-induced heterogeneity on savanna
vegetation along a climatic gradient in West Africa. J.Trop. Ecol. 29:11–23.
Fall S., A. L. Brauman,and J.-L. Chotte. 2001. Comparative distribution of or-
ganic matter in particle and aggregate size fractions in the mounds of ter-
mites with different feeding habits in Senegal: Cubitermes niokoloensis
and Macrotermes bellicus. Appl. Soil Ecol. 17:131–140.
Francis M. L., F. Ellis, J. J. N. Lambrechts, and R. M. Poch. 2013. A micromor-
phological view through a Namaqualand termitaria (Heuweltjie, a Mima-
like mound). Catena. 100:57–73.
Garnier-Sillam E., and M. Harry. 1995. Distribution of humic compounds in
mounds of some soil-feeding termite species of tropical rainforests: Its in-
fluence on soil structure stability. Insectes Sociaux. 42:167–185.
Holt A. J., and M. Lepage. 2000. Termites and soil properties. In: Termites:
Evolution, Sociality, Symbioses, Ecology. Abe T., D. E. Bignell, and M.
Higashi, (eds). Kluwer Academic Publishers, Netherlands, 18:389–407.
Janeau J. L., and C. Valentin. 1987. Relationships between termite mounds of
Trinervitermes and soil surface: Rearrangement, runoff and erosion. Revue
D'Ecologie Et De Biologie Du Sol. 24:637–647.
Jones C. G., J. H. Lawton, and M. Shachak. 1994. Organisms as ecosystem en-
gineers. Oikos. 69:373–386.
Jones D. T., F. X. Susilo, D. E. Bignell, S. Hardiwinoto, A. N. Gillison, and
P. Eggleton. 2003. Termite assemblage collapse along a land-use inten-
sification gradient in lowland central Sumatra, Indonesia. J. Appl. Ecol.
40:380–391.
Jouquet P., L. Mamou, M. Lepage, and B. Velde. 2002. Effect of termites on
clay minerals in tropical soils: Fungus-growing termites as weathering
agents. Eur. J. Soil Sci. 53:1–7.
Jouquet P., D. Tessier, and M. Lepage. 2004. The soil structural stability of
termite nests:Roleof clays in Macrotermes bellicosus (Isoptera, Macrotermitinae)
mound soils. Eur. J. Soil Biol. 40(1):23–29.
Jouquet P., P. Barré, M. Lepage, and B. Velde. 2005a. Impact of subterranean
fungus-growing termites (Isoptera, Macrotermitinae) on soil properties in
a West African savanna. Biol. Fertil. Soils. 41:365–370.
Jouquet P., V. Tavernier, T. Rugolino, L.Abbadie,and M. Lepage. 2005b. Nests
of subterranean fungus-growing termites (Isoptera, Macrotermitinae) as nu-
trient patches in savannah ecosystems. Afr. J. Ecol. 43:191–196.
Jouquet P., L. Ranjard, M. Lepage, and J. C. Lata. 2005c. Incidence of fungus-
growing termites (Isoptera, Macrotermitinae)on the structure of soil micro-
bial communities. Soil Biol. Biochem. 37:1852–1859.
Soil Science •Volume 181, Number 3/4, March/April 2016 Termites as Neglected Soil Engineers
© 2016 Wolters Kluwer Health, Inc. All rights reserved. www.soilsci.com 163
Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.

Jouquet P., J. Dauber, J. Lagerlof, P. Lavelle, and M.Lepage. 2006. Soil inverte-
brates as ecosystem engineers: Intended and accidental effects on soil and
feedback loops. Appl. Soil Ecol. 32:153–164.
Jouquet P., J. Mathieu, C. Choosaï, and S. Barot. 2007b. Soil engineers as eco-
system heterogeneity drivers. In: Ecology Research Progress. Munoz S. I. (ed).
Nova Science Publishing. New York NY, Chap, 7:187–199.
Jouquet P., S. Traoré, C. Choosai, C. Hartmann, and D. Bignell. 2011. Influence
of termites on ecosystem functioning. Ecosystem services provided by ter-
mites. Eur. J. Soil Biol. 47:215–222.
Jouquet P., J. L. Janeau, A. Pisano, H. Tran Sy, D. Orange, L. T. Nguyet Minh,
and C. Valentin. 2012. Soil engineers influence water runoff, soil detach-
ment and the transfer of nutrients in a tropical steep slope fallow. Appl. Soil
Ecol. 61:161–168.
Jouquet P., E. Blanchart, and Y. Capowiez. 2014. Utilization of earthworms
and termites for the restoration of ecosystem functioning. Appl. Soil Ecol.
73:34–40.
Jouquet P., N. Guilleux, S. Chintakunta, M. Mendez, and R. R. Shanbhag. 2015.
The influence of termites on soil sheeting properties varies depending on
the materials on which they feed. Eur. J. Soil Biol. 69:74–78.
Jungerius P. D., J. A. M. Van Den Ancker, and H.J. Mücher. 1999. The contri-
bution of termites to the microgranular structure of soils on the Uasin Gishu
Plateau, Kenya. Catena. 34:349–363.
Konaté S., X. Le Roux, D. Tessier, and M. Lepage. 1999. Influence of large ter-
mitaria on soil characteristics, soil water regime, and tree leaf shedding pat-
tern in a West African savanna. Plant Soil. 206:47–60.
Korb J., and K. E. Linsenmair. 1998. The effects of temperature on the architec-
ture and distribution of Macrotermes bellicosus (Isoptera, Macrotermitinae)
mounds in different habitats of a West African Guinea savanna. Insectes
Sociaux. 45:51–65.
Korb J., and K. E. Linsenmair. 2000. Thermoregulation of termite mounds:
What role does ambient temperature and metabolism of the colony play?
Insectes Sociaux. 47:357–363.
Krishna K., D. A. Grimaldi, V. Krishna, and M. S. Engel. 2013. Treatise on the
Isoptera of the world. Bull. Am. Mus. Nat. Hist. 377:1–200.
LéonardJ., and J. L. Rajot.2001. Influence of termiteson runoff and infiltration:
Quantification and analysis. Geoderma. 104:17–40.
Léonard J., E. Perrier, and J. L. Rajot. 2004. Biological macropores effect on
runoff and infiltration: A combined experimental and modelling approach.
Agric. Ecosyst. Environ. 104:277–285.
Lévêque T., Y. Capowiez, E. Schreck, S. Mombo, C. Mazzia, Y. Foucault, and
C. Dumat. 2015. Effects of historic metal(loid) pollution on earthworm
communities. Sci. Total Environ. 511:738–746.
Lopez-Hernandez D., M. Brossard, J.- C. Fardeau, and M. Lepage. 2006. Ef-
fect of different termite feeding groups on P sorption and P availability in
African and South American savannas. Biol. Fertil. Soils. 42: 207–214.
Loveridge J. P., and S. R. Moe. 2004. Termitaria as browsing hotspots for Afri-
can megaherbivores in miombo woodland. J. Trop. Ecol. 20:337–343.
Mando A., L. Stroosnijder, and L. Brussaard. 1996. Effets of termites on infil-
tration into crusted soil. Geoderma. 74:107–113.
Mills A. J., A. Milewski, M. V. Fey, A. Groengroeft, and A.Petersen. 2009.Fun-
gus culturing, nutrient mining and geophagy: A geochemical investigation
of Macrotermes and Trinervitermes mounds in southern Africa. J. Zool.
278:24–35.
Moe S. R., R. Mobaek, and A. K. Narmo. 2009. Mound buildingtermites con-
tribute to savannavegetation heterogeneity. Plant Ecol. 202:31–40.
Mora P., E. Miambi, J. J.Jiménez, T.Decaëns, and C. Rouland. 2005. Functional
complement of biogenic structures produced by earthworms, termites and
ants in the neotropical savannas. Soil Biol. Biochem. 37:1043–1048.
Mora P., C. Seuge, J. P. Rossi, and C. Rouland. 2006. Abundance of biogenic
structures of earthworms and termites in a mango orchard. Eur. J. Soil Biol.
42:250–253.
Moura E. G., A. D. F. Aguiar, A. R. Piedade, and G. X. Rousseau. 2015.
Contribution of legume tree residues and macrofauna to the improve-
ment of abiotic soil properties in the eastern Amazon. Appli. Soil Ecol.
86:91–99.
Muvengwi J., M. Mbiba, and T. Nyenda. 2013. Termite mounds maynot be for-
aging hotspots for mega-herbivores in a nutrient-rich matrix. J. Trop. Ecol.
29:551–558.
Muvengwi J., H. G. T. Ndagurwa, T. Nyenda, and I. Mlambo. 2014. Termitaria
as preferred browsing patches for black rhinoceros (Diceros bicornis)in
Chipinge Safari Area, Zimbabwe. J. Trop. Ecol. 30:591–598.
Mujinya B. B., E. Van Ranst, A. Verdoodt, G. Baert, and L. M. Ngongo. 2010.
Termite bioturbation effects on electro-chemical properties of Ferralsols in
the Upper Katanga (DR Congo). Geoderma. 158:233–241.
Mujinya B. B., F. Mees, P. Boeckx, S. Bodé, G. Baert, H. Erens, S. Delefortrie,
A. Verdoodt,M. Ngongo, and E. Van Ranst. 2011. The origin of carbonates
in termite mounds of the Lubumbashi area, D.R. Congo. Geoderma.
165:95–105.
Mujinya B. B., F. Mees, H. Erens, M.Dumon, G. Baert, P. Boeckx, M. Ngongo,
and E. Van Ranst. 2013. Claycomposition and properties in termitemounds
of the Lubumbashi area, D.R. Congo. Geoderma. 192:304–315.
Mujinya B. B., M. Adam, F. Mees, J. Bogaert, I. Vranken, H. Erens, G. Baert,
M. Ngongo, and E. Van Ranst. 2014. Spatial patterns and morphology of
termite (Macrotermes falciger) mounds in the Upper Katanga, D.R. Congo.
Catena. 114:97–106.
Mwabvu T. 2005. The density and distribution of millipedes on termite mounds
in Miombo woodland, Zimbabwe. Afr. J. Ecol. 43:400–402.
Obi J. C., and A. O. Ogunkunle. 2009. Influence of termite infestation on the
spatial variabilityof soil properties in the Guinea savanna region of Nigeria.
Geoderma. 148:357–363.
Pagenkemper S. K., M. Athmann, D. Uteau, T. Kautz, S. Peth, and R.
Horn. 2015. The effect of earthworm activity on soil bioporosity—
Investigated with X-ray computed tomography and endoscopy. Soil Till.
Res. 146:79–88.
Pardeshi M., and B. A. K. Prusty. 2010. Termites as ecosystem engineers and
potentials for soil restoration. Curr. Sci. 99:11.
Potts A., J. Midgley, and C. Harris. 2009. Stable isotope and
14
C study of bio-
genic calcrete in a termite mound, Western Cape, South Africa, and its
palaeoenvironmental significance. Quatern. Res. 722:258–264.
Pringle R.M., D. F. Doak, A.K. Brody, R. Jocque, and T. M. Palmer. 2010. Spa-
tial pattern enhances ecosystem functioning in an African Savanna. PLoS
Biol. 8:e1000377.
ReattoA.,A.Bruand,E.D.Martins,F.Muller,E.M.daSilva,O.A.de
Carvalho, M. Brossard, and G. Richard. 2009. Development and ori-
gin of the microgranular structure in latosols of the Brazilian Central
Plateau: Significance of texture, mineralogy, and biological activity.
Catena. 76:122–134.
Renard D., J. J. Birk, A. Zangerlé, P. Lavelle, B. Glaser, R. Blatrix, and D.
McKey. 2013. Ancient human agricultural practices can promote activities
of contemporary non-human soil ecosystem engineers: A case study in
coastal savannas of French Guiana. Soil Biol. Biochem. 62:46–56.
Roose-Amsaleg C., P. Mora, and M. Harry. 2005. Physical, chemical and phos-
phatase activities characteristics in soil-feeding termite nests and tropical
rainforest soils. Soil Biol. Biochem. 37:1910–1917.
Rückamp D., W. Amelung, L. D. Borma, L.P. Naval,and C. Martius. 2009. Car-
bon and nutrient leaching from termite mounds inhabited by primary and
secondary termites. Appli. Soil Ecol. 43:159–162.
Rückamp D., W. Amelung, N. Theisz, A. G. Bandeira, and C. Martius. 2010.
Phosphorusforms in Brazilian termite nests and soils: Relevance offeeding
guild and ecosystems. Geoderma. 155:269–279.
Rückamp D., C. Martius, L. Bornemann, D. Kurzatkowski, L. P. Naval, and W.
Amelung. 2012. Soil genesis and heterogeneity of phosphorus forms and
carbon below mounds inhabited by primary and secondary termites.
Geoderma. 170:239–250.
Jouquet et al. Soil Science •Volume 181, Number 3/4, March/April 2016
164 www.soilsci.com © 2016 Wolters Kluwer Health, Inc. All rights reserved.
Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.

Sako A., A. J. Mills, and A. N. Roychoudhury. 2009. Rare earth and trace
element geochemistry of termite mounds in central and northeastern
Namibia: Mechanisms for micro-nutrient accumulation. Geoderma.
153:217–230.
Sarcinelli T. S., C. E. G. R. Schaefer, L. D. S. Lynch, H. D. Arato, J. H. M.
Viana, M. R. D. A. Filho, and T. T. Gonçalves. 2009. Chemical, physical
and micromorphological properties of termite mounds and adjacent soils
along a toposequence in Zona da Mata, Minas Gerais State, Brazil. Catena.
76:107–113.
Schaefer C. E. R. 2001. Brazilian latosols and their B horizon microstructure as
long-term biotic constructs. Aust. J. Soil Res. 39:909–926.
Seymour C.L., A. V. Milewski, A. J. Mills, G.S. Joseph, G. S. Cumming,D. H.
M. Cumming, and Z. Mahlangu. 2014. Do the large termite mounds of
Macrotermes concentrate micronutrients in addition to macronutrients in
nutrient-poor African savannas? Soil Biol. Biochem. 68:95–105.
Sileshi G. W., M. A. Arshad, S. Konaté, and P. O. Y. Nkunika. 2010. Termite-
induced heterogeneity in African savanna vegetation: Mechanisms and pat-
terns. J. Veg. Sci. 21:923–937.
TraoréS., M. Tigabu, S. J. Ouedraogo, J. I. Boussim, S. Guinko, and M. Lepage.
2008. Macrotermes mounds as sites for tree regeneration in a Sudanian
woodland (Burkina Faso). Plant Ecol. 198:285–295.
TraoréS.,S.J.Ouédraogo,P.Jouquet,N.B.H.,B.J.I.,G.S.,andL.M.2015.
Long-termeffects of Macrotermes termites, herbivores and annual earlyf ire
on woody undergrowth community in Sudanian woodland, Burkina Faso.
Flora. 211:40–50.
Turner J. S. 2004. Extended phenotypes and extended organisms. Biol. Philos.
V19:327–352.
Van der Plas F., R. Howison, J. Reinders, W. Fokkema, and H. Olff. 2013. Func-
tional traits of trees on and off termite mounds: Understanding the origin of
biotically driven heterogeneity in savannas. J. Veg. Sci. 24:227–238.
Villenave C., D. Djigal, A. Brauman, and C. Rouland-Lefevre. 2009. Nema-
todes, indicators of the origin of the soil used by termites to construct
biostructures. Pedobiol. 52:301–307.
Wood T. G., and W. A. Sand. 1978. The role of termites in ecosystems. In:Pro-
duction Ecology ofAnts and Termites. Brian M. V. (ed). Cambridge Univer-
sity Press, Cambridge, UK, pp. 245–292.
Soil Science •Volume 181, Number 3/4, March/April 2016 Termites as Neglected Soil Engineers
© 2016 Wolters Kluwer Health, Inc. All rights reserved. www.soilsci.com 165
Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.