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Resource Opportunities From the Nest of Dying Subterranean Termite (Isoptera: Rhinotermitidae) Colonies: A Laboratory Case of Ecological Succession

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Subterranean termites such as Coptotermes formosanus Shiraki inhabit underground nests consisting of a complex network of galleries resulting in a highly modified environment relative to the surrounding soils. A healthy colony can maintain homeostatic conditions within the nest, limiting opportunities for pathogens, parasites, and predators to exploit the termite colony as a resource. However, a stressed or senescent colony can display a lack of nest maintenance, leading to the colonization of the nest as an opportunistic niche by other organisms. In this study, we described the nest colonization by microbes and arthropods during the collapse of three dying C. formosanus laboratory colonies. The carton nest and the tunnel lining that are mostly made out of termite fecal material were invaded by a variety of fungi, and Acari and Collembolan populations quickly increased during the senescence phase of the termite colony, presumably scavenging on the fungal material. Finally, the carton colonized by fungal mycelia hosted numerous larvae of a sciarid fly, Bradysia sp. (Diptera). This fungus gnat used the decomposing carton material as a breeding site, and numerous adults of this fly were found hovering above the dying termite colony. Bradysia larvae also showed infestation by parasitic nematodes, suggesting the presence of multiple trophic levels in the resource utilization of the nest of a declining termite colony. We concluded that a dying subterranean colony represents a resource opportunity for scavenging organisms and that the nest structure represents an opening niche that initiates an ecological succession.
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Resource Opportunities From the Nest of Dying Subterranean Termite
(Isoptera: Rhinotermitidae) Colonies: A Laboratory Case of Ecological
Ann. Entomol. Soc. Am. 106(6): 771Ð778 (2013); DOI:
ABSTRACT Subterranean termites such as Coptotermes formosanus Shiraki inhabit underground
nests consisting of a complex network of galleries resulting in a highly modiÞed environment relative
to the surrounding soils. A healthy colony can maintain homeostatic conditions within the nest,
limiting opportunities for pathogens, parasites, and predators to exploit the termite colony as a
resource. However, a stressed or senescent colony can display a lack of nest maintenance, leading to
the colonization of the nest as an opportunistic niche by other organisms. In this study, we described
the nest colonization by microbes and arthropods during the collapse of three dying C. formosanus
laboratory colonies. The carton nest and the tunnel lining that are mostly made out of termite fecal
material were invaded by a variety of fungi, and Acari and Collembolan populations quickly increased
during the senescence phase of the termite colony, presumably scavenging on the fungal material.
Finally, the carton colonized by fungal mycelia hosted numerous larvae of a sciarid ßy, Bradysia sp.
(Diptera). This fungus gnat used the decomposing carton material as a breeding site, and numerous
adults of this ßy were found hovering above the dying termite colony. Bradysia larvae also showed
infestation by parasitic nematodes, suggesting the presence of multiple trophic levels in the resource
utilization of the nest of a declining termite colony. We concluded that a dying subterranean colony
represents a resource opportunity for scavenging organisms and that the nest structure represents an
opening niche that initiates an ecological succession.
KEY WORDS termite, microbe, senescent colony, opportunist, trophic level
Social insects with a subterranean lifestyle such as the
Formosan subterranean termite Coptotermes formosa-
nus Shiraki excavate soil to create an underground nest
where the colony can be established (Messenger et al.
2005, Li and Su 2008). As the colony matures, it can
build up to a million individuals (Su and Scheffrahn
1988) and the tunnel system expands into a complex
network of galleries, which connect foraging sites to
the different chambers of the nests over long distances
(King and Spink 1969). Over time, the tunnel walls are
coated with a fecal lining and the chambers are Þlled
with carton material, a sponge-like structure mainly
composed of fecal material and chewed wood parti-
cles (King and Spink 1969, Wood 1988, Bardunias
2013). The maintenance of the gallery system in many
termite species results in a highly modiÞed microen-
vironment when compared with the surrounding soils
(Brauman 2000, Holt and Lepage 2000, Jouquet et al.
2005, Bignell 2006, Fall et al. 2007). Healthy colonies
can maintain the proper humidity, temperature, and
associated microbial communities to provide a ho-
meostatic environment (Wood 1988, Hughes et al.
2008, Chouvenc et al. 2011b). Although the subterra-
nean lifestyle may protect against ßuctuations in the
above-ground environment and reduce predation, the
colony can be under pathogenic and parasitic pressure
from the surrounding soils (Blackwell and Rossi 1986,
SchmidÐHempel 1998). As a result, subterranean so-
cial insects have evolved disease resistance mecha-
nisms (Chouvenc and Su 2010, Rosengaus et al. 2011)
that reduce the survival of pathogens within the nest
and prevent the risk of epizootics. The active main-
tenance of the nest is one of these mechanisms
(Rosengaus et al. 1998; Cremer et al. 2007; Chouvenc
et al. 2008, 2009; Hamilton et al. 2011; Chouvenc and
Su 2012). We hypothesize that stressed or senescent
colonies can display a lack of nest maintenance and
that typically excluded organisms can then colonize
the nest, using it as an opportunistic niche, primarily
as the termite colony enters into a declining phase.
Department of Entomology and Nematology, Ft. Lauderdale Re-
search and Education Center, University of Florida, Institute of Food
and Agricultural Sciences, 3205 College Ave., Ft. Lauderdale, FL
Corresponding author, e-mail: tomchouv@uß.edu.
Department of Plant Pathology, Ft. Lauderdale Research and
Education Center, University of Florida, Institute of Food and Agri-
cultural Sciences, 3205 College Ave., Ft. Lauderdale, FL 33314.
0013-8746/13/0771Ð0778$04.00/0 2013 Entomological Society of America
However, observing the decline of a subterranean nest
in Þeld conditions is difÞcult because of their cryptic
lifestyle (Grace et al. 1995); therefore, we performed
our observation on laboratory-kept colonies.
Until recently, the collapse of laboratory groups of
termites was often attributed to the rapid growth of
harmful microorganisms due in part to the artiÞcial
environment (Toumanoff 1966, Chouvenc et al.
2011a). However, it was recently shown that such
microorganism growth was mainly the result of the
already declining termite group and not the cause of
the decline (Chouvenc et al. 2012). In our laboratory,
we have maintained colonies of C. formosanus in large
containers for experimental purposes. Such colonies
are able to build and maintain their nests and expand
their foraging galleries. Some of the colonies have
been obtained from founding alates that were paired
in the laboratory. However, it can take 4Ð5 yr for the
colony to reach a large enough size for us to perform
some bioassays. Alternatively, some colonies were ob-
tained from a large sampling of mature-Þeld colonies.
With the latter method, we were able to accumulate
hundreds of thousands of individuals from single col-
onies within a short period (1 yr) and maintain them
in large containers in the laboratory for multiple years.
Some of these Þeld-collected colonies have produced
replacement reproductives, with the presence of Þrst
instar workers, even after 4 yr in the laboratory. How-
ever, some of these Þeld-collected groups of termites
have apparently failed to produce replacement repro-
ductives after 3 yr in the laboratory, at which time only
senescent individuals could be found. Such relatively
large and low-vigor individuals matched the descrip-
tion by Grace et al. (1995) of a declining colony. The
laboratory colonies that failed to produce secondary
reproductives ultimately collapsed. Because these col-
onies were collected from the Þeld, many microor-
ganisms and associated arthropods were also collected
during the sampling, but apparently remained in low
prevalence (or below level of detection), and did not
hindered the health of the laboratory-kept termite
colonies over the years.
During the last 3 mo of activity of these senescent
laboratory colonies, we observed changes in the prev-
alence of organisms associated with the nest material.
The objective of this study was to describe the use of
the termite nest material as a resource by typically
excluded organisms, as the laboratory termite colonies
declined, and to demonstrate that such organisms re-
main either dormant or in low prevalence until the
niche opens to them, therefore initiating an ecological
Materials and Methods
Termite Collection and Maintenance. Laboratory
colonies of C. formosanus were established by
monthly or bimonthly trapping of individuals from
Þve Þeld colonies (Broward County, FL) between
2008 and 2009, using the Þeld traps described by Su
and Scheffrahn (1986). Termites were processed us-
ing the method described by Tamashiro et al. (1973).
The laboratory-kept termite groups (220,000 to
1,000,000 individuals per colony of origin) were con-
tained in individual Plexiglas cubes (1 by 1 by 1 m; Fig.
1) with openings for aeration and access to the nests,
and maintained at 28C and 75% relative humidity
(RH). This setup was described in detail by Su (2013).
Laboratory colonies were fed with spruce blocks (Pi-
cea sp.). Each colony had access to a ßoral foam block
that was regularly saturated with water, so that ter-
mites could regulate the water content inside the nest.
During 2012, three of the Þve colonies showed signs of
senescence with accumulation of large individuals,
usually reßecting a relative old age (Grace et al. 1995),
and an overall decline in colony health, while the two
other colonies contained active reproductives and ap-
parently healthy individuals. The two healthy colonies
were used as controls and were compared with the
three colonies in decline regarding the prevalence of
organisms associated with the nest material.
Fig. 1. Laboratory containers (1 by 1 by 1 m) to maintain
large termite groups (up to 1 million individuals) over time
(3 yr). (A) A container shortly after introducing groups of
Þeld-harvested termites, and (B) established colony after 3
yr maintained in the laboratory. (Online Þgure in color.)
Microbial and Arthropod Observation. Because the
diversity and prevalence of bacteria in nest materials
was too complex to determine with just a culture-
based approach (Chouvenc et al. 2011b), this study
was mostly restricted to fungi and arthropods. How-
ever, because the occurrence of the bacterium Serra-
tia marcescens Bizio is common in dying groups of
termites (Toumanoff and Toumanoff 1959, Lund
1965), it was conÞrmed in this study through the
examination of dead termites, as the cadavers turned
red. It was also isolated from nest material samples. It
was identiÞed by its characteristic morphology when
grown on one Þfth strength potato dextrose agar
(PDA). Therefore, our study focused on the presence
and the prevalence of fungi in the nest of healthy
colonies and those in decline. For healthy colonies,
the diversity and the prevalence of fungi was deter-
mined by isolating single fungal colony forming units
(CFUs) from the termite nests and from termite ca-
davers. Three 0.5-g nest material samples were sub-
mitted to a serial dilution and plated on one Þfth
strength PDA supplemented with Streptomycin (100
mg/liter) to prevent bacterial growth. For dying col-
onies, the mass of mycelium was subsampled on one
Þfth strength PDA to obtain a range of isolates. Fungal
isolates with unique morphological characteristics
were identiÞed by sequencing their internal tran-
scribed spacer (ITS) region using primers ITS1and
ITS4, and sequences were submitted to a BLAST se-
quence analysis for identiÞcation in GenBank. Fungi
repeatedly observed were then identiÞed by morphol-
ogy matching or by ITS sequencing in absence of clear
morphological traits.
From each nest of origin, three 10-g samples of nest
material were collected, and all arthropods were
counted and identiÞed. The primary method of iden-
tiÞcation was through the use of morphological traits,
but if necessary, the cytochrome oxidase II (COII)
gene of specimens was sequenced using primers A-
tLeu B-tLys. The prevalence of arthropods between
healthy and declining colonies was compared with a
Regardless of each colonies state of health, numer-
ous fungi were associated with the nest material, in-
cluding Aspergillus, Penicillium, Trichoderma, and
Lecanicillium. However, the density of these fungi in
healthy nest material (Fig. 2A) was 10
CFUs per
gram, presumably as spores, while the life stages of
such fungi in the dying termite colonies were mainly
mycelia with sporulating areas (Fig. 2B), or sclerotia
(Fig. 2C) within the nest material. Because the nest
material of dying colonies were mostly invaded by
these fungi as mycelia, a quantitative comparison of
fungal CFUs from the nest material of healthy colonies
was not relevant. However, by washing the nest ma-
terial to separate the mycelia from the carton particle,
it was possible to measure the fungal biomass in the
samples. Fungi represented 4% (dry weight, n3) of
the mass of nest material from dying colonies, while no
mycelia could be extracted from nest material of
healthy colonies (0%). A qualitative comparison of
the presence of fungi was provided in Table 1. S.
marcescens was found in low concentrations in the nest
material of both types of termite colonies (10
per gram). However, in dying colonies in which we
observed a rapid accumulation of cadavers, some
showed signs of S. marcescens colonization with the
typical red pigmentation (10
CFU per dead ter-
mite when submitted to serial dilution and plated on
one Þfth strength PDA). Other saprophytic microor-
ganisms were observed growing on cadavers and con-
sisted mostly of Aspergillus.
Fig. 2. Termite carton nests. (A) Healthy carton material
from an active termite colony, (B) carton material invaded
by mycelia of various fungal species, and (C) carton nest
invaded by Aspergillus flavus (here, sclerotia are forming
inside the gallery system). (Online Þgure in color.)
As the fungal mycelia invaded the carton nest of
dying colonies, the prevalence of mycophagous coll-
embolans (Entomobryidae: Entomobryinae; Fig. 3A)
increased (P0.004; t-test) from an average of four
individuals per gram of nest material (healthy colo-
nies) to 45 per gram of nest material (dying colonies).
Similarly, Acotyledon sp. and Histiostoma sp. mites
(Acaridae; Fig. 3B) were present in relatively low
densities in the nest material of healthy colonies (av-
erage of eight individuals, both species combined, per
gram of nest material) while dying colonies had higher
(P0.001; t-test) numbers of mites (92 per gram of
nest material; Fig. 4). Adult mites were observed feed-
ing on decomposing termite cadavers and fungal ma-
terial. However, hypopi (nonfeeding phoretic deu-
teronymph) were mostly found on the surface of the
head capsule of senescent individuals from declining
In the containers with a declining termite colony,
we observed the presence of small ßies hovering
above the nest material. These were identiÞed as Bra-
dysia sp. (Diptera: Sciaridae) (Fig. 5A), which are
fungus gnats commonly associated with decaying or-
ganic material containing fungal growth. While pro-
cessing the carton material invaded with various fungi
Table 1. Presence of fungi in the nest material of five long-term
field-collected laboratory colonies of C. formosanus
colony A
colony B
colony C
colony D
colony E
Acremonium sp. X X X
Bionectria sp. X X
Fusarium solani XX X
Microascus sp. X X
Penicillium sp. X X X X X
Talaromyces sp. X X
In healthy termite colonies, isolates where obtained from serial
dilution of nest material on one Þfth strength PDA.
In dying colonies, isolates where obtained by sampling fungal struc-
tures growing from the nest material, subcultured on one Þfth
strength PDA.
Fig. 3. Arthropods commonly associated with declining
termite colonies. (A) Entomobryid collembolan, and (B)
mites, here Acotyledon sp. present as hypopi on termite head
capsules. Scale bar 0.5 mm. (Online Þgure in color.)
Fig. 4. Presence of Collembolan and Acari in healthy
(n2) and dying termite colonies (n3). Average SD
number per gram of nest material from three samples per
colonies of origin. For both types of arthropods, there was a
signiÞcant increase of number of individuals in the dying
termite colonies (P0.05; t-test).
Fig. 5. Bradysia sp. associated with a declining colony of
C. formosanus. (A) Adult male and female, and (B) larva.
Scale bar 1 mm. (Online Þgure in color.)
mycelia and sclerotia, we found Diptera larvae (Fig.
5B) apparently feeding on the decaying carton mate-
rial (4.3 1.2 larvae per gram of nest material),
whereas no larvae were found in the nest material of
healthy colonies. The COII gene proÞle of the adult
ßies and the Diptera larvae matched, indicating that
they were the same species.
Finally, we found a nematode species associated
with Bradysia larvae. Each larvae had three or four
females of the parasitic nematode Tetradonema plicans
Cobb (Nematoda: Tetranematidae) (Fig. 6A), and
microscopic observations also showed the presence of
males from this nematode species in the ßy larvae (Fig.
In comparison with surrounding soil, subterranean
termite nests represent a unique type of resource
because of the accumulation of organic material orig-
inating from the fecal deposition of the termites
throughout the nest (Bignell 2006, Jouquet et al. 2011,
Chouvenc et al. 2011b). As healthy colonies can main-
tain homeostatic conditions within the nest, the carton
material had low densities of opportunistic arthropods
and fungi. In contrast, as the nest maintenance de-
clined in dying colonies, the carton nest was invaded
by fungal mycelia and sclerotia, and several opportu-
nistic arthropods increased their populations, appar-
ently by consuming the decomposing nest material
and termite cadavers.
Fungi are commonly found in termite nest material,
but as long as the colony is healthy and the nest
maintained by the termites, these fungi remain at
relatively low densities, presumably in a nonpropaga-
tive life stage (Zoberi and Grace 1990, Milner et al.
1998, Rosengaus et al. 1998, Rojas et al. 2001, Jayasimha
and Henderson 2007, Chouvenc et al. 2011b). The
similar fungal diversity among the nest material of our
laboratory termite colony may be because of two fac-
tors, as 1) all termite colonies were collected within a
20-km radius, and such fungi may be common in the
local soils; and 2) fungal isolates may have been able
to disperse from one laboratory colony to another
during their maintenance over time within the same
laboratory. Irrespective of their origin, such microor-
ganisms are common in soils, and as the termites forage
underground, fungal spores can opportunistically be
carried back inside the nest and incorporated within
the nest material. In a similar fashion, some macroter-
mitine termites may recruit their Termitomyces sym-
biont from surrounding soils (Aanen et al. 2002). In
addition, many of the fungi associated with the termite
nests in our study have been found to be associated
with the nest material of ant colonies (Rodrigues et al.
2011, Reber and Chapuisat 2012), suggesting that both
ants and termites living in a subterranean habitat can
passively incorporate common fungal isolates from the
surrounding soils into their nest material. Because the
nest material of some Rhinotermitidae possesses fun-
gistatic properties (Chouvenc et al. 2009, Hamilton et
al. 2011), fungi may remain in spore form until the
termite colony declines. Presumably, the lack of nest
maintenance results in a chemical shift allowing the
dormant spores to germinate and the resulting mycelia
to use the nest resource for nutrition. We suggest that
the transition of the niche from a fungal-suppressed
environment to a fungal-dominated environment al-
lows for the initiation of a community shift, which in
the long-term, can result in an ecological succession.
In our dying laboratory colonies, collembolans and
mites were the arthropods that directly beneÞted from
the niche opening. Most of the entomobryid collem-
bolans were found associated with fungal mycelia, and
mites were scavenging on termite cadavers invaded by
fungi and bacteria. We took into account that our
observations were limited to laboratory termite colo-
nies where the system was relatively simple with only
a handful of arthropod species. However, by having a
controlled environment, we were able to monitor the
shift in prevalence of these species, which would have
been difÞcult, if not impossible, to do with Þeld col-
onies. Incidentally, it can be expected that in dying
Þeld colonies, many organisms from the surrounding
environment can use this opening niche. The termite
nest represents a nutritional resource opportunity for
microorganisms and various arthropods and also pro-
vides a potential shelter for others. In dead colonies of
Nasutitermes and Cubitermes (Termitidae), both of
which possess a central nest, it was demonstrated that
Fig. 6. The nematode T. plicans associated with larvae of
Bradysia. (A) Female T. plicans in the process of leaving from
a ßy larvae, and (B) male T. plicans. (Online Þgure in color.)
ants primarily occupy vacant termite nests, along with
a wide range of other arthropods (Martius et al. 1994,
Dejean et al. 1997), and occasionally vertebrates
(Brosset and Darchen 1967, GrifÞths and Christian
1996, Brightsmith 2000). Furthermore, neighboring
termite colonies or new incipient colonies of the same
termite species may reuse the existing nest structure
for their own advantage (Dejean and Ruelle 1995,
Messenger et al. 2005). Field observations from pre-
vious studies and laboratory observations from the
current study show that the nest of a dead termite
colony remains a valuable resource for any opportu-
nistic organisms that can reuse such a resource and
Many ßy species (Phoridae) are known to parasitize
termite nests (Disney and Kistner 1990, Disney and
Dupont 2009), but to our knowledge, this is the Þrst
report of a sciarid ßy associated with a termite nest.
This association is not likely to be parasitic, as the
presence of the ßy larvae in the nest was secondary to
the invasion of the carton material by fungal mycelia.
The presence of the adult ßies hovering over a termite
colony was invariably a signal that the colony was
either in decline, or already dead. From this anecdotal
observation, it was coined the ßy of death(R. Pepin,
personal communication). The presence of the ento-
moparasitic nematode T. plicans in the larvae of the
sciarid ßy (Cobb 1919, Hudson 1974, Peloquin and
Platzer 1990) implies that multiple trophic levels are
involved during the invasion of the nest material by
detritivorous arthropods, directly increasing the over-
all biodiversity. In the current study, we did not an-
alyze the nest material or the termites for nematodes
(parasitic or commensal); however, previous studies
have shown that nematodes are commonly associated
with low-vigor termites (Wang et al. 2002, Carta and
Osbrink 2005) as well as with apparently healthy ter-
mites (Kanzaki et al. 2012). Therefore, the decline of
a termite colony may offer new resource possibilities
for nematodes and probably other microorganisms not
discussed in this study.
The presence of mites associated with declining
colonies has been previously documented (Phillipsen
and Coppel 1977b, Eraky 1999, Wang et al. 2002), and
it has been suggested that such mites were the cause
of some laboratory colony collapses (Lund 1962, Phil-
lipsen and Coppel 1977a). However, experiments that
tested mites as parasites of termites did not take the
termite biology into account, as healthy groups of
termites are able to maintain their nest to prevent the
accumulation of such mites, as observed in our current
study. Mites are usually present in high density only in
dying colonies (Wang et al. 2002, Myles 2002), as
conÞrmed by our observations. Therefore, testing
mites as termite parasites by using large densities of
mites on a small termite group that cannot maintain its
environment (Petri dish bioassays do not permit ter-
mites to quickly establish a nest structure) represents
conditions that would only occur in a termite colony
already in a declining phase (Chouvenc et al. 2011c,
2012; Chouvenc and Su 2012). Mites can be an addi-
tional burden to a colony in decline, especially when
hypopi larvae build up on the surface of the cuticle of
termite individuals. In addition, we often observed
that mite and collembolan exocuticles were covered
by spores of various fungi (Aspergillus, Trichoderma,
and Penicillium), which directly helped the fungi in
dispersing through the nest material, as previously
suggested by Myles (2002). This implies that the
interaction between detritivorous arthropods and
fungi may be more complex than a simple trophic
relationship, as the arthropods may indirectly pro-
vide a beneÞt to such fungi by dispersing them
throughout the nest and giving them easier access to
previously unavailable resources (Malloch and
Blackwell 1990).
To conclude, termites can be considered ecosys-
tem engineers(Jones et al. 1994) because of their
capacity to participate in resource ßow by helping
recycle a signiÞcant amount of carbon sequestered in
plant materials (Jouquet et al. 2006). Termites trans-
form (predigest, churn, and redistribute) such inac-
cessible resources into resources that can be available
for other organisms (DangerÞeld et al. 1998). Our
study showed that, after the death of a termite colony,
fungi previously inhibited by the active colony can use
this resource, and mites and collembolans can in turn
feed on this fungal material. These arthropods may
also provide positive feedback to such fungi by dis-
persing their spores throughout the nest. Indepen-
dently, the sciarid ßy larvae that also fed on fungal
material in this study arrived as progeny of attracted
adult fungus gnats. These gnat larvae were subse-
quently parasitized by a nematode, which demon-
strates the existence of multiple trophic levels within
the collapsed termite colony. These Þndings suggest
that, while a live healthy termite colony can physically
and chemically alter local soils by enriching these soils
with novel resources (Bignell 2006, Jouquet et al.
2011), a dead termite colony leaves a resource foot-
print in the form of nutrients and shelter. The obser-
vations made from our laboratory colonies may have
shown limited diversity colonization because of a
mostly closed system; however, the death of the Þeld
colony can result into a rapid change in the prevalence
of organisms originating from the surrounding soil,
into the carton nest. Therefore, the carton nest of
termite Þeld colonies may be reused by any opportu-
nistic organisms, resulting ultimately in an ecological
succession at a local scale and in a potential increase
of biodiversity.
We thank Stephanie Osorio, Elizabeth Des Jardin, Ron
Pepin, and Aaron Mullins for their technical help (University
of Florida), and Lucas Carnohan and two anonymous re-
viewers for their constructive comments. This study was
supported in part by a research opportunity SEED fund
from the University of Florida under the grant agreement
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Received 26 June 2013; accepted 29 August 2013.
... The mycobiomes of captive and free-living subterranean termites and their nest compartments have therefore been investigated to identify the dominant taxa. [1][2][3][4][5] The genera Debaryomyces, Candida, Exophiala, GS23 (Umbelopsidomycetes), Scytalidium, Talaromyces, Trichoderma and Xylaria were found to be more abundant in the nest material than the surrounding environment, and have the potential for both mutualistic and parasitic interactions. [1][2][3] Mutualistic yeasts are present in the termite gut, where they facilitate the digestion of wood and support detoxification. ...
... [1][2][3][4][5] The genera Debaryomyces, Candida, Exophiala, GS23 (Umbelopsidomycetes), Scytalidium, Talaromyces, Trichoderma and Xylaria were found to be more abundant in the nest material than the surrounding environment, and have the potential for both mutualistic and parasitic interactions. [1][2][3] Mutualistic yeasts are present in the termite gut, where they facilitate the digestion of wood and support detoxification. [6] Similarly, fungi present in termite nests, such as Trichoderma spp., may be mutualistic under most circumstances, but they may also be opportunists that can later become antagonistic, as shown for Xylariales spp. ...
... are abundant in habitats linked to termites that feed on decayed wood, but it is unclear whether they are beneficial or detrimental. [2,3,8,31] They are ubiquitous saprophytes and endophytes that produce numerous secondary metabolites, [32] including bioactive peptaibols, alkaloids, polyketides and nonribosomal peptides (NRPs) [16,17] with antibacterial, cytotoxic, antifungal, antiviral and anti-inflammatory properties. [10,33] Trichoderma virens and others have been evaluated as biocontrol agents against subterranean termites. ...
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Termites live in a dynamic environment where colony health is strongly influenced by surrounding microbes. However, little is known about the mycobiomes of lower termites and their nests, and how these change in response to disease. Here we compared the individual and nest mycobiomes of a healthy subterranean termite colony ( Coptotermes testaceus ) to one infected and ultimately eradicated by a fungal pathogen. We identified Trichoderma species in the materials of both nests, but they were also abundant in the infected termites. Methanolic extracts of Trichoderma sp. FHG000531, isolated from the infected nest, were screened for secondary metabolites by UHPLC‐HR MS/MS‐guided molecular networking. We identified many bioactive compounds with potential roles in the eradication of the infected colony, as well as a cluster of six unknown peptides. The novel peptide FE011 was isolated and characterized by NMR spectroscopy. The function of this novel peptide family as well as the role of Trichoderma species in dying termite colonies therefore requires further investigation.
... Although many of these saprophytes are not insect pathogens, colonies must still protect themselves from microbes that can infest and consume the nest. In collapsed laboratory colonies of the Formosan subterranean termite, Coptotermes formosanus, the colony is no longer able to inhibit the growth of microbes in the nest, and, as a result, the remaining resources of the nest are consumed by a succession of saprophytic organisms [12]. ...
... Interestingly, only five pathogenic fungi were found on the cuticle, whereas nine were found in the gallery and 12 in the soil (Fig. 5c). The fungal genus Trichoderma was found in all three substrates [12]. The unclassified Bacillus sp. and Trichoderma hamatum had high relative abundance in the soil that decreased in gallery and cuticle samples. ...
... Taxa that have only been identified to genus level could not be classified further using the SILVA or UNITE databases and Trichoderma. The fungal genus Trichoderma does not directly infect termites, but it can colonize their nests [12]. This reduction could be due to the antimicrobial effects of termite feces and salivary gland secretions that are incorporated into the galleries, or the presence of Streptomyces in the galleries mentioned above [19,20,23]. ...
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Termites are intimately tied to the microbial world, as they utilize their gut microbiome for the conversion of plant cellulose into necessary nutrients. Subterranean termites must also protect themselves from the vast diversity of harmful microbes found in soil. However, not all soil microbes are harmful, such as Streptomyces and methanotrophic bacteria that some species of termites harbor in complex nest structures made of fecal material. The eastern subterranean termite, Reticulitermes flavipes, has a simple nest structure consisting of fecal lined galleries. We tested the hypothesis that R. flavipes maintains a select microbial community in its nests to limit the penetration of harmful soilborne pathogens and favor the growth of beneficial microbes. Using Illumina sequencing, we characterized the bacterial and fungal communities in the surrounding soil, in the nest galleries, and on the cuticle of workers. We found that the galleries provide a more beneficial microbial community than the surrounding soil. Bacterial and fungal diversity was highest in the soil, lower in the galleries, and least on the cuticle. Bacterial communities clustered together according to the substrate from which they were sampled, but this clustering was less clear in fungal communities. Most of the identified bacterial and fungal taxa were unique to one substrate, but the soil and gallery communities had very similar phylum-level taxonomic profiles. Notably, the galleries of R. flavipes also harbored both the potentially beneficial Streptomyces and the methanotrophic Methylacidiphilales, indicating that these microbial associations in fecal material pre-date the emergence of complex fecal nest structures. Surprisingly, several pathogenic groups were relatively abundant in the galleries and on the cuticle, suggesting that pathogens may accumulate within termite nests over time while putatively remaining at enzootic level during the lifetime of the colony.
... Chouvenc et al. 2011). The core of the termite nest is filled with 'carton material', a sponge-like structure composed of nutritious chewed wood particles and fecal material that promotes the growth of mutualistic and opportunistic microbes, including parasites and pathogens (Chouvenc et al. 2013a). Preventing pathogenic fungi or other microbes from proliferating in the termite colony and on the fecal nest structure requires multiple mechanisms, including mutual-and self-grooming behavior by the termites to avoid bringing spores or fungal mycelia into the nest (Yanagawa et al. 2008;Chouvenc and Su 2010;Chouvenc and Su 2012). ...
... The current study led to the identification of eleven known biologically active bacteria-derived metabolites with antimicrobial activity. Interestingly, one Streptomyces metabolite induces the production of cryptenol (1), t22-azaphilone (2), and homodimericin A (3) in Trichoderma harzianum (Fig. 1), an ecologically relevant soil fungus that is known to take over the carton material of collapsed termite nests (Chouvenc et al. 2013a). The induction of these metabolites led to insights into the chemical interactions that are possibly occurring among microbes within the termite nest. ...
... 4231 and T. harzianum WC13 (Genbank: KX694115) were both isolated from C. formosanus colonies, though were not found in the same colonies. T. harzianum WC13 was isolated from a dying C. formosanus colony and as the microbial community from the carton nest also collapsed, T. harzianum became the dominant saprophyte in a case of ecological succession (Chouvenc et al. 2013a). The actinobacterial strains were grown on 1/5 potato dextrose agar (DB Difco PDA) or 1/5 potato dextrose broth (DB Difco PDB) for 14 days. ...
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Bacteria and fungi in shared environments compete with one another for common substrates, and this competition typically involves microbially-produced small molecules. An investigation of one shared environmental niche, the carton material of the Formosan subterranean termite Coptotermes formosanus, identified the participants on one of these molecular exchanges. Molecular characterization of several termite-associated actinobacteria strains identified eleven known antimicrobial metabolites that may aid in protecting the C. formosanus colony from pathogenic fungal infections. One particular actinobacterial-derived small molecule, bafilomycin C1, elicited a strong chemical response from Trichoderma harzianum, a common soil saprophyte. Upon purification and structure elucidation, three major fungal metabolites were identified, t22-azaphilone, cryptenol, and homodimericin A. Both t22-azaphilone and homodimericin A are strongly upregulated, 123- and 38-fold, respectively, when exposed to bafilomycin C1, suggesting each play a role in defending T. harzianum from the toxic effect of bafilomycin C1. Electronic supplementary material The online version of this article (10.1007/s10886-017-0900-6) contains supplementary material, which is available to authorized users.
... The required passage of the wood through the termite gut may, therefore, reflect the ancestral mechanism of how nutritional external symbionts initially took advantage of the feacal nest. An added argument is that carton nests in dying Coptotermes colonies or abandoned sections of the nest, can be invaded by a series of saprophytic microorganisms, including Basidiomycetes soil fungi, such as Leucocoprinus [209] (Fig. 6). Such observations demonstrate that opportunistic microorganisms may be suppressed from the carton by Coptotermes or its allied microorganisms, but it remains a niche for potential decomposers. ...
... The opportunistic saprophytes are indeed inhibited by termites and their associated microbes [139,141,209], however, the ancestor of Termitidae may have let certain saprophytes use parts of the fecal nest or abandoned foraging sites. Once termites started reusing such processed faecal nests, it would have allowed access to novel metabolites and enhanced wood-digestion processes. ...
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Termites are a clade of eusocial wood-feeding roaches with > 3000 described species. Eusociality emerged ~ 150 million years ago in the ancestor of modern termites, which, since then, have acquired and sometimes lost a series of adaptive traits defining of their evolution. Termites primarily feed on wood, and digest cellulose in association with their obligatory nutritional mutualistic gut microbes. Recent advances in our understanding of termite phylogenetic relationships have served to provide a tentative timeline for the emergence of innovative traits and their consequences on the ecological success of termites. While all “lower” termites rely on cellulolytic protists to digest wood, “higher” termites (Termitidae), which comprise ~ 70% of termite species, do not rely on protists for digestion. The loss of protists in Termitidae was a critical evolutionary step that fostered the emergence of novel traits, resulting in a diversification of morphology, diets, and niches to an extent unattained by “lower” termites. However, the mechanisms that led to the initial loss of protists and the succession of events that took place in the termite gut remain speculative. In this review, we provide an overview of the key innovative traits acquired by termites during their evolution, which ultimately set the stage for the emergence of “higher” termites. We then discuss two hypotheses concerning the loss of protists in Termitidae, either through an externalization of the digestion or a dietary transition. Finally, we argue that many aspects of termite evolution remain speculative, as most termite biological diversity and evolutionary trajectories have yet to be explored.
... The highly facultative nature of the association between termite alates and nematodes would indicate a commensal interaction, as nematodes may opportunistically invade subterranean termite nests from surrounding soils and feed on the microbiome associated with the termite nest (Chouvenc et al. 2013a). During dispersal flight events of mature termite colonies, nematodes can opportunistically use termite alates as vehicles (passively or actively) to disperse in the environment and colonize new niches, in a case of phoresy. ...
... This strongly supports the claim that termite colonies can independently acquire nematodes such as Bunonema and Halicephalobus from surrounding soils and from within-colony transmission. The multiple origins of such associations make it opportunistic and dynamic, as the termite colony can observe ecological successions of nematodes over its life span (Chouvenc et al. 2013a). Therefore, our results do not support the von Lieven and Sudhaus (2008) hypothesis of a termite-specialized Halicephalobus. ...
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Termites and their nests are potential resources for a wide assemblage of taxa including nematodes. During dispersal flight events from termite colonies, co-occurring nematodes in the nest may have phoretic opportunities to use termite alates as transportation hosts. The two subterranean termite species Coptotermes gestroi (Wasmann) and Coptotermes formosanus Shiraki are both invasive and established in south Florida. Alates of both species (n = 245) were collected during dispersal flight events in 2015-2016 from six locations, of which 30 (12.2%) were associated with one or more species of nematodes. Species of Bunonema Jägerskiöld (Rhabditida: Bunonematidae), Halicephalobus Timm (Rhabditda: Panagrolaimidae), and Poikilolaimus regenfussi (Sudhaus) Sudhaus and Koch (Rhabditida: Rhabditidae) were isolated from 5.3, 4.9, and 0.4% of termite alates, respectively, and Bunonema and Halicephalobus were concomitant in 1.6% of alates. Additional C. formosanus alates were field-collected to establish laboratory colonies in sterilized rearing containers (SRC) to determine if alate-associated nematodes would colonize the newly established nest and/or brood. Among 1-yr-old termite colonies reared in SRCs, 26.9% of the colonies were positive for nematodes confirming that within-colony transmission of nematodes occurred. All three isolated nematode genera are free-living bacterivores capable of asexual reproduction. This suggests that these common co-occurring, termite-associated nematodes are opportunistic and facultative symbionts that receive increased opportunities of geographical dispersion through phoresy during termite dispersal flight events.
... Besides the physiological defense of every individual, insect societies have evolved a suite of collective mechanisms of pathogen defense, termed 'social immunity', which has surely allowed to cope with high pathogen risks associated with group living (Boomsma et al. 2005;Cremer et al. 2007Cremer et al. , 2018Cremer and Sixt 2009;Wilson-Rich et al. 2009;Masri and Cremer 2014;Malagocka et al. 2019;Liu et al. 2019). These collective immune responses are based on interactions between individuals, such as allogrooming (Qiu et al. 2014;Westhus et al. 2014), antimicrobial transfers between workers through socially exchanged fluids (i.e., trophallaxis; Hamilton et al. 2011;Konrad et al. 2012), deposition of antimicrobial substances on nest galleries (Aguero et al. 2021a;Chouvenc et al. 2013;Tranter et al. 2014), and nest hygiene (Hart and Ratnieks 2002;Sun and Zhou 2013;Farji-Brener et al. 2016;Perreira et al. 2020). In addition to group living, elevated levels of relatedness within colonies facilitate disease spread among genetically similar worker hosts. ...
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Group diversity is usually associated with a reduced risk of disease outbreak and a slower rate of pathogen transmission. In social insects, multiple mating by queens (polyandry) evolved several times although reducing worker’s inclusive fitness. One major hypothesis suggests that polyandry has been selected for to mitigate the risk of outbreak thanks to increased genetic diversity within colonies. We investigated this hypothesis in the ant Cataglyphis mauritanica , in which nestmate workers are produced by several clonal, single-mated queens. Using natural colonies, we correlated genetic diversity with worker survival to a fungal entomopathogen. We further tested whether workers from different paternal lineages (but a common maternal genome) show differential resistance in experimentally singleor multiple-patriline groups, and whether an increased number of patrilines in a group improved disease incidence. We show that workers from distinct patrilines vary in their resistance to pathogen in single-patriline colonies, but the difference among patrilines disappears when they are mixed in multiple-patriline colonies. Furthermore, pathogen resistance was affected by the number of patrilines in a group, with twoand three-patriline groups being more resistant than single-patriline groups. However, resistance did not differ between groups made of two and three patrilines; similarly, it was not associated with genetic diversity in natural colonies. Overall, our results suggest that collective disease defenses might homogenize workers’ resistance from different patrilines and, thereby, stabilize colony resistance.
... However, starting in 1995, the colony progressively accumulated old workers until 1997 when the colony finally collapsed and died (as a result, monitoring was terminated), supporting the observations by Grace et al. (1995) and Chouvenc (2018) that senescent colonies primarily contain old individuals. Such observation reveals that reproduction stopped relatively suddenly, with the putative death of the queen(s) in late 1994, as it was previously observed that in absence of reproduction, Coptotermes workers and soldiers can survive for 3-4 years in laboratory and then die of old age (Chouvenc et al., 2013b). Alternatively, queens may stop laying eggs several months prior to their death (Bess 1970), implying that reproduction may have stopped while the presence of the live queen could have temporarily inhibited the production of secondary reproductives (Costa-Leonardo et al., 2004;Chouvenc and Su, 2014), although the socio-physiological processes involved in the emergence of replacement or supplementary reproduction in Coptotermes remain poorly understood. ...
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A eusocial insect colony represents a complex biological entity that must ensure degrees of perennity once it reaches maturity (production of dispersing imagoes over many successive years) to optimize its reproductive success. It is known that a subterranean termite colony invests differentially in different castes over time and adjusts colony functions depending on colony internal and external conditions over many years of activity. However, the current study demonstrates that Coptotermes formosanus Shiraki field mature colonies go through dramatic demographic changes and breeding structure shifts, even many years after they have reached reproductive success. By analyzing the changes in age demography of C. formosanus colonies from four field sites, we here provide a new perspective on how a colony may function over decades, which reveals that each colony demographic trajectory is unique. In a way, throughout its life, a termite colony displays its own “demographic individuality” that drives its growth, its foraging ability, its competitiveness, its age demography, its senescence and ultimately its death. This study is therefore a narrated story of the life -and death- of different C. formosanus field colonies over decades of observation.
... Uncircumstantial associations with other well-known eusocial insects, the termites (Blattodea, Termitidae and Rhinotermitidae), have been documented for a few isolates: Talaromyces flavus from the coarse debris of wood infested by Reticulitermes sp. in Mississippi (USA) [24], Talaromyces spp. from the nests of Coptotermes formosanus under experimental rearing conditions in Florida (USA) [40] and combs of the fungus-growing species Macrotermes carbonarius in Vietnam [39], while Talaromyces stollii was reported from the combs of Macrotermes barneyi in China [47]. ...
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Facing the urgent need to reduce the input of agrochemicals, in recent years, the ecological relationships between plants and their associated microorganisms have been increasingly considered as an essential tool for improving crop production. New findings and data have been accumulated showing that the application of fungi can go beyond the specific role that has been traditionally assigned to the species, employed in integrated pest management as entomopathogens or mycoparasites, and that strains combining both aptitudes can be identified and possibly used as multipurpose biocontrol agents. Mainly considered for their antagonistic relationships with plant pathogenic fungi, species in the genus Talaromyces have been more and more widely reported as insect associates in investigations carried out in various agricultural and non-agricultural contexts. Out of a total of over 170 species currently accepted in this genus, so far, 27 have been found to have an association with insects from 9 orders, with an evident increasing trend. The nature of their mutualistic and antagonistic relationships with insects, and their ability to synthesize bioactive compounds possibly involved in the expression of the latter kind of interactions, are analyzed in this paper with reference to the ecological impact and applicative perspectives in crop protection.
... If we assume that the comb took over the role of gut protozoa it is likely that the ancestral comb was already inhabited by cellulolytic microorganisms. It has also been shown that in Coptotermes abandoned carton nests or parts of the nest which are abandoned can be colonized by saprophytic basidiomycetes such as Leucocoprinus (Chouvenc, Bardunias, et al. 2013). This indicates that the ancestral comb was an attractive substrate for microorganisms. ...
... However, the subterranean termite fecal nest is a dynamic modular system, with a heterogeneous nutritional quality of the carton nest within the colony (Supp Fig. S6 [online only]). New galleries and foraging sites are excavated regularly, whereas other parts of the nest are abandoned by the colony, so if harmful microbes become dominant in a part of the nest, the area is abandoned and sealed off by the termites (Chouvenc and Su 2012, Yanagawa et al. 2012, Chouvenc et al. 2013b). Therefore, we agree with Stanton's (2003) hypothesis: '[with] lineages of symbionts spatially segregated within hosts with modular construction, it may be possible for the host to associate with a more rewarding partner simply by eliminating a less productive module', where the subterranean termite foraging territory is a dynamic system. ...
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Mutualistic associations between insects and microorganisms must imply gains for both partners, and the emphasis has mostly focused on coevolved host-symbiont systems. However, some insect hosts may have evolved traits that allow for various means of association with opportunistic microbial communities, especially when the microbes are omnipresent in their environment. It was previously shown that colonies of the subterranean termite Coptotermes formosanus Shiraki (Blattodea: Rhinotermitidae) build nests out of fecal material that host a community of Streptomyces Waksman and Henrici (Actinomycetales: Streptomycetaceae). These Actinobacteria produce an array of bioactive metabolites that provides a level of protection for termites against certain entomopathogenic fungi. How C. formosanus acquires and maintains this association remains unknown. This study shows that the majority of Streptomyces isolates found in field termite fecal nest materials are identical to Streptomyces isolates from soils surrounding the nests and are not vertically inherited. A survey of Streptomyces communities from C. formosanus fecal nest materials sampled at 20 locations around the world revealed that all nests are reliably associated with a diverse Streptomyces community. The C. formosanus fecal nest material therefore provides a nutritional framework that can recruit beneficial Streptomyces from the soil environment, in the absence of long-term coevolutionary processes. A diverse Streptomyces community is reliably present in soils, and subterranean termite colonies can acquire such facultative symbionts each social cycle into their fecal nest. This association probably emerged as an exaptation from the existing termite nest structure and benefits both the termite and the opportunistic colonizing bacteria.
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Results of previous field excavation of nest structure of Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae), the Formosan subterranean termite, indicated that the total length of the gallery system ranged up to 580 m, and its total space may occupy >34,800 cm³. Because Formosan subterranean termite does not build mounds, it has been speculated that it creates tunnel space by compacting soil. The objective of this study is to test a “modified soil-compaction hypothesis” that Formosan subterranean termite removed and compacted soil to increase space during tunnel excavation. Contrary to the hypothesis, the deposited sand was less dense than the unexcavated sand in all replications; thus, we rejected the soil-compaction hypothesis. Instead, we offered wood-consumption hypothesis that termites gain the tunnel space as a result of consuming wood. When termites were placed with wood pieces for 30 d, the decreased volume of consumed wood was significantly higher than the increased volume of carton material. The net increased space is ≈;50% of volume of consumed wood. We speculate that the space created by wood consumption could be transformed into tunnel space during soil displacement.
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Eight species of mites were found in association with laboratory cultures of the eastern subterranean termite, Reticulitermes flavipes Kollar. These included members of the Orders Acariformes and Parasitiformes. Among the Acariformes were members of the Acaridae (Acarus farris Oudemans, Acarus sp., and Caloglyphus sp.) and the Histiostomatidae (Histiostoma sp.). Among the Parasitiformes were members of the Machrochelidae [Macrocheles muscaedomesticae (Scopoli)], Parasitidae [Parasitus americanus (Berlese), and Parasitus sp.], and the Ascidae [Proctolaelaps hypadari (Oudemans) = P. pygmaeus (Muller)]. Some observations were recorded on termite-mite interactions, mite-mite interactions and mite-fungus interactions.
I documented the use by nesting birds and availability of arboreal termite nests (termitaria) in the Peruvian Amazon. Birds occupy about 1% of the termitaria annually, suggesting that termitarium availability does not limit reproductive output. Birds choose termitaria that are larger and higher than average, and the three most common termitarium-nesting species differ in their use of termitaria. Two species of Brotogeris parakeets use termitaria with similar characteristics, but Tui Parakeets (B. sanctithomae) nest in young forests and edge habitats whereas Cobalt-winged Parakeets (B. cyanoptera) use mature forests. Termitaria used by Black-tailed Trogons (Trogon melanurus) are larger and lower than those used by the two Brotogeris species. The contention that birds usually nest in termitaria still occupied by termites was upheld, but the presence or absence of termites did not explain a significant proportion of the difference between used and available termitaria after removing the effects of height, volume, and substrate type. Birds choose to nest in termitaria inhabited by both termites and aggressive biting ants (Dolichoderus sp.). These ants may be protecting the birds' nests by attacking predators or by providing a sort of “olfactory camouflage.”
A single female specimen collected from a termite nest in Laos and preserved in alcohol was initially examined and photographed by SD before being sent to RHLD, who mounted it on a slide in Berlese Fluid (Disney 2001). It proved to be an unknown genus which is described below. The termite host was identified as Macrotermes gilvus (Hagen) with the keys of Ahmad (1965), Chhotani (1997) and Tho (1992) and is not covered by the monograph on Chinese termites (Huang, Li & Zu 1989), which covers more species of this termite genus but does not include this species. The major soldiers are somewhat more robust compared with some specimens from Malaysia attributed to this species (Disney, Neoh & Lee 1999). The termite species, whose type series came from Java, is evidently somewhat variable with the differences being either due to geographical variation, as currently assumed, or possibly this widely distributed species may prove to be a sibling species complex. Voucher specimens from the termite nest are deposited in Copenhagen (queen, soldiers, workers) and Cambridge (soldiers, workers).
This chapter reviews the advances made in our knowledge of the effects of termites on the physical, chemical and biological properties of soils. Emphasis has been placed on more recent contributions, particularly those that explore new concepts in the ecology of termites and soils. There are sections dealing with the effects of termite activity on soil profile development, soil physical properties, soil chemical properties, soil microbiology and plant growth. The physical effects of termites on soils range from micromorphological to soil profile evolution and structure. Recent evidence points to the substantial positive influence of termites on soil hydraulic conductivity and infiltration rates. Their influence on organic matter decomposition and nutrient recycling rates are well recognized and in some landscapes termite mounds act as foci for nutrient redistribution. New information on the microbiology of termite mounds suggests that most are sites of diverse bacterial and fungal activity. Furthermore, the association between mound-building termites and the microbial population present in the structures has a synergistic effect on organic matter decomposition and hence nutrient cycling and availability. Examination of the effects of termite activity on plant production generally indicates a positive influence.
Application of large quantities of persistent insecticides to control termites poses an increasing environmental threat as human populations increase because of possible contamination of water resources. Chemical insecticides may also have an effect on non-target organisms. Biological control rather than persistent insecticides may provide an environmental friendly and long-lasting insect control. Our previous studies showed that on PDYA medium Aspergillus flavus Link and Trichoderma harzianum Rifai which are associated with Coptotermesformosanus Shiraki can control the brown rot fungus, Gloeophyllum trabeum (Pers.: Fr.) Murril, a destructive wood pathogen. Our goal was to determine if A. flavus and T. harzianum have a negative effect on the survival of C. formosanus. To test this, termites were surface sterilized and one of three different concentrations of fungal spore suspension was topically applied to the termites. The number of surviving termites was counted after 12 days of incubation. Results showed that A. flavus was toxic to termites, but T. harzianum was not. A. flavus has potential to be used as biocontrol agent to control brown rot fungus, G. trabeum and also to control C. formosanus; while T. harzianum appears to benefit termites by controlling a competitive wood consumer, G. trabeum.