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ECOLOGY AND POPULATION BIOLOGY
Resource Opportunities From the Nest of Dying Subterranean Termite
(Isoptera: Rhinotermitidae) Colonies: A Laboratory Case of Ecological
CAROLINE A. EFSTATHION,
MONICA L. ELLIOTT,
AND NAN-YAO SU
Ann. Entomol. Soc. Am. 106(6): 771Ð778 (2013); DOI: http://dx.doi.org/10.1603/AN13104
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 䉷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 28⬚C 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.)
772 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 106, no. 6
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
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
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, n⫽3) 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.)
November 2013 CHOUVENC ET AL.: ECOLOGICAL SUCCESSION IN SUBTERRANEAN TERMITES 773
As the fungal mycelia invaded the carton nest of
dying colonies, the prevalence of mycophagous coll-
embolans (Entomobryidae: Entomobryinae; Fig. 3A)
increased (P⫽0.004; 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
(P⬍0.001; 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
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
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
(n⫽2) and dying termite colonies (n⫽3). 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 (P⬍0.05; 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.)
774 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 106, no. 6
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.)
November 2013 CHOUVENC ET AL.: ECOLOGICAL SUCCESSION IN SUBTERRANEAN TERMITES 775
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
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
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
776 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 106, no. 6
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Received 26 June 2013; accepted 29 August 2013.
778 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 106, no. 6