ArticlePDF AvailableLiterature Review

Biology of Subterranean Termites: Insights from Molecular Studies of Reticulitermes and Coptotermes


Abstract and Figures

Molecular genetic techniques have made contributions to studies on subterranean termites at all levels of biological organization. Most of this work has focused on Reticulitermes and Coptotermes, two ecologically and economically important genera. DNA sequence data have significantly improved our understanding of the systematics and taxonomy of these genera. Techniques of molecular biology have provided important new insights into the process of caste differentiation. Population genetic markers, primarily microsatellites, have furthered our understanding of the life history, population biology, community ecology, and invasion biology of subterranean termites. Recent results on the behavioral ecology of subterranean termites reveal a picture different from long-held views, especially those concerning colony breeding structures and foraging ranges. As additional molecular tools and genomic resources become available, and as more subterranean termite researchers incorporate molecular techniques into their approaches, we can expect accelerating advances in all aspects of the biology of this group.
Content may be subject to copyright.
ANRV363-EN54-20 ARI 23 October 2008 13:50
Biology of Subterranean
Termites: Insights from
Molecular Studies of
Reticulitermes and Coptotermes
Edward L. Vargo1and Claudia Husseneder2
1Department of Entomology, North Carolina State University, Raleigh,
North Carolina 27695-7613; email: ed
2Department of Entomology, Louisiana State University, Agricultural Center,
Baton Rouge, Louisiana 70803; email:
Annu. Rev. Entomol. 2009. 54:379–403
First published online as a Review in Advance on
September 15, 2008
The Annual Review of Entomology is online at
This article’s doi:
Copyright c
2009 by Annual Reviews.
All rights reserved
Key Words
Rhinotermitidae, population genetics, molecular ecology,
microsatellites, caste determination, breeding structure
Molecular genetic techniques have made contributions to studies on
subterranean termites at all levels of biological organization. Most of
this work has focused on Reticulitermes and Coptotermes, two ecologically
and economically important genera. DNA sequence data have signifi-
cantly improved our understanding of the systematics and taxonomy of
these genera. Techniques of molecular biology have provided important
new insights into the process of caste differentiation. Population genetic
markers, primarily microsatellites, have furthered our understanding
of the life history, population biology, community ecology, and inva-
sion biology of subterranean termites. Recent results on the behavioral
ecology of subterranean termites reveal a picture different from long-
held views, especially those concerning colony breeding structures and
foraging ranges. As additional molecular tools and genomic resources
become available, and as more subterranean termite researchers in-
corporate molecular techniques into their approaches, we can expect
accelerating advances in all aspects of the biology of this group.
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
Click here for quick links to
Annual Reviews content online,
Other articles in this volume
Top cited articles
Top downloaded articles
• Our comprehensive search
Fur ther
ANRV363-EN54-20 ARI 23 October 2008 13:50
Subterranean termites (Rhinotermitidae) are a
large and important group of social insects.
They are the most widely distributed family
of termites, occurring throughout the tropical,
subtropical, and temperate regions of the world
(32). They are especially abundant in temper-
ate areas, where their biomass can approach that
of many tropical termites (15, 39). In addition,
they frequently attack human-made structures,
exerting a major economic impact estimated to
be as high as $11 billion per year in damage and
control costs in the United States alone (119).
Subterranean termites occupy an important
evolutionary position within the Isoptera. Ter-
mites are typically divided into the higher ter-
mites (Termitidae), containing some 80% of all
species, and the lower termites, represented by
the remaining six families. Of the lower ter-
mites, the Rhinotermitidae are the most de-
rived (59). Reticulitermes and Coptotermes are es-
pecially important as transitional taxa between
the lower and higher termites for three rea-
sons. First, new phylogenetic analyses (5, 59,
75) show that the clade containing these genera
is likely the sister group of the Termitidae, indi-
cating that Reticulitermes and Coptotermes share
an especially close affinity with the higher ter-
mites. Second, these two genera contain more
species than any other genus of subterranean
termites and are among the most species-rich
genera of all the lower termites (63). Third, they
exhibit features intermediate between lower
and higher termites (59), such as feeding habits
typical of lower termites, nesting habits inter-
mediate between the single-site nesting of more
basal lower termites (in which colonies use a
single piece of wood as both nesting site and
food source) (116) and the central-site nesting
of higher termites (in which colonies use mul-
tiple sources of food away from the nest site)
(116), as well as the presence of a true worker
caste, a trait primarily associated with higher
termites. Thus, understanding basic features of
the life history, behavior, and ecology of Reti-
culitermes and Coptotermes can provide insights
into the evolution and remarkable radiation of
the higher termites.
Termites have attracted increasing attention
from entomologists. This is especially true of
subterranean termites, where a search of the
worldwide literature shows that between 2000
and the date of this review there have been
more papers published on this group (934) than
during all of the previous century (694). Al-
though aspects of the biology of this group have
been the subjects of many excellent reviews,
these have tended to be regionally and/or taxo-
nomically limited in nature. Some more recent
reviews of this group include summaries of the
biology of Reticulitermes spp. (130) and Coptoter-
mes formosanus (122, 142), the life histories of
termites in general (116), the evolution and de-
velopment of termite castes (109), and the gut
symbionts of wood-feeding termites (16).
Molecular genetic methods are providing
exceptional new insights into the biology of
subterranean termites. In addition to elucidat-
ing such basic processes as development and
caste differentiation, molecular techniques give
us a window into the breeding structure, as well
as colony and population dynamics, that has re-
mained elusive owing to the cryptic nesting and
foraging habits characteristic of these species.
Here, we review some of the progress that has
been made using molecular methods in the ar-
eas of taxonomy, caste differentiation, breeding
structure, behavioral biology, and community
ecology. We focus on Reticulitermes and Cop-
totermes because these genera have been the
subject of more than three-quarters of these
studies, and because these genera contain the
most economically important termites in many
parts of the world, especially temperate and
subtropical regions.
Subterranean termites pose many taxonomic
challenges at the species level and above. The
taxonomy of both Reticulitermes and Coptotermes
380 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
Table 1 Species status of Reticulitermes in North America
Species Distribution Status Reference(s)
R. flavipes Throughout eastern and central United States Valid (11)
R. arenincola Sandy soils near the Great Lakes Nomen dubium (4)
R. virginicus Throughout eastern and central United States Valid (4)
R. hageni Throughout eastern and central United States Valid, but may be species complex (44)
R. malletei Eastern United States Valid (11)
R. tibialis Western and Midwestern United States Valid, but may be species complex (24, 44)
R. hesperus Western United States Valid, but may be species complex (24, 44)
R. okanaganensis Pacific Northwest Valid (124)
is far from settled. At the present time, these
two genera are by far the largest within the
Rhinotermitidae, with 75 and 71 described
species, respectively, accounting for nearly half
of all subterranean termite species among the
15 recognized genera (63). The large number
of species in these two genera is due largely
to a plethora of new species descriptions that
have appeared in China over the past 60 years
(31). These genera are in need of careful mono-
graphic revisions, with particular emphasis on
Oriental forms.
Existing taxonomic keys are spotty in cover-
age, both in terms of taxonomic breadth and ge-
ographic region, and the characters used to dis-
tinguish species are often too variable to provide
reliable determinations (125). The recent appli-
cation of molecular genetic data, especially in
combination with cuticular hydrocarbon com-
position, morphological characters, and flight
phenologies, has helped clarify the taxonomy
of these genera.
The past five years have seen significant
changes in the taxonomy of Reticulitermes in the
United States, where there are currently seven
recognized species (Table 1). On the basis of
primarily molecular data, these changes include
the probable synonomy of one species (R. aren-
incola is considered to be R. flavipes) (4) and the
addition of two new species: R. malletei (4) in
the eastern United States and R. okanaganen-
sis in the Pacific Northwest (124). From all the
available evidence, there are likely other unde-
scribed species, especially within R. tibialis and
R. hageni, both of which appear to be species
complexes (24, 44).
Compared to the still unsettled situation in
the United States, the taxonomic status of Reti-
culitermes seems well resolved in Europe, where
there are currently seven recognized taxa:
R. balkanensis,R. grassei,R. banyulensis,R. urbis,
R. lucifugus lucifugus,R. l. corsicus, and the in-
troduced R. flavipes (=R. santonensis) (22, 134).
These taxonomic designations have been sup-
ported by a number of studies using DNA
sequence data (13, 81, 82, 134).
What little taxonomic work has been done
on Coptotermes suggests this genus is in seri-
ous need of revision. The widespread and de-
structive C. gestroi was apparently described
as several different species that have recently
been synonymized (66, 144), including C. hav-
ilandi and C. vastator, previously recognized
as invasive pest species. In Australia, where
there are six currently described Coptotermes
species, there are likely several more unrecog-
nized species (74). We can certainly expect to
see many taxonomic changes in this genus in
the future as greater attention is given to this
widespread and economically important taxon.
Molecular Tools for
Species Identification
The application of molecular genetic tech-
niques to clarify species relationships has
provided PCR-based tools for species identifi-
cation. PCR-restriction fragment length poly-
morphism methods have been developed for
distinguishing among Reticulitermes species in
the south-central United States (125) and for
differentiating C. formosanus from other species Biology of Subterranean Termites 381
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
of Coptotermes (126). The advantages of such di-
agnostic methods are (a) they remove much of
the ambiguity of identification based on mor-
phological keys, (b) they can be used with any
caste or developmental stage, and (c) they can be
performed on a single individual. These tech-
niques have allowed for more extensive stud-
ies of species ranges, for detection of species
introduced into locations outside their native
ranges, and for the determination of the rel-
ative abundance of species in particular geo-
graphic areas (7–10, 125). For example, the
relative abundance of Reticulitermes species in
the eastern and central United States has re-
ceived much recent attention. Three species,
R. flavipes,R. virginicus, and R. hageni, are sym-
patric over much of this region (118). In addi-
tion, they often occur together with R. malletei
(4) in the eastern United States, R. tibialis in
the central United States, and the introduced
C. formosanus throughout much of the south-
ern portions of their ranges (120). Studies of
samples collected across the range (7–9, 27, 92,
101) show varying species compositions, with
R. flavipes occurring most commonly, ranging
from 74% to 90% of all samples, and R. vir-
ginicus and R. hageni present at much lower fre-
quencies. The one clear exception to this pat-
tern was a South Carolina coastal site, where
R. hageni was the most common species, occur-
ring at a slightly higher frequency (43%) than
R. flavipes (37%) (141).
Little is known about the determinants of
species diversity in subterranean termite com-
munities, or the factors that contribute to co-
existence of species that are apparently so sim-
ilar in their ecological roles and life histories.
Future studies of relative species abundance,
combined with population genetic characteris-
tics such as gene flow and dispersal, will pro-
vide insights into both environmental factors
and population processes that influence species
richness in subterranean termite communities.
Phylogeography and Diversification
Phylogeography, the study of historical pro-
cesses and their effects on species distributions
(14), has great potential to elucidate the evolu-
tionary relationships among subterranean ter-
mite taxa, the processes leading to speciation,
and the factors determining current distribu-
tions. So far only Reticulitermes spp. in southern
Europe and the Middle East have received at-
tention in this regard (6, 20, 22, 68, 80–82, 85).
Results of these studies suggest that there were
four refugia scattered through southern Europe
and the Middle East during the last glacial max-
imum, each harboring one or more species or
subspecies. The northward expansion and ra-
diation of populations from these refugia fit
reasonably well with the current distributions
of species and subspecies throughout southern
Europe, especially if one assumes that the rate
of mitochondrial DNA evolution in this group
has occurred at 10 times the rate normally as-
sumed for insects, as appears to be the case (80).
Our understanding of the taxonomy and evolu-
tionary history of the Reticulitermes spp. would
benefit from similar analyses in other parts of
the world.
Termites are unique among the social insects
because they undergo incomplete metamor-
phosis and display a remarkably complex and di-
versified caste polyphenism (109). Within each
mature colony, morphologically differentiated
castes (workers, soldiers, reproductives) and un-
differentiated immatures cooperate in a highly
integrated manner. This functional network of
behaviorally and morphologically specialized
individuals is the cornerstone of the advanced
eusociality characteristic of termites.
The terminology regarding caste, especially
in the lower termites, is complicated and some-
what controversial. Here we follow the nomen-
clature of Thorne (128). There appears to
be considerable variation in the developmen-
tal pathways within the large and diverse fam-
ily Rhinotermitidae (109), but Reticulitermes
and Coptotermes share many similarities in their
382 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
caste patterns. In principle, larvae develop into
workers or nymphs. Nymphs develop either
into alates with wings and eyes (imagoes) that
disperse and become primary colony founders,
or they develop into brachypterous (second
form) neotenic reproductives with rudimentary
wings and no eyes that do not disperse but
supplement or replace the reproductives within
the colony. Workers can transform into apter-
ous (third form) neotenic reproductives with
no wings and eyes, remain workers, or become
presoldiers that molt into soldiers. Diagrams
depicting the various developmental pathways
within colonies of subterranean termites have
been presented for Reticulitermes spp. (70, 145),
C. formosanus (106), and C. lacteus (110).
As with other types of polyphenisms, caste
determination is the result of the interaction of
endogenous and exogenous factors during crit-
ical stages in development (96). Although little
progress has been made in identifying exoge-
nous factors involved in caste determination in
termites, morphogenic hormones, primarily ju-
venile hormone ( JH), play a pivotal role in caste
determination (46, 96). With the new tools of
molecular biology, such as expressed sequence
tag (EST) libraries, DNA arrays, quantitative
PCR, and gene silencing via RNA interference,
termite researchers are now able to investigate
the molecular mechanisms modulating the ac-
tion of JH, as well as elucidate the downstream
effects of JH and the genomic network under its
control. In addition, molecular studies are pro-
viding important new insights into gene expres-
sion levels associated with caste-specific mor-
phogenesis in general.
Soldier Differentiation
A number of studies have shown that in both
Reticulitermes and Coptotermes relatively high JH
levels in workers will induce them to molt into
soldiers (33, 84, 100, 113). On the basis of gene
expression profiles and gene silencing experi-
ments (114, 115, 145–147), Zhou et al. (147)
proposed that hexameric proteins play a cen-
tral role in regulating soldier caste determi-
nation by modulating the availability of JH in
the hemolymph. A first approach to determine
how JH action modulates expression of caste-
specific genotypes is to identify genes whose
expression levels change in response to JH ac-
tion during caste differentiation. Zhou et al.
(147) identified various genes associated with
morphogenesis that were up- or downregulated
in response to silencing of a hexamerin gene,
including genes involved in signal transduc-
tion, transcription, translation, and cytoskele-
tal structure. These genes are likely part of the
hexamerin-controlled JH-dependent gene net-
work that regulates soldier differentiation.
Zhou et al. (147) proposed a model in which
JH production is influenced by extrinsic and in-
trinsic factors. According to the model, various
intrinsic factors modulate hexamerin levels that
in turn attenuate the effects of JH. The pos-
sible extrinsic factors affecting JH production
include both environmental and social stim-
uli. Intrinsic factors that may affect JH pro-
duction and/or hexamerin levels are nutritional
status, allatostatins (143), sex, and developmen-
tal stage. The link between caste differentiation
and nutritional status is especially intriguing
given the role of hexamerins as both storage
proteins and putative JH binding proteins that
may regulate caste polyphenism in the euso-
cial wasp Polistes metricus (49), suggesting a
widespread role for hexamerins in social insect
caste determination.
Differentiation of
the Reproductive Caste
Although the process of reproductive caste dif-
ferentiation, either in the form of imagoes or
neotenics, has received less attention than sol-
dier determination, it is likely that many of the
same processes are involved (96). Elliott & Stay
(33) found elevated JH titers in the differenti-
ation of both soldiers and apterous neotenics
from workers in R. flavipes, but individuals ap-
parently destined to become soldiers had higher
JH levels than those developing into neoten-
ics. Although both apterous and brachypter-
ous neotenics readily develop in colonies of
Reticulitermes lacking functional reproductives Biology of Subterranean Termites 383
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
(93, 102, 103), neotenics are not formed in labo-
ratory colonies of C. formosanus devoid of active
reproductives (106). Raina et al. (106) have pro-
posed that nymph development and subsequent
neotenic differentiation in this latter species re-
quire a yet undetermined nymph induction fac-
tor produced by reproductives.
To shed light on the genomic network in-
volved in differentiation of the reproductive
caste, Scharf et al. (115) identified genes that
were differentially expressed in nymphs and re-
productives. A gene coding for a hexamerin
protein showed highest expression in nymphs
and neotenic reproductives and is thus assumed
to play a role in reproductive differentiation
(115), possibly by modulating the availability
of JH in the hemolymph. Following the gen-
eral model of insect development, low JH titers
during critical JH-sensitive periods in develop-
ment almost certainly regulate differentiation
into reproductives in subterranean termites, al-
though the number and timing of these critical
periods are likely to differ between develop-
ment into primary reproductives and develop-
ment into neotenics (96).
Genetic Caste Determination
Differentiation into primary reproductives in
R. speratus, at least in the laboratory, may have a
sex-linked genetic component (45). According
to a proposed model, the production of primary
reproductives occurs exclusively in colonies
headed by neotenics, but so far this has not
been confirmed in field colonies of R. speratus
or other Reticulitermes spp. Existing data on R.
flavipes and R. virginicus do not support genetic
caste determination as an important mechanism
regulating alate production in these species, be-
cause alates are not produced mainly or exclu-
sively by neotenic-headed colonies in the field
(17, 28). Although the possibility of genetic
caste determination in subterranean termites is
intriguing, additional studies are needed to con-
firm that this occurs under field conditions.
Although we still have a very rudimentary
understanding of the genetic and physiological
mechanisms influencing development and caste
determination in subterranean termites, there
have been several important and promising ad-
vances in this field. It is clear that the applica-
tion of molecular tools together with reliable
bioassays have shed new light on the processes
regulating caste polyphenism.
In general, colonies of subterranean termites
are founded by monogamous pairs of repro-
ductives following large synchronous mating
flights that occur in response to climatic condi-
tions during species-specific times of the year
(61, 98). After the mating flight, individuals
land on the ground, shed their wings, and begin
the process of searching for partners. Partner-
finding in some subterranean termite species,
including Reticulitermes spp., is facilitated by a
sex pheromone emitted by the female, whereas
in other species, such as C. formosanus, females
do not appear to produce a chemical attractant
(99, 107). After shedding their wings, partners
run in tandem with the female in the lead. As
soon as a suitable nest site is found, pairs move
underground or into wood to mate and repro-
duce. There is high mortality and thus intense
selection during the founding phase.
Partner Selection
There are a number of reasons to believe that
both male and female termites should be se-
lective in their choice of mates. First, termites
mate for life and perform intensive biparental
care. Second, large body size and/or weight can
be advantageous in mate selection, because the
first generation of larvae is entirely dependent
on the fat reserves of the founding pair until for-
agers emerge to provide the young colony with
nutrition (67, 88, 117). Third, genetic charac-
teristics of potential partners, such as genetic
diversity and relatedness, may influence colony
fitness. For example, males of C. formosanus
are more likely to pair with females exhibiting
higher levels of heterozygosity (55). However,
tandem pair formation in C. formosanus appears
384 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
to be random with respect to kinship (55), as was
reported for the Japanese subterranean termite,
R. kanmonensis (67), and R. flavipes (28). The lack
of evidence supporting kin discrimination dur-
ing colony founding in subterranean termites is
surprising considering the mounting evidence
of negative effects of inbreeding in many plants
and animals (64) and in subterranean termites
(28, 36, 54), but data on more species, espe-
cially those that undergo short-range dispersal
flights, are needed before we can rule this out
as a mechanism promoting outbreeding in this
Dispersal Distances
One possible mechanism that could promote
outbreeding is long-range dispersal of alates
reducing the likelihood that nestmates en-
counter each other during tandem pair for-
mation. Flight distances appear to vary among
species of subterranean termites, ranging from
a few meters to 1 km or further, and likely have
been underestimated in some cases (61, 98).
Genetic studies of alates from mass swarms of
C. formosanus in New Orleans, Louisiana, sug-
gest alates can fly at least 1 km (57). Dispersal
distance in this species is sufficient to guaran-
tee mixing of up to 29 colonies within a swarm
aggregation in areas of high population den-
sity; under conditions of random mating up to
90% of alate pairings would be among non-
nestmates (57).
Studies of gene flow in Reticulitermes sug-
gest that alate dispersal distances can be suffi-
cient to promote outbreeding in some species,
e.g., R. virginicus (28), yet insufficient in oth-
ers, leading to the probable pairing of related
primary reproductives during colony founding,
e.g., R. hageni (138, 141). In a study of R. flavipes,
some 20% of founding pairs were composed of
likely siblings, but few of these successfully es-
tablished colonies, presumably because of in-
breeding depression during colony foundation
(28). The apparent variation in the tolerance
to the potential effects of inbreeding in closely
related sympatric species merits further inves-
Colony breeding
structure: number
and degree of
relatedness of the
individuals within
Simple family
colony: group of
cohabiting individuals
produced by a
monogamous pair of
reproductives, usually
the primary founders
Extended family
colony: group of
cohabiting individuals
produced by multiple
inbred neotenic
descended from the
original founding pair
Sex-Biased Alate Production
by Colonies
Another potential mechanism promoting out-
breeding is sex-biased alate production by
colonies, in which individual colonies in-
vest predominantly in alates of one sex (61).
Such bias may occur as a function of colony
breeding structure. Experimentally orphaned
colonies of Australian Coptotermes spp. that were
subsequently headed by inbreeding neotenics
produced almost exclusively males (72, 111).
Genetic analysis of swarming alates of C. for-
mosanus found that male alates in most swarm
aggregations were significantly more inbred
than females (57), a finding consistent with pre-
dominant male production in neotenic-headed
(inbred) colonies. One factor promoting female
alate production in outbred colonies in this
species could be sexual selection favoring het-
erozygous females during mate selection (55),
as mentioned above. In R. virginicus, DeHeer
and Vargo (28) inferred that female alates were
produced primarily in inbred colonies on the
basis of lower levels of heterozygosity compared
to males. The extent of sex-biased alate pro-
duction and its possible role in promoting out-
breeding in subterranean termites deserve fur-
ther study.
After establishment by the founding pair,
colony growth is initially slow, reaching a pop-
ulation size after one year of about 30 to 50 in-
dividuals in the case of Reticulitermes spp. (130)
and 20 to 90 in C. formosanus (107, 122). During
this initial phase, the colony is a simple fam-
ily composed of a monogamous pair of repro-
ductives and their offspring. Eventually one or
both of the primary reproductives senesces or
dies, and these are replaced by neotenics, ei-
ther apterous or, more commonly, brachypter-
ous forms that develop from within the colony
(95, 130), producing an extended family colony.
The number of neotenics in these extended
family colonies can vary from a few to several Biology of Subterranean Termites 385
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
dozen, and these colonies can undergo several
generations of inbreeding. In addition to sim-
ple family and extended family colonies, it has
been assumed that colonies often fuse to create
genetically complex groups consisting of mixed
families (21, 87, 132).
Owing to the cryptic nesting habits of this
group, it has been difficult to conduct exten-
sive studies of colony breeding structure. How-
ever, this has changed with the application
of highly sensitive molecular genetic markers
(58), combined with population genetic model-
ing of subterranean termite breeding systems
(17, 132). The main approach to investigat-
ing colony breeding structure is to genotype
groups of foragers at numerous genetic loci us-
ing codominant markers, such as microsatellites
(27, 58, 136). The genotypes of the individuals
are then subjected to pedigree analysis to deter-
mine family structure.
Once the family structure of a colony is de-
termined, more detailed information about the
relatedness of reproductives, degree of inbreed-
ing within the colony, and the numbers of re-
productives within extended family colonies can
be inferred from the coefficients of inbreeding
and relatedness (17, 132). There is significant
variation in all aspects of colony breeding struc-
ture both within and among species (Table 2).
In most cases, colonies are either simple fam-
ilies or extended families, with simple families
more common in many populations.
Simple Family Colonies
Colony breeding structure has now been char-
acterized in populations of six species of Retic-
ulitermes, with four species represented by mul-
tiple populations (Table 2). In most species and
most populations, the majority of colonies—
often 75% or more—are simple families. One
major exception is the European species R. gras-
sei, in which simple families comprised a minor-
ity of colonies in all four populations studied,
with one population containing no simple fami-
lies at all. The other conspicuous exceptions are
(a) populations of R. flavipes in Massachusetts,
at the northern edge of the range of this species
where only about 25% of the colonies were sim-
ple families, and (b) populations of R. flavipes in
France, where this species was introduced and
no simple families have been found.
There is both inter- and intraspecific vari-
ation in the degree to which the kings and
queens heading simple family colonies are re-
lated. Colonies of R. flavipes,R. virginicus, and
R. hesperus appear to be headed by unrelated re-
productives, whereas the reproductives in sim-
ple family colonies of R. hageni and R. malletei
appear to be related (101, 138, 141), most likely
because primary reproductives often pair with
relatives during colony foundation (138). The
European species R. grassei exhibits variation
among populations, with closely related repro-
ductives in one French population and largely
unrelated reproductives in a Portuguese popu-
lation (Table 2).
Studies of Coptotermes have largely con-
cerned introduced populations of C. formosanus,
in which considerable variation in colony
breeding structure has been found (Table 2).
The proportion of simple families varies from
nearly 100% in two Japanese populations (139)
to no simple families present in a population
from the native range in southern China (54).
However, in six of nine C. formosanus popula-
tions studied to date, simple families were more
common than extended families. The degree
of relatedness between the kings and queens
heading simple families varies from essentially
zero in New Orleans to full siblings (r=
0.6) in one Japanese population (53, 139, 140).
In the only other Coptotermes species studied
to date, the Australian mound-building C. lac-
teus, all 39 colonies examined genetically (127)
were simple families headed by slightly related
Extended Family Colonies
Extended families can vary both in the numbers
of neotenics present, from a few to dozens, and
in the number of generations of inbreeding they
have undergone. Of particular importance in
inferring details regarding the breeding struc-
ture of extended families is the coefficient of
386 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
Table 2 Summary of colony breeding structures in Reticulitermes spp. and Coptotermes spp. termites as inferred by
microsatellite markers except where noted
Simple families Extended families Mixed families
(N=no. colonies) Percent
relatedaPercent FICb
Inferred no.
neotenics Percent
FIT Reference(s)
Reticulitermes flavipes
Central North
78.4% 19.7% –0.209 <10 1.9% 0.052 (27, 101, 135,
136, 138)
Charleston, South
72.2% 22.2% –0.140 <10 5.6% 0.030 (141)
27.3% 59.1% 0.097 >100 13.6% 0.289 (17)
Central Tennesseec
NR NR NR 0.260dNR NR 0.680a(108, 132)
Paris, Franced
0% N/A 100% 0.032 >100 0% 0.386 (30)
eron Island,
0% N/A 100% –0.001 >100 0% 0.168 (30)
Reticulitermes hageni
Raleigh, North
86.7% ++ 13.3% –0.257 <10 0% 0.357 (101, 138)
Charleston, South
95.2% +4.8% N/A <10 0% 0.140 (141)
Reticulitermes malleteif
Duke Forest, North
53.8% +46.2% –0.257 <10 0% 0.190 (138)
Reticulitermes virginicus
Raleigh, North
75.0% 25.0% –0.332 <10 0% 0.037 (101, 135)
Charleston, South
100% 0% N/A N/A 0% –0.04 (141)
Reticulitermes hesperus
Northern California
73.3% 26.7% –0.185 <10 0% 0.081 (23)
Reticulitermes grassei
France, population
0% N/A 100% 0.019 >100 0%h0.294 (26)
(Continued ) Biology of Subterranean Termites 387
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
Table 2 (Continued )
Simple families Extended families Mixed families
(N=no. colonies) Percent
relatedaPercent FICb
Inferred no.
neotenics Percent
FIT Reference(s)
France, population
26.7% ++ 73.3% –0.038 10–100 0%h0.306 (26)
France, population
43.7% +56.3% –0.113 <10 0%h0.210 (26)
Central Portugal
33.3% – 53.4%i–0.310 <10 13.3% –0.020 (97)
Coptotermes lacteus
Southern Australia
100% +0% N/A N/A 0% NR (127)
Coptotermes formosanus
New Orleans,
57.0% 43.0% –0.147 <10 0% 0.159 (53, 56, 140)
Charleston, South
48.0% +52.0% –0.058 10–100g0% 0.139 (140)
Rutherford County,
North Carolinae
75.0% +25.0% –0.127 <10 0% 0.239 (140)
Kyushu, Japane
85.0% +15.0% 0.012 >100 0% 0.161 (139)
Fukue, Japane
100% ++ 0% N/A N/A 0% 0.461 (139)
Oahu, Hawaiie
36.8% +63.2% –0.10 <10 0% 0.32 (54)
Province, China
0% N/A 100% –0.14 <10 0% 0.18 (54)
a–, coefficient of relatedness (r) not significantly different from zero; +,0<r<0.25; ++,r>0.25.
bStrongly negative FIC (<–0.14) suggests low numbers of reproductively active neotenics (fewer than 10), whereas values close to zero suggest many
neotenics (10 to 100).
cAllozyme markers used to infer breeding structure.
dEstimated by Thorne et al. (132).
eIntroduced population.
fOriginally reported as the Duke Forest population of R. hageni.
gLow power to distinguish extended from mixed families.
hAuthors refer to extended families as pleometrotic families.
iMay exhibit a degree of assortative mating in some colonies.
NR, not reported.
388 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
inbreeding in individuals relative to their
colony (FIC), a statistic that is especially sen-
sitive to the numbers of reproductives present
(17, 27, 29, 97, 132).
The FIC values for extended families from
a number of populations are given in Table 2
along with the inferred numbers of functional
neotenics. There was variation among pop-
ulations of the European species, R. gras-
sei, suggesting large numbers of neotenics in
some populations and low numbers in oth-
ers (Table 2). In North American Reticuliter-
mes species, extended families in most popu-
lations contained relatively few reproductives,
and these were likely the direct offspring of
the founding pair (17, 132). These conclusions
are strikingly similar to results from laboratory
colonies in which the reproductive composi-
tion was censused (79). Laboratory studies of
R. flavipes (42, 76) have shown that neoten-
ics may sometimes coexist alongside primary
reproductives. Husseneder et al. (51) found a
primary king together with 25 female neoten-
ics in the African subterranean termite Sche-
dorhinotermes lamanianus, demonstrating that
primary and neotenic reproductives of other
species do sometimes occur alongside each
other in the field.
A couple of populations are worth spe-
cial mention. First, colonies of R. flavipes in
France (previously called R. santonensis) differ
radically from those studied so far in the na-
tive range. Detailed studies of populations in
Paris and northwestern France (30) found only
highly inbred colonies headed by many neoten-
ics (Table 2). These invasive populations will
be discussed in more detail later. Second, an
older study of R. flavipes in central Tennessee
using allozymes (108) reported extremely high
levels of inbreeding (FIT =0.680), almost twice
as high as the next most inbred native popula-
tion (see Table 2). The reasons for the large dis-
crepancy between this population and the many
other populations studied are not known.
In introduced populations of C. formosanus,
the inferred numbers of reproductives in
extended family colonies vary considerably.
FIC:coefficient of
inbreeding in
individuals relative to
their colony
FIT:coefficient of
inbreeding in
individuals relative to
their population
Colonies in populations from New Orleans,
Louisiana; Charleston, South Carolina; and
Rutherford County, North Carolina, had lev-
els of inbreeding indicative of low numbers of
neotenics (<10) (2, 53, 140), whereas colonies
from Japan and Hawaii were more inbred, sug-
gesting higher numbers of reproductives (54,
139). Whether these differences are due to the
inherent genetic structure of introduced popu-
lations or are responses to local ecological con-
ditions is not known. Extensive studies of na-
tive populations of this species from mainland
China are needed to determine how the num-
ber of reproductives in extended family colonies
varies in natural environments and how these
numbers compare with introduced populations.
One sample of 12 colonies from a native popula-
tion in Guangdong Province consisted entirely
of extended families presumably headed by rel-
atively few neotenics (54). The inferred number
of neotenics in these colonies is consistent with
data from nest excavations in China (142), in
which the number of neotenics in colonies was
generally fewer than 20.
Within extended family colonies, genetic
substructuring can occur through a couple of
processes. First, the presence of spatially sepa-
rated groups of reproductives with little or no
interbreeding between them coupled with lim-
ited movement of workers from their natal nest
can lead to genetic differentiation within the
colony. In an expansive colony of C. formosanus,
Husseneder et al. (53) found evidence of sub-
structure among foragers feeding on monitor-
ing stations located 25 to 100 m apart. Similar
results were reported for a colony of the African
subterranean termite S. lamanianus (50). In a
large introduced colony of R. flavipes in France,
foragers occurring further apart were geneti-
cally more differentiated than those occurring
closer together (30).
Another process that can lead to differenti-
ation among foraging groups is kin-biased for-
aging. In S. lamanianus, groups of foragers col-
lected away from the nest were more closely
related than workers taken from the nest cen-
ter (62), which suggests that workers sorted Biology of Subterranean Termites 389
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
Mixed-family colony:
group of cohabiting
individuals produced
by multiple unrelated
themselves into kin groups while foraging. It
is not known whether genetic substructuring,
either through kin-biased sorting or as a re-
sult of spatially separated reproductive cen-
ters, is widespread in subterranean termites,
but it is likely to occur mainly in species
with expansive colonies. Studies of several
species, especially North American Reticuliter-
mes, show that colonies are often localized, so
opportunities for genetic substructuring within
colonies of these species are most likely limited
(27, 101, 141).
Geographic Variation
in Breeding Structure
Populations spanning much of the eastern
seaboard of the United States show strong cli-
nal variation in colony breeding structure in
R. flavipes, with a greater proportion of extended
family colonies and higher levels of inbreed-
ing in northern populations (137). Studies of
R. grassei in France and Portugal, although
more limited in scope, indicate a similar trend
in increasing levels of inbreeding from north
to south (Table 2) (26, 97). The apparent geo-
graphic variation in these species suggests that
colony breeding structure is responsive to local
ecological conditions, and that these conditions
vary in a gradual manner along latitudinal gradi-
ents. One of the big challenges in subterranean
termite biology will be to determine the ecolog-
ical factors that shape colony breeding struc-
ture, especially those factors that may select
against inbreeding. Studies in additional subter-
ranean termite species focusing on clinal varia-
tion in colony breeding structure similar to that
found in R. flavipes and R. grassei should prove
particularly fruitful.
Mixed-Family Colonies
and Colony Fusion
Among subterranean termites, mixed-family
colonies in the field have so far only been
demonstrated in R. flavipes (27, 29, 101, 138)
and R. grassei (97). Several mechanisms can
potentially lead to mixed families, but colony
fusion is the only mechanism that has been
documented in subterranean termites (27).
Pleometrotic association of multiple same-sex
reproductives is another means, but to date
this route has been found only in some termi-
tids (3, 43). Results of field (29) and laboratory
(37) studies indicate that the presence of multi-
ple unrelated groups of reproductives in fused
colonies of R. flavipes is generally rather short-
lived; over time reproduction in fused colonies
is usually restricted to individuals from just one
of the original source colonies.
The factors underlying colony fusion are not
clear. Matsuura & Nishida (87) proposed that
colonies with numerous nymphs preparing to
molt into alates would be more likely to accept
individuals from foreign colonies, but this hy-
pothesis has not been rigorously tested in the
field. In a study of mixed-family colonies in
North Carolina and South Carolina, DeHeer
& Vargo (29) showed that individuals origi-
nating from different families had identical or
nearly identical mtDNA haplotypes but were
unrelated at nuclear microsatellite loci. These
results suggest some maternally inherited fac-
tor underlying colony fusion, but the nature
of this factor is not known. Because mixed-
family colonies have low genetic relatedness,
and therefore lower inclusive fitness of colony
members, the factors influencing colony fusion,
including similarities in mtDNA haplotype, are
worthy of further study.
Colony Longevity, Breeding Structure,
and Effects of Inbreeding
The proportions of simple families in a pop-
ulation can provide insights into its age struc-
ture. Assuming that a population has reached a
stable age distribution, the presence of a high
proportion of simple family colonies, as we find
in most Reticulitermes spp. populations studied
to date, suggests that most colonies in these
populations do not survive past the death of
one of the primaries. The life span of pri-
mary reproductives in the field is not known
for any species, but in a laboratory study of
30 R. flavipes colonies, reproductives began to
390 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
die after 6 years but some were still alive af-
ter 11 years (78). Long-term demographic stud-
ies are needed to determine how long colonies
live with both primary reproductives present,
and how long they survive once neotenics are
Because relatively few colonies in many pop-
ulations of subterranean termites do not sur-
vive the death of the primary reproductives,
there may be a cost associated with reproduc-
tion by neotenics. The production of neotenics
appeared early in the evolution of the Isoptera
and is thought to confer many advantages (129).
Principal among these is that neotenic repro-
duction gives workers the option of differentiat-
ing into reproductives in their natal colony and
inheriting existing resources, thereby foregoing
the risks of embarking on mating flights (95,
116, 129). A major consequence of neotenic re-
production is elevated levels of inbreeding. The
possibility of inbreeding depression in subter-
ranean termites has received little attention to
Recent results from dampwood and subter-
ranean termites give somewhat mixed views re-
garding the possible importance of inbreeding
depression in termites. Sibling founding pairs
of the dampwood termite, Zootermopsis angusti-
collis, survived better than pairs in which males
and females were unrelated (112). Similarly,
sibling founding pairs of C. formosanus had
higher survivorship than pairs of unrelated indi-
viduals, but the survivors in the latter group had
higher growth rates (36). Other studies have
shown a cost to inbreeding in termites through
increased susceptibility to some diseases (19)
and reduced survivorship of colonies founded
by related primary reproductives in the field
(28). In addition, some studies report an effect
of inbreeding (77) or numbers of reproductives
(54) on worker size in subterranean termites,
although possible fitness consequences of these
differences are unknown. The costs and benefits
associated with neotenic reproduction should
be addressed in future research, including both
ecological factors related to breeding structure
and potential physiological and behavioral con-
sequences of inbreeding.
recapture (MRR):
method used to delimit
colony-foraging areas
and sometimes for
estimating colony
population size
Colony Reproduction by Budding
Although it has often been assumed that subter-
ranean termite colonies frequently reproduce
by budding (95, 116, 130, 132), in which a por-
tion of a colony splits off or becomes isolated
from the natal nest and functions as an indepen-
dent colony, results from a number of studies on
several species do not support this view. If com-
mon, budding should lead to high population
viscosity in which colonies located near each
other are genetically more similar than colonies
further apart. Yet, several fine-scale studies of
Reticulitermes species (17, 26, 27, 136, 138, 141)
and C. formosanus (53, 140) have failed to find
such a relationship. However, Husseneder et al.
(50) did find evidence for budding in a pop-
ulation of S. lamanianus, suggesting that this
mode of reproduction may occur in some sub-
terranean termite species.
Parthenogenetic Reproduction
Parthenogenetic reproduction occurs in the
laboratory in R. virginicus (48) and R. sper-
atus (86). In the latter species, the mecha-
nism of parthenogenetic reproduction has been
identified (86). However, to date there are
no clear cases of parthenogenetic colonies re-
ported from field populations of any species, so
the significance of this mode of reproduction
under natural conditions remains uncertain.
The application of the mark-release-recapture
(MRR) technique to connect spatially separated
groups of foragers to the same colony (69)
was an important advance in delimiting colony-
foraging areas and has been used extensively
over the past three decades (122, 130). The use
of molecular markers, such as highly variable
microsatellite markers, offers many advantages
over MRR for assigning workers to colonies, for
determining the limits of colony-foraging areas,
and for determining the numbers of colonies
in an area (101). Chief among the advantages Biology of Subterranean Termites 391
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
Table 3 Foraging ranges of Reticulitermes spp. and Coptotermes spp. as determined by genetic markers
Species Location (N) Linear foraging distance (m)aForaging area (m2) Reference(s)
Reticulitermes flavipes North Carolina (169) 1–26 1–174 (101)
North Carolina (122)b1–85 NR (135, 136, 138)
North Carolina (29) 1–12 1–96 (27)
South Carolina (18)b1NR (141)
Massachusetts (22) 1–76 1–800 (17)
France (26) 1–320 1–90,000 (30)
R. hageni North Carolina (15) 1–11 1–21 (27, 101)
North Carolina (3)b1 1 (138)
South Carolina (21)b1NR (141)
R. malleteicNorth Carolina (13)b1 1 (138)
R. virginicus North Carolina (8) 1–50 1–318 (27, 101)
North Carolina (4)b1–122 NR (135, 138)
South Carolina (4)b1–125 NR (141)
R. hesperusdCalifornia (30) 1–15 NR (23)
R. grassei France (71) 1–70 NR (26)
Portugal (15) 1–10 NR (97)
Coptotermes formosanus Louisiana (13)e40–175 83–1,634 (90, 91)
North Carolina, South
Carolina, Louisiana (115)b
1–144 NR (2, 53, 56, 140)
aColonies found in only one station or feeding site were assumed to have a foraging range of 1 m.
bStudy not specifically designed to map colony foraging areas.
cOriginally reported as the Duke Forest population of R. hageni.
dSpecies was not specified but occurs in area where R. hesperus is common.
eUsed both mark-release-recapture and genetic methods to delimit colony foraging areas.
N, number of colonies studied; NR, not reported.
of using genetic markers are (a) studies can be
done faster with less effort, (b) far fewer foragers
are required for determining colony identity,
and (c) studies can be conducted over a period
of years without losing the ability to identify
colonies. Thus, more colonies can be studied
over a larger area and over a period of months
or years, allowing for extensive long-term stud-
ies of colony dynamics and colony-level effects
of termiticide treatments.
Colony Foraging Area
Here, we summarize what has been learned
about the foraging ranges of Reticulitermes
and Coptotermes since 2001 using genetic
markers (Table 3). The picture has changed
significantly since the last reviews done more
than a decade ago, before the application of
molecular methods (122, 130). For example, it
now appears that small, localized colonies are
the norm for many Reticulitermes species. Con-
spicuous exceptions to small foraging areas in
Reticulitermes spp. are colonies of R. virginicus,
which frequently forage over 100 linear meters
(135, 138, 141), and introduced populations of
R. flavipes in France that can cover thousands
of square meters (30). Similarly, colonies of
C. formosanus in introduced areas are often
expansive, extending >100 linear meters
(90, 140).
It has been generally assumed that the
large worker populations and expansive forag-
ing ranges attained by colonies of some sub-
terranean termite species can only be achieved
by the reproductive output of multiple female
392 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
neotenic reproductives (42, 130). Although the
very large colonies of R. flavipes in France,
which are among the largest subterranean ter-
mite colonies known, are headed by numer-
ous neotenics (30), these are introduced pop-
ulations and do not appear to be representative
of natural populations. Studies of natural pop-
ulations of R. flavipes and R. virginicus show that
colonies headed by a single queen (simple fam-
ily) do not differ in the size of their foraging
areas from colonies headed by multiple queens
(extended families) (27, 101, 138, 141), suggest-
ing that colony family structure does not influ-
ence the size of the worker population. Similar
results reported for an introduced population
of C. formosanus suggest that the presence of
multiple queens in colonies does not necessar-
ily allow for larger colony size in this species ei-
ther (53). Support for the lack of larger colony
size in colonies headed by neotenics also comes
from a recent laboratory study by Long et al.
(78). There was no difference in colony size
(either all individuals or numbers of work-
ers) between laboratory-established colonies
containing their original primary reproductive
pairs and colonies headed by neotenics (78).
Population Densities
Data from molecular studies in which individual
colonies are identified are now accumulating,
showing that colony densities can be high in
some areas. A study of forests in central North
Carolina (27) found densities of up to 300 Reti-
culitermes spp. colonies per hectare, consisting
overwhelmingly of R. flavipes; these are among
the highest densities recorded for any termite
species in any ecosystem (73). Colony densities
can be high in urban environments as well. On
residential properties in North Carolina, Par-
man and Vargo (101) found an average popu-
lation density of 62 colonies per hectare, with
a maximum of 185 colonies per hectare, over
90% of which were R. flavipes.
Relative abundance is likely to vary with
habitat and geographic location. In an undis-
turbed site in Massachusetts, near the far north-
ern edge of the range of R. flavipes, Bulmer et al.
(17) found a much lower population density
than that found in North Carolina—only about
seven colonies per hectare. The lower colony
density in this northern population is associated
with a higher frequency of inbred colonies.
Colony density of C. formosanus in a park
in New Orleans was 1.5 colonies per hectare
(53, 90). This is similar to the 1.0 colonies per
hectare for this species reported for a park in
Charleston (140). The lower colony densities
of this species compared with Reticulitermes spp.
are consistent with the larger colonies it forms,
with foraging ranges often exceeding 100 linear
meters (90, 122, 140).
Intraspecific interactions among colonies
undoubtedly play an important role in deter-
mining colony density. Recent studies show
that colonies of R. flavipes and C. formosanus
in relatively undisturbed sites appear to form
territories that are remarkably stable over a pe-
riod of years (27, 90) with little or no infringe-
ment by neighboring colonies. Further evi-
dence supporting territorial interactions comes
from studies in which colonies were removed by
baiting. In areas of relatively high population
density, the territories of eliminated colonies
are quickly invaded by neighboring colonies in
both R. flavipes (135) and C. formosanus (56, 91).
The apparently weak intraspecific agonism
displayed by R. flavipes (18, 104) and by intro-
duced populations of C. formosanus (52, 89, 121)
suggests that some mechanism other than ag-
gressive behavior is responsible for intraspe-
cific territoriality, at least in some cases. This
is in marked contrast to many termite species
that show strong intraspecific agonism (131),
including the African subterranean termite
S. lamanianus (50).
Use of Genetic Markers for Applied
Studies in the Field
The use of molecular markers to identify large
numbers of individual colonies and track them
over time allows for more rigorous field evalu-
ations of insecticide treatments than was pre-
viously possible (35, 56, 135). By comparing
the genotypic profiles of colonies present before Biology of Subterranean Termites 393
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
and after treatment, we can determine whether
termites that reinfest treated areas or bait
stations are remnants of targeted colonies, in-
vading neighboring colonies, or previously un-
detected hidden colonies. For example, stud-
ies of C. formosanus found that foraging areas
of colonies eliminated by baiting with chitinase
inhibitors were often reinvaded, and that the
source of reinfesting termites was either known
neighboring colonies or hidden colonies (56,
91). Similar results were obtained in baiting
studies with Reticulitermes spp. (135). Although
reinfestation after treatment is common in ar-
eas with high colony density, reinfestation rates
decline with repeated treatment (56, 135), indi-
cating such treatments have a population-level
effect, at least on a small scale.
The use of genetic markers in applied studies
also allows us to compare the breeding structure
of colonies present before and after treatment
to determine whether family type or the de-
gree of inbreeding influences treatment success
(56). To date, studies have indicated that breed-
ing structure of colonies does not affect treat-
ment success, because all treated colonies of
both Reticulitermes and Coptotermes were elimi-
nated regardless of family type (56, 135). In one
study, new colonies appearing within treated
areas were primarily simple families, whereas
a disproportionate number of hidden C. for-
mosanus colonies taking over vacated foraging
areas were extended families (56), suggesting
that simple families and extended families dif-
fer in their response to vacated territories.
A number of termites have been introduced and
have become established in new locations, but
in only a few cases can these be considered truly
invasive in the sense that they have significant
ecological and economic impact in their intro-
duced ranges. Termites that have most often
been introduced and have become established
in new areas are drywood termites (Kalotermi-
tidae) and subterranean termites (Rhinotermi-
tidae) (38). Among the subterranean termites,
species of Coptotermes and Reticulitermes are the
most common and the most destructive. The
Formosan subterranean termite, C. formosanus,
is considered among the 100 worst invasive
species (40). Coptotermes gestroi has been intro-
duced into several places around the world (60).
R. flavipes is well established in Europe (11) and
South America (123).
The use of molecular markers can provide
powerful tools for identifying the source pop-
ulations of introduced species (83). DNA se-
quence data established that populations of
R. santonensis in France and South America were
introduced populations of R. flavipes (11, 123),
a native of eastern and central United States. In
addition, R. flavipes has been introduced into
areas of North America north of the native
range (34, 65). The precise locations of pop-
ulations within the United States serving as
the sources of introduced populations have not
been identified. Attempts have been made to
identify the source populations and routes of
introduction of invasive populations of C. for-
mosanus (12) and C. gestroi (60), but small sam-
ple sizes and low variation in the mitochondrial
genes used in these studies render conclusions
from this work tentative at best (94). Studies us-
ing highly variable markers, such as microsatel-
lites, should provide greater power in identify-
ing likely source populations (25, 105) and the
routes of introduction of invasive subterranean
A major area of inquiry in invasion biology
concerns the factors that make some species
successful invaders. The attributes of success-
ful ant invaders have received considerable at-
tention (47). Among the most prominent fea-
tures of many invasive ants is the breakdown of
colony boundaries resulting in large unicolo-
nial populations that become ecologically dom-
inant within introduced ranges. The behavioral
changes in introduced populations most likely
result from reduced genetic variation associated
with introduction events, resulting in a homog-
enization of the cues used by ants to distinguish
nestmates. This reduced ability to recognize
394 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
nestmates in turn leads to fusion of colonies into
large aggregations (133).
Do invasive subterranean termites share any
of the unicolonial characteristics of invasive
ants? The evidence to date shows a mixed pic-
ture. French populations of R. flavipes exhibit
reduced genetic variation compared with native
populations at both microsatellite loci (30, 136,
141) and mitochondrial genes (11). The popu-
lations in France form exclusively large, highly
polygamous extended family colonies (30), and
this appears to be true of populations intro-
duced into North America as well (34, 41). This
is in contrast to colonies in the native range
that tend to be primarily simple families with
localized foraging areas. Thus, there are some
intriguing parallels between these introduced
populations of R. flavipes and those of some in-
vasive ants. It is of interest to know whether
other introduced populations of R. flavipes, such
as those in Chile (123), also form expansive,
highly polygamous colonies.
Studies of introduced populations of
C. formosanus also show reduced genetic
variation compared with native populations
at microsatellite loci (53, 54, 139, 140). De-
spite little or no agonistic behavior among
colonies in the introduced range (52, 89,
121), invasive populations of this species do
not form large, unicolonial societies. Rather,
they form genetically distinct colonies that
are either simple families or secondarily
polygamous (extended) families derived from
simple families. In contrast, the dozen colonies
characterized to date from the native range
were all polygamous (54). Thus, although the
data are still limited, it appears that introduced
populations of C. formosanus are not charac-
terized by higher numbers of reproductives
than native populations. This may not be
true of all Coptotermes spp., however. Three
species of mound-building Coptotermes native
to Australia, C. lacteus,C. acinaciformis, and
C. frenchi, all form almost exclusively simple
families in Australia but colonies in New
Zealand, where they have been introduced,
contain many neotenics (71).
There is growing interest among scientists in
the biology of subterranean termites. Molec-
ular techniques have begun to make signifi-
cant contributions to nearly all areas of sub-
terranean biology. Progress in some areas, such
as systematics and taxonomy, the molecular ba-
sis of caste differentiation, and colony breeding
structure, will largely depend on continued ap-
plication of molecular methods. In other areas,
such as foraging ecology, population dynam-
ics, and community ecology, molecular tech-
niques can provide important information on
colony identity, allowing for much more de-
tailed and comprehensive studies than would
otherwise be possible. Recent molecular eco-
logical studies are already changing long-held
views about the breeding structure and dynam-
ics of subterranean termite colonies. In addi-
tion, the use of molecular markers is playing
an increasingly important role in applied stud-
ies to assess colony-level effects of termiticide
treatments in the field.
Although molecular techniques will grow
increasingly important in studies of subter-
ranean termite biology and management, the
results generated by these methods will have
greatest utility as part of a multidisciplinary
approach. For example, a more complete
understanding of the mechanisms regulating
caste differentiation will involve integrating
molecular tools with physiological methods,
chemical ecological approaches, and behav-
ioral studies. Molecular genetic markers have
proven invaluable for elucidating colony
breeding structure and how it varies within and
among species. But understanding the factors
underlying this variation will require ecological
studies of the biotic and abiotic factors that
shape colony breeding structure. Studies of
colony-colony dynamics and relative species
abundance will need to combine molecular
markers for colony identifications with ecolog-
ical, behavioral, and demographic approaches
to understand the factors determining popu-
lation dynamics and species richness. Thus, in
our view, the future of subterranean termite Biology of Subterranean Termites 395
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
biology is one of an interdisciplinary approach,
with molecular techniques occupying a central
position. The development of additional
tools, especially in genomics and proteomics,
will lead to many new possibilities. We can
look forward to rapid advances in all areas of
subterranean termite biology in the coming
1. Coptotermes and Reticulitermes are two of the most species-rich genera of lower termites,
but they are in need of careful taxonomic revision using both morphological and molec-
ular methods.
2. Recent studies have provided important insights into the molecular processes under-
lying caste differentiation, especially in soldier development in Reticulitermes, in which
hexamerins play a key role in modulating the activity of JH.
3 Although it is well known that termites often inbreed, recent evidence suggests that
inbreeding depression may occur in some subterranean termite species with possible
consequences for mate choice and colony breeding structure.
4. Dispersal and sex-biased alate production can promote outbreeding in some subterranean
termite species, but to date there is no evidence for kin discrimination during partner
5. Molecular markers provide a powerful tool for inferring the breeding structure of sub-
terranean termite colonies. There is considerable variation within and among species in
the relative frequencies of simple and extended family colonies, but many populations
are composed of mainly simple families. Mixed-family colonies, which can form through
colony fusion, appear to be rare.
6. Colonies of most species of Reticulitermes studied to date have fairly limited foraging
ranges, usually less than 10 linear meters, and colony densities can be quite high, reach-
ing up to 300 per hectare in some populations of R. flavipes. Colonies of introduced
populations of R. flavipes are a notable exception, with foraging ranges up to 100 m or
more, rivaling the expansive colonies often formed by C. formosanus.
7. Colonies of Reticulitermes and Coptotermes appear to be territorial with well-established
boundaries, but the mechanisms by which these boundaries are established and main-
tained have yet to be identified.
8. Species of Reticulitermes and Coptotermes are among the most important and destructive
invasive termite species. Current studies are using genetic markers to identify source
populations and to investigate the factors underlying their invasion success.
The authors are not aware of any biases that might be perceived as affecting the objectivity of this
We thank Paul Labadie and Dawn Simms for assistance in preparing the manuscript. Warren
Booth provided helpful comments. This work was partially supported by grants from the USDA
396 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
National Research Initiative Competitive Grants Program (2004-35302-14880) to Coby Schal and
ELV; by the W.M. Keck Center for Behavioral Biology at North Carolina State University; by
USDA-ARS Specific Cooperative Agreements to CH; by grants provided by the State of Louisiana
to CH; by grants from USDA T-STAR to J. Kenneth Grace, CH, and ELV; and by a grant from
the National Geographic Society to ELV and CH.
1. Abe T, Bignell DE, Higashi M, eds. 2000. Termites: Evolution, Sociality, Symbioses, Ecology. Dordrecht,
The Netherlands: Kluwer Acad.
2. Aluko GA, Husseneder C. 2007. Colony dynamics of the Formosan subterranean termite in a frequently
disturbed urban landscape. J. Econ. Entomol. 100:1037–46
3. Atkinson L, Adams ES. 1997. The origins and relatedness of multiple reproductives in colonies of the
termite Nasutitermes corniger.Proc. R. Soc. London Sci. Ser. B 264:1131–36
4. Austin JW, Bagn `
eres AG, Szalanski AL, Scheffrahn RH, Heintschel BP, et al. 2007. Reticulitermes malletei
(Isoptera: Rhinotermitidae): a valid Nearctic subterranean termite from eastern North America. Zootaxa
5. Austin JW, Szalanski AL, Cabrera BJ. 2004. Phylogenetic analysis of the subterranean termite family
Rhinotermitidae (Isoptera) by using the mitochondrial cytochrome oxidase II gene. Ann. Entomol. Soc.
Am. 97:548–55
6. Austin JW, Szalanski AL, Ghayourfar R, Kence A, Gold RE. 2006. Phylogeny and genetic variation of
Reticulitermes (Isoptera: Rhinotermitidae) from the Eastern Mediterranean and Middle East. Sociology
7. Austin JW, Szalanski AL, Gold RE, Foster BT. 2004. Genetic variation and geographic distribution of
the subterranean termite genus Reticulitermes in Texas. Southwest. Entomol. 29:1–11
8. Austin JW, Szalanski AL, Kard BM. 2004. Distribution and genetic variation of Reticulitermes (Isoptera:
Rhinotermitidae) in Oklahoma. Fla. Entomol. 87:152–58
9. Austin JW, Szalanski AL, Messenger MT. 2004. Mitochondrial DNA variation and distribution of the
subterranean termite genus Reticulitermes (Isoptera: Rhinotermitidae) in Arkansas and Louisiana. Fla.
Entomol. 87:473–80
10. Austin JW, Szalanski AL, Messenger MT, McKern JA, Gold RE. 2006. Genetic variation and phyloge-
netics of Reticulitermes (Isoptera: Rhinotermitidae) from the American Great Plains. Sociobiology 48:1–19
11. Austin JW, Szalanski AL, Scheffrahn RH, Messenger MT, Dronnet S, Bagn`
eres A-G. 2005. Genetic
evidence for the synonymy of two Reticulitermes species: Reticulitermes flavipes and Reticulitermes santonensis.
Ann. Entomol. Soc. Am. 98:395–401
12. Austin JW, Szalanski AL, Scheffrahn RH, Messenger MT, McKern JA, Gold RE. 2006. Genetic ev-
idence for two introductions of the Formosan subterranean termite, Coptotermes formosanus (Isoptera:
Rhinotermitidae), to the United States. Fla. Entomol. 89:183–93
13. Austin JW, Szalanski AL, Uva P, Bagn`
eres A-G, Kence A. 2002. A comparative genetic analysis of the
subterranean termite genus Reticulitermes (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Am. 95:753–60
14. Avise JC. 2000. Phylogeography: The History and Formation of Species. Cambridge, MA: Harvard Univ.
15. Bignell DE, Eggleton P. 2000. Termites in ecosystems. See Ref. 1, pp. 363–87
16. Breznak JA. 2000. Ecology of prokaryotic microbes in the guts of wood- and litter-feeding termites. See
Ref. 1, pp. 209–31
17. Bulmer MS, Adams ES, Traniello JFA. 2001. Variation in colony structure in the subterranean termite
Reticulitermes flavipes.Behav. Ecol. Sociobiol. 49:236–43
18. Bulmer MS, Traniello JFA. 2002. Lack of aggression and spatial association of colony members in
Reticulitermes flavipes.J. Insect. Behav. 15:121–26
19. Calleri DV II, Reid EM, Rosengaus RB, VargoEL, Traniello JFA. 2007. Inbreeding and disease resistance
in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis.
Proc. R. Soc. London Sci. Ser. B 273:2633–40 Biology of Subterranean Termites 397
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
20. Cl´
ement J-L. 1981. Enzymatic polymorphism in the European populations of various Reticulitermes
species (Isoptera). In Biosystematics of Social Insects, ed. PE Howse, J-L Cl´
ement, pp. 49–62. London/New
York: Academic
21. Cl´
ement J-L. 1986. Open and closed societies in Reticulitermes termites (Isoptera, Rhinotermitidae):
geographic and seasonal variations. Sociobiology 11:311–23
22. Cl´
ement J-L, Bagn`
eres A-G, Uva P, Wilfert L, Quintana A, et al. 2001. Biosystematics of Reticulitermes
termites in Europe: morphological, chemical and molecular data. Insectes Soc. 48:202–15
23. Copren KA. 2004. Genetic and social structure of the western subterranean termite, Reticulitermes hesperus
(Isoptera: Rhinotermitidae). PhD thesis. Univ. Calif., Davis. 98 pp.
24. Copren KA, Nelson LJ, Vargo EL, Haverty MI. 2005. Phylogenetic analyses of mtDNA sequences
corroborate taxonomic designations based on cuticular hydrocarbons in subterranean termites. Mol.
Phylogenet. Evol. 35:689–700
25. Cornuet J-M, Piry S, Luikart G, Estoup A, Solignac M. 1999. New methods employing multilocus
genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000
26. DeHeer CJ, Kutnik M, Vargo EL, Bagn`
eres A-G. 2005. The breeding system and population structure
of the termite Reticulitermes grassei in southern France. Heredity 95:408–15
27. Documented colony
fusion of subterranean
termites in the field.
27. DeHeer CJ, Vargo EL. 2004. Colony genetic organization and colony fusion in the termite
Reticulitermes flavipes as revealed by foraging patterns over time and space. Mol. Ecol. 13:431–41
28. DeHeer CJ, Vargo EL. 2006. An indirect test of inbreeding depression in the termites Reticulitermes
flavipes and Reticulitermes virginicus.Behav. Ecol. Sociobiol. 59:753–61
29. DeHeer CJ, Vargo EL. 2008. Strong mitochondrial DNA similarity but low relatedness at microsatellite
loci among families within fused colonies of the termite Reticulitermes flavipes.Insectes Soc. 55:190–99
30. Dronnet S, Chapuisat M, Vargo EL, Louhou C, Bagn`
eres A-G. 2005. Genetic analysis of the breeding
system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Mol.
Ecol. 14:1311–20
31. Eggleton P. 1999. Termite species description rates and the state of termite taxonomy. Insectes Soc. 46:1–5
32. Eggleton P. 2000. Global patterns of termite diversity. See Ref. 1, pp. 25–51
33. Elliott KL, Stay B. 2008. Changes in juvenile hormone synthesis in the termite Reticulitermes flavipes
during development of soldiers and neotenic reproductives from groups of isolated workers. J. Insect
Physiol. 54:492–500
34. Esenther GR. 1969. Termites in Wisconsin. Ann. Entomol. Soc. Am. 62:1274–84
35. Evans TE, Lenz M, Gleeson PV. 1999. Estimating population size and forager movement in a tropical
subterranean termite (Isoptera: Rhinotermitidae). Environ. Entomol. 28:823–30
36. Fei HX, Henderson G. 2003. Comparative study of incipient colony development in the Formosan
subterranean termite, Coptotermes formosanus Shiraki (Isoptera, Rhinotermitidae). Insectes Soc. 50:226–33
37. Fisher ML, Gold RE, Vargo EL, Cognato AI. 2004. Behavioral and genetic analysis of colony fusion in
Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 44:565–76
38. Gay FJ. 1969. Species introduced by man. In Biology of Termites, ed. K Krishna, FM Weesner, 1:459–94.
New York: Academic
39. Gentry JB, Whitford WG. 1982. The relationship between wood litter infall and relative abundance and
feeding activity of subterranean termites Reticulitermes spp. in three southeastern coastal plain habitats.
Oecologia 54:63–67
40. Global Invasive Species Database. 2005. Coptotermes formosanus.
41. Grace JK. 1996. Temporal and spatial variation in caste proportions in a northern Reticulitermes flavipes
colony (Isoptera: Rhinotermitidae). Sociobiology 28:225–31
42. Grube S, Forschler BT. 2004. Census of monogyne and polygyne laboratory colonies illuminates dy-
namics of population growth in Reticulitermes flavipes (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Am.
43. Hacker M, Kaib M, Bagine RKM, Epplen JT, Brandl R. 2005. Unrelated queens coexist in colonies of
the termite Macrotermes michaelseni.Mol. Ecol. 14:1527–32
44. Haverty MI, Nelson LJ, Forschler BT. 1999. New cuticular hydrocarbon phenotypes of Reticulitermes
(Isoptera: Rhinotermitidae) from the United States. Sociobiology 34:1–21
398 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
45. First report of
genetic caste
differentiation in
45. Hayashi Y, Lo N, Miyata H, Kitade O. 2007. Sex-linked genetic influence on caste determination
in a termite. Science 318:985–87
46. Henderson G. 1998. Primer pheromones and possible soldier caste influence on the evolution of sociality
in lower termites. In Pheromone Communication in Social Insects: Ants, Wasps, Bees, and Termites, ed. RK
Vander Meer, MD Breed, KE Espelie, ML Winston, pp. 314–30. Boulder, CO: Westview
47. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ. 2002. The causes and consequences of ant
invasions. Annu. Rev. Ecol. Syst. 33:181–233
48. Howard RW, Mallett EJ, Haverty MI, Smythe RV. 1981. Laboratory evaluation of within-species,
between-species, and parthenogenetic reproduction in Reticulitermes flavipes and Reticulitermes virginicus.
Psyche 88:75–87
49. Hunt JH, Kensinger BJ, Kossuth JA, Henshaw MT, Norberg K, et al. 2007. A diapause pathway
underlies the gyne phenotype in Polistes wasps, revealing an evolutionary route to caste-containing insect
societies. Proc. Natl. Acad. Sci. USA 104:14020–25
50. Husseneder C, Brandl R, Epplen C, Epplen JT, Kaib M. 1998. Variation between and within colonies
in the termite: morphology, genomic DNA, and behaviour. Mol. Ecol. 7:983–90
51. Husseneder C, Brandl R, Epplen C, Epplen JT, Kaib M. 1999. Within-colony relatedness in a termite
species: genetic roads to eusociality? Behaviour 136:1045–63
52. Husseneder C, Grace JK. 2001. Evaluation of DNA fingerprinting, aggression tests and morphometry
as tools for colony delineation of the Formosan subterranean termite. J. Insect Behav. 14:173–86
53. Husseneder C, Messenger MT, Su N-Y, Grace JK, Vargo EL. 2005. Colony social organization and
population genetic structure of an introduced population of Formosan subterranean termite from New
Orleans, Louisiana. J. Econ. Entomol. 98:1421–34
54. Husseneder C, Powell JE, Grace JK, Matsuura K, Vargo EL. 2008. Worker size in the Formosan sub-
terranean termite in relation to colony breeding structure as inferred from molecular markers. Environ.
Entomol. 37:400–8
55. Husseneder C, Simms DM. 2008. Size and heterozygosity influence partner selection in the Formosan
subterranean termite. Behav. Ecol. 19:764–73
56. Husseneder C, Simms DM, Riegel C. 2007. Evaluation of treatment success and patterns of reinfestation
of the Formosan subterranean termite (Isoptera: Rhinotermitidae). J. Econ. Entomol. 100:1370–80
57. Husseneder C, Simms DM, Ring DR. 2006. Genetic diversity and genotypic differentiation between
the sexes in swarm aggregations decrease inbreeding in the Formosan subterranean termite. Insect. Soc.
58. Husseneder C, Vargo EL, Grace JK. 2003. Molecular genetic methods: new approaches to termite
biology. In Wood Deterioration and Preservation: Advances in Our Changing World, ed. B Goodell, TP
Schultz, DD Nicholas, ACS Symp. Ser. 845:358–70. Washington, DC: Am. Chem. Soc.
59. Inward DJG, Vogler AP, Eggleton P. 2007. A comprehensive phylogenetic analysis of termites (Isoptera)
illuminates key aspects of their evolutionary biology. Mol. Phylogenet. Evol. 44:953–67
60. Jenkins TM, Jones SC, Lee C-Y, Forschler BT, Chen Z, et al. 2007. Phylogeography illuminates maternal
origins of exotic Coptotermes gestroi (Isoptera: Rhinotermitidae). Mol. Phylogenet. Evol. 42:612–21
61. Jones SC, La Fage JP, Howard RW. 1988. Isopteran sex ratios: phylogenetic trends. Sociobiology 14:89–
62. Kaib M, Husseneder C, Epplen C, Epplen JT, Brandl R. 1996. Kin-biased foraging in a termite. Proc.
R. Soc. London Sci. Ser. B 263:1527–32
63. Kambhampati S, Eggleton P. 2000. Taxonomy and phylogeny of termites. See Ref. 1, pp. 1–23
64. Keller LF, Waller DM. 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17:230–41
65. Kirby CS. 1965. The distribution of termites in Ontario after 25 years. Can. Entomol. 97:310–14
66. Kirton LG, Brown VK. 2003. The taxonomic status of pest species of Coptotermes in Southeast Asia:
resolving the paradox in the pest status of the termites, Coptotermes gestroi,C. havilandi and C. travians
(Isoptera: Rhinotermitidae). Sociobiology 42:43–63
67. Kitade O, Hayashi Y, Kikuchi Y, Kawarasaki S. 2004. Distribution and composition of colony founding
associations of a subterranean termite, Reticulitermes kanmonensis.Entomol. Sci. 7:1–8
68. Kutnik M, Uva P, Brinkworth L, Bagn`
eres AG. 2004. Phylogeography of two European Reticulitermes
(Isoptera) species: the Iberian refugium. Mol. Ecol. 13:3099–113 Biology of Subterranean Termites 399
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
69. Lai PY. 1977. Biology and ecology of the Formosan subterranean termite, Coptotermes formosanus, and its
susceptibility to the entomogenous fungi, Beauvaria bassiana and Metarrhizium anisopliae. PhD thesis. Univ.
Hawaii, Honolulu. 140 pp.
70. Good review of life
cycle and caste
developmental pathways
in Reticulitermes spp.
70. Lain´
e LV, Wright DJ. 2003. The life cycle of Reticulitermes spp. (Isoptera: Rhinotermitidae):
What do we know? Bull. Entomol. Res. 93:267–78
71. Lenz M, Barrett RA. 1982. Neotenic formation in field colonies of Coptotermes lacteus (Froggatt) in
Australia, with comments on the roles of neotenics in the genus Coptotermes (Isoptera, Rhinotermitidae).
Sociobiology 7:47–59
72. Lenz M, Runko S. 1993. Long-term impact of orphaning on field colonies of Coptotermes lacteus (Froggatt)
(Isoptera: Rhinotermitidae). Insectes Soc. 40:439–56
73. Lepage M, Darlington JPEC. 2000. Population dynamics of termites. See Ref. 1, pp. 333–61
74. Lo N, Eldridge RH, Lenz M. 2006. Phylogeny of Australian Coptotermes (Isoptera: Rhinotermitidae)
species inferred from mitochondrial COII sequences. Bull. Entomol. Res. 96:433–37
75. Lo N, Kitade O, Constantino R, Matsumoto T. 2004. Molecular phylogeny of the Rhinotermitidae.
Insectes Soc. 51:365–71
76. Long CE, Thorne BL. 2006. Resource fidelity, brood distribution and foraging dynamics in complete
laboratory colonies of Reticulitermes flavipes (Isoptera Rhinotermitidae). Ethol. Ecol. Evol. 18:113–25
77. Long CE, Thorne BL, Breisch NL. 2003. Termite colony ontogeny: a long-term assessment of repro-
ductive lifespan, caste ratios and colony size in Reticulitermes flavipes (Isoptera: Rhinotermitidae). Bull.
Entomol. Res. 93:439–45
78. Long CE, Thorne BL, Breisch NL. 2007. Termite colony ontogeny: supplemental data in the long-term
assessment of reproductive lifespan, female neotenic production and colony size in Reticulitermes flavipes
(Isoptera: Rhinotermitidae). Bull. Entomol. Res. 97:321–25
79. Long CE, Vargo EL, Thorne BL, Juba TR. 2006. Genetic analysis of breeding structure in laboratory-
reared colonies of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Fla. Entomol. 89:521–23
80. Luchetti A, Marini M, Mantovani B. 2005. Mitochondrial evolutionary rate and speciation in termites:
data on European Reticulitermes taxa (Isoptera, Rhinotermitidae). Insectes Soc. 52:218–21
81. Luchetti A, Marini M, Mantovani B. 2007. Filling the European gap: biosystematics of the eusocial system
Reticulitermes (Isoptera, Rhinotermitidae) in the Balkanic Peninsula and Aegean area. Mol. Phylogenet.
Evol. 45:377–83
82. Luchetti A, Trenta M, Mantovani B, Marini M. 2004. Taxonomy and phylogeny of north Mediterranean
Reticulitermes termites (Isoptera, Rhinotermitidae): a new insight. Insectes Soc. 51:117–22
83. Manel S, Gaggiotti OE, Waples RS. 2005. Assignment methods: matching biological questions with
appropriate techniques. Trends Ecol. Evol. 20:136–42
84. Mao L, Henderson G, Liu Y, Laine RA. 2005. Formosan subterranean termite (Isoptera: Rhinotermi-
tidae) soldiers regulate juvenile hormone levels and caste differentiation in workers. Ann. Entomol. Soc.
Am. 98:340–45
85. Marini M, Mantovani B. 2002. Molecular relationships among European samples of Reticulitermes
(Isoptera, Rhinotermitidae). Mol. Phylogenet. Evol. 22:454–59
86. Matsuura K, Fujimoto M, Goka K. 2004. Sexual and asexual colony foundation and the mechanism of
facultative parthenogenesis in the termite Reticulitermes speratus (Isoptera, Rhinotermitidae). Insectes Soc.
87. Matsuura K, Nishida T. 2001. Colony fusion in a termite: What makes the society “open”? Insectes Soc.
88. Matsuura K, Nishida T. 2001. Comparison of colony foundation success between sexual pairs and female
asexual units in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Popul. Ecol. 43:119–24
89. Messenger MT, Su N-Y. 2005. Agonistic behavior between colonies of the Formosan subterranean
termite (Isoptera: Rhinotermitidae) from Louis Armstrong Park, New Orleans, Louisiana. Sociobiology
90. Messenger MT, Su N-Y. 2005. Colony characteristics and seasonal activity of the Formosan subterranean
termite (Isoptera: Rhinotermitidae) in Louis Armstrong Park, New Orleans, Louisiana. J. Entomol. Sci.
400 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
91. Messenger MT, Su N-Y, Husseneder C, Grace JK. 2005. Elimination and reinvasion studies with Cop-
totermes formosanus (Isoptera: Rhinotermitidae) in Louisiana. J. Econ. Entomol. 98:916–29
92. Messenger MT, Su N-Y, Scheffrahn RH. 2002. Current distribution of the Formosan subterranean
termite and other termite species (Isoptera: Rhinotermitidae, Kalotermitidae) in Louisiana. Fla. Entomol.
93. Miyata H, Furuichi H, Kitade O. 2004. Patterns of neotenic differentiation in a subterranean termite,
Reticulitermes speratus (Isoptera: Rhinotermitidae). Entomol. Sci. 7:309–14
94. Muirhead JR, Gray DK, Kelly DW, Ellis SM, Heath DD, Macisaac HJ. 2008. Identifying the source of
species invasions: sampling intensity vs genetic diversity. Mol. Ecol. 17:1020–35
95. Myles TG. 1999. Review of secondary reproduction in termites (Insecta: Isoptera) with comments on
its role in termite ecology and social evolution. Sociobiology 33:1–87
96. Nijhout HF. 1994. Insect Hormones. Princeton, NJ: Princeton Univ. Press
97. Nobre T, Nunes L, Bignell DE. 2008. Colony interactions in Reticulitermes grassei population assessed
by molecular genetic methods. Insectes Soc. 55:66–73
98. Nutting WL. 1969. Flight and colony foundation. In Biology of Termites, ed. K Krishna, FM Weesner,
1:233–82. New York: Academic
99. Park YI, Bland JM, Raina AK. 2004. Factors affecting postflight behavior in primary reproductives of
the Formosan subterranean termite, Coptotermes formosanus (Isoptera: Rhinotermitidae). J. Insect Physiol.
100. Park YI, Raina AK. 2004. Juvenile hormone III titers and regulation of soldier caste in Coptotermes
formosanus (Isoptera: Rhinotermitidae). J. Insect Physiol. 50:561–66
101. Parman V, VargoEL. 2008. Population density, species abundance and breeding structure of subterranean
termite colonies in and around infested houses in central North Carolina. J. Econ. Entomol. 101:1349–59
102. Pawson BM, Gold RE. 1996. Caste differentiation and reproductive dynamics of three subterranean
termites in the genus Reticulitermes (Isoptera: Rhinotermitidae). Sociobiology 28:241–51
103. Pichon A, Kutnik M, Leniaud L, Darrouzet E, Chaline N, et al. 2007. Development of experimentally
orphaned termite worker colonies of two Reticulitermes species (Isoptera: Rhinotermitidae). Sociobiology
104. Polizzi JM, Forschler BT. 1999. Factors that affect aggression among the worker caste of Reticulitermes
spp. subterranean termites (Isoptera: Rhinotermitidae). J. Insect. Behav. 12:133–46
105. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype
data. Genetics 155:945–59
106. Raina A, Osbrink N, Park YI. 2004. Nymphs of the Formosan subterranean termite (Isoptera: Rhinoter-
mitidae): aspects of formation and transformation. Ann. Entomol. Soc. Am. 97:757–64
107. Raina A, Park YI, Florane C. 2003. Behavior and reproductive biology of the primary reproductives of
the Formosan subterranean termite (Isoptera: Rhinotermitidae). Sociobiology 41:37–48
108. Reilly LM. 1987. Measurements of inbreeding and average relatedness in a termite population. Am. Nat.
109. Roisin Y. 2000. Diversity and evolution of caste patterns. See Ref. 1, pp. 95–119
110. Roisin Y, Lenz M. 1999. Caste developmental pathways in colonies of Coptotermes lacteus (Froggat)
headed by primary reproductives (Isoptera, Rhinotermitidae). Insectes Soc. 46:273–80
111. Roisin Y, Lenz M. 2002. Origin of male-biased sex allocation in orphaned colonies of the termite,
Coptotermes lacteus.Behav. Ecol. Sociobiol. 51:472–79
112. Rosengaus RB, Traniello JFA. 1993. Disease risk as a cost of outbreeding in the termite Zootermopsis
angusticollis.Proc. Natl. Acad. Sci. USA 90:6641–45
113. Scharf ME, Ratliff CR, Hoteling JT, Pittendrigh BR, Bennett GW. 2003. Caste differentiation
responses of two sympatric Reticulitermes termite species to juvenile hormone homologs and synthetic
juvenoids in two laboratory assays. Insectes Soc. 50:346–54
114. Scharf ME, Wu-Scharf D, Pittendrigh BR, Bennett GW. 2003. Caste- and development-associated gene
expression in a lower termite. Genome Biol. 4:R62
115. Scharf ME, Wu-Scharf D, Zhou X, Pittendrigh BR, Bennett GW. 2005. Gene expression profiles among
immature and adult reproductive castes of the termite Reticulitermes flavipes.Insect Mol. Biol. 14:31–44 Biology of Subterranean Termites 401
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
116. Shellman-Reeve JS. 1997. The spectrum of eusociality in termites. In Social Behavior in Insects and Arach-
nids, ed. JC Choe, BJ Crespi, pp. 52–93. Cambridge, UK: Cambridge Univ. Press
117. Shellman-Reeve JS. 1999. Courting strategies and conflicts in a monogamous, biparental termite. Proc.
R. Soc. London Sci. Ser. B 266:137–44
118. Snyder TE. 1954. Order Isoptera. The Termites of the United States and Canada. New York: Natl. Pest
Control Assoc.
119. Su N-Y. 2002. Novel technologies for subterranean termite control. Sociobiology 40:95–101
120. Su N-Y. 2003. Overview of the global distribution and control of the Formosan subterranean termite.
Sociobiology 41:7–16
121. Su N-Y, Haverty MI. 1991. Agonistic behavior among colonies of the Formosan subterranean termite,
Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae), from Florida and Hawaii: lack of correlation
with cuticular hydrocarbon composition. J. Insect Behav. 4:115–28
122. Su N-Y, Tamashiro M. 1987. An overview of the Formosan subterranean termite (Isoptera: Rhinotermi-
tidae) in the world. In Biology and Control of the Formosan Subterranean Termite. Research Extension Series
083, ed. M Tamashiro, N-Y Su, pp. 3–14. Honolulu: Univ. Hawaii
123. Su N-Y, Ye W, Ripa R, Scheffrahn RH, Giblin-Davis RM. 2006. Identification of Chilean Reticuliter-
mes (Isoptera: Rhinotermitidae) inferred from three mitochondrial gene DNA sequences and soldier
morphology. Ann. Entomol. Soc. Am. 99:352–63
124. Szalanski AL, Austin JW, McKern J, Messenger MT. 2006. Genetic evidence for a new subterranean
termite species (Isoptera: Rhinotermitidae) from western United States and Canada. Fla. Entomol. 89:299–
125. Szalanski AL, Austin JW, Owens CB. 2003. Identification of Reticulitermes spp. (Isoptera: Reticuliter-
matidae [sic]) from south central United States by PCR-RFLP. J. Econ. Entomol. 96:1514–19
126. Szalanski AL, Austin JW, Scheffrahn RH, Messenger MT. 2004. Molecular diagnostics of the Formosan
subterranean termite (Isoptera: Rhinotermitidae). Fla. Entomol. 87:145–51
127. Thompson GJ, Lenz M, Crozier RH, Crespi BJ. 2007. Molecular-genetic analyses of dispersal and
breeding behaviour in the Australian termite Coptotermes lacteus: evidence for nonrandom mating in a
swarm-dispersal mating system. Aust. J. Zool. 55:219–27
128. Thorne BL. 1996. Termite terminology. Sociobiology 28:253–61
129. Thorne BL. 1997. Evolution of eusociality in termites. Annu. Rev. Ecol. Syst. 28:27–54
130. Excellent review of
general biology of
Reticulitermes spp.
130. Thorne BL. 1998. Biology of subterranean termites of the genus Reticulitermes.InNPCA Research
Report on Subterranean Termites, pp. 1–30. Dunn Loring, VA: Natl. Pest Control Assoc.
131. Thorne BL, Haverty MI. 1991. A review of intracolony, intraspecific, and interspecific agonism in
termites. Sociobiology 19:115–45
132. Presents
quantitative predictions
for coefficients of
inbreeding and
relatedness for possible
breeding systems in
subterranean termites.
132. Thorne BL, Traniello JFA, Adams ES, Bulmer M. 1999. Reproductive dynamics and colony struc-
ture of subterranean termites of the genus Reticulitermes (Isoptera Rhinotermitidae): a review of
the evidence from behavioral, ecological and genetic studies. Ethol. Ecol. Evol. 11:149–69
133. Tsutsui ND, Suarez AV, Grosberg RK. 2003. Genetic diversity, asymmetrical aggression, and recognition
in a widespread invasive species. Proc. Natl. Acad. Sci. USA 100:1078–83
134. Uva P, Cl´
ement JL, Austin JW, Aubert J, Zaffagnini V, et al. 2004. Origin of a new Reticulitermes termite
(Isoptera, Rhinotermitidae) inferred from mitochondrial and nuclear DNA data. Mol. Phylogenet. Evol.
135. Vargo EL. 2003. Genetic structure of Reticulitermes flavipes and R. virginicus (Isoptera: Rhinotermitidae)
colonies in an urban habitat and tracking of colonies following treatment with hexaflumuron bait. Environ.
Entomol. 32:1271–82
136. Vargo EL. 2003. Hierarchical analysis of colony and population genetic structure in the eastern subter-
ranean termite, Reticulitermes flavipes, using two classes of molecular markers. Evolution 57:2805–18
137. Vargo EL. 2006. Genetic analysis of breeding systems and population structure in species of Reticulitermes from
the eastern U.S. Presented at XV Congr. Int. Union Study Soc. Insects. Washington, DC
138. Vargo EL, Carlson JC. 2006. Comparative study of breeding systems of sympatric subterranean termites
(Reticulitermes flavipes and R. hageni) in central North Carolina using two classes of molecular genetic
markers. Environ. Entomol. 35:173–87
402 Vargo ·Husseneder
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
ANRV363-EN54-20 ARI 23 October 2008 13:50
139. Vargo EL, Husseneder C, Grace JK. 2003. Colony and population genetic structure of the Formosan
subterranean termite, Coptotermes formosanus, in Japan. Mol. Ecol. 12:2599–608
140. Vargo EL, Husseneder C, Woodson D, Waldvogel MG, Grace JK. 2006. Genetic analysis of colony
and population genetic structure of three introduced populations of the Formosan subterranean termite
(Isoptera: Rhinotermitidae) in the continental United States. Environ. Entomol. 35:151–66
141. Vargo EL, Juba TR, DeHeer CJ. 2006. Relative abundance and comparative breeding structure of
subterranean termite colonies (Reticulitermes flavipes,R. hageni,R. virginicus, and Coptotermes formosanus)
in a South Carolina lowcountry site as revealed by molecular markers. Ann. Entomol. Soc. Am. 99:1101–9
142. Wang CL, Powell JE, Liu YZ. 2002. A literature review of the biology and ecology of Coptotermes
formosanus (Isoptera: Rhinotermitidae) in China. Sociobiology 40:343–64
143. Yagi KJ, Kwok R, Chan KK, Setter RR, Myles TG, et al. 2005. Phe-Gly-Leu-amide allatostatin in
the termite Reticulitermes flavipes: content in brain and corpus allatum and effect on juvenile hormone
synthesis. J. Insect Physiol. 51:357–65
144. Yeap B-K, Othman AS, Lee VS, Lee C-Y. 2007. Genetic relationship between Coptotermes gestroi and
Coptotermes vastator (Isoptera: Rhinotermitidae). J. Econ. Entomol. 100:467–74
145. Important paper
identifying a gene of
major influence on caste
determination in a
145. Zhou X, Oi FM, Scharf ME. 2006. Social exploitation of hexamerin: RNAi reveals a major caste-
regulatory factor in termites. Proc. Natl. Acad. Sci. USA 103:4499–504
146. Zhou X, Tarver MR, Bennett GW, Oi FM, Scharf ME. 2006. Two hexamerin genes from the termite
Reticulitermes flavipes: sequence, expression, and proposed functions in caste regulation. Gene 376:47–58
147. Zhou X, Tarver MR, Scharf ME. 2007. Hexamerin-based regulation of juvenile hormone-dependent
gene expression underlies phenotypic plasticity in a social insect. Development 134:601–10 Biology of Subterranean Termites 403
Annu. Rev. Entomol. 2009.54:379-403. Downloaded from
by NORTH CAROLINA STATE UNIVERSITY on 12/10/08. For personal use only.
... The social arrangement of termite colonies is divided into different castes. All members of the colony, including undifferentiated immatures, cooperate in a highly integrated manner [119]. Some individuals are infertile workers and soldiers, while others are fertile, reproductive individuals. ...
... Flights occur in response to specific climatic conditions depending on the species [121]. Supplementary reproductives (or neotenics), either brachypterous (with rudimentary wings) or apterous, have the role of supporting primary reproductives in the procreation activity [119] and originate from nymphs or workers, particularly after the death of the primary reproductives, or in those cases in which a group of individuals moves away from the nest and loses influence from the original progenitors. ...
... The distribution of the main native Reticulitermes species in Europe, and the foreseen shift in the population of the introduced Reticulitermes flavipies due to climate change, are shown in Figure 5. Subterranean termites form large colonies (from several hundred thousand to millions of individuals) and can destroy dry wood structures (Figure 4a). They build their nests in the soil at 70-100 cm deep and explore wood sources in their surroundings, usually within a radius of less than 10 m, with the exception of introduced populations of R. flavipes, with foraging ranges of up to 100 m or more [119]. Because they require high levels of moisture, damage by subterranean termites is usually associated with high moisture contents in buildings and can be found frequently in basements or in other floors as a consequence of failure in sanitation and canalization systems. ...
Full-text available
In recent years, the use of wood has gained social interest, leading to a global increase in its demand. Yet, this demand is often covered by the production of woods of low natural durability against biological deterioration. The main biological agents with the potential to attack the structural integrity of wood are wood-decay fungi, saproxylic beetles, termites, and marine molluscs and crustaceans. In most circumstances, fungi are the main wood-deteriorating agents. To attack the cell wall, wood-decay fungi combine a complex enzymatic mechanism with non-enzymatic mechanisms based on low-molecular-weight compounds. In some cases, the larvae of saproxylic beetles can also digest cell wood components, causing serious deterioration to wooden structures. The impact of subterranean termites in Europe is concentrated in the Southern countries, causing important economic losses. However, alien invasive species of voracious subterranean termites are expanding their presence in Europe. Wooden elements in permanent contact with marine water can be readily deteriorated by mollusc and crustacean borers, for which current preservatives lack efficacy. The natural durability of wood is defined as the inherent resistance of wood to catastrophic action by wood-destroying organisms. Besides exposure to the climate, product design and use conditions, the natural durability of wood is key to the prediction of the service life of wooden products, which can be shortened due to the impact of global change. The major wood properties involved in natural durability are related to the composition of lignin in the cell wall, the anatomy of the xylem, nutrient availability, the amount and composition of heartwood extractives, and the presence of moisture-regulating components since wood moisture content influences the establishment of wood-degrading organisms.
... Subterranean termites constitute one of the most widely dispersed termite families (Rhinotermitidae) worldwide, and are found in tropical, subtropical, and temperate regions [171,172]. They commonly attack human-built structures and lead to high economic losses, which are estimated to be as high as 11 billion USD per year in the United States [172]. ...
... Subterranean termites constitute one of the most widely dispersed termite families (Rhinotermitidae) worldwide, and are found in tropical, subtropical, and temperate regions [171,172]. They commonly attack human-built structures and lead to high economic losses, which are estimated to be as high as 11 billion USD per year in the United States [172]. Reticulitermes virginicus, Heterotermes indicola, and Coptotermes heimi are examples of subterranean termites that have been reported to be associated with economic losses in different regions of the world [173,174]. ...
Active principles extracted from plants, such as essential oils, have been commonly described in the literature as therapeutic targets for numerous pathological conditions. Cannabis sativa, which has an ancient and peculiar history, has been used for various purposes, from recreational to compounds of pharmacotherapeutic and industrial importance, such as pesticides based on this plant. It is a plant that contains approximately 500 described cannabinoid compounds and is the target of in vitro and in vivo studies at different locations. This review clarifies the role of cannabinoid compounds in parasitic infections caused by helminths and protozoa. In addition, this study briefly presented the use of C. sativa constituents in the formulation of pesticides for vector control, as the latter topic is justified by the economic burden faced by several regions where vector-borne diseases are a troubling reality. Studies involving cannabis compounds with pesticidal potential should be encouraged, especially those that evaluate their effectiveness against the different life cycles of insects, seeking to interrupt vector proliferation after egg laying. Actions aimed at the management and cultivation of plant species with ecologically correct pharmacotherapeutic and pesticide potentials are becoming urgent.
... Termites are small detrimental creatures that cause severe economic losses to forests and agro-ecosystems by feeding plantations below the soil surface and destroying the internal root systems of plants by making tunnels (Vargo and Husseneder, 2009;Shelton et al., 2014). The efficacy of different integrated termite management approaches has been compromised primarily due to the cryptic feeding behavior of this pest. ...
Full-text available
Termites have become a global concern, and their effective management has remained a challenge since time immemorial. Certain microbial and botanical agents have been used for their management, but their efficacy has been compromised, particularly in field conditions. Hence, the current study was designed to check the efficacy of low doses of different pesticides, such as chlorpyrifos, fipronil, bifenthrin, and chlorantraniliprole, against mortality and behavioral responses of Odontotermes obesus at two different temperatures (16 ± 1 and 26 ± 1°C). The discrete behavioral symptoms included intoxication, ataxia, moribundity, and death. Laboratory-maintained termite workers were exposed to different concentrations of pesticides through a filter paper bioassay. All tested pesticides and their concentrations differed significantly regarding their lethal time (LT 50 ) values compared to the mortality of termite workers. Moreover, the LT 50 values of pesticides gradually decreased with increased pesticidal concentrations. Temperature also had a significant effect on the efficacy of tested pesticides as all pesticides showed better results at higher temperatures. At both tested temperatures, chlorantraniliprole (5 ppm) proved to be the most effective pesticide against termite workers. Similarly, the behavioral symptoms also varied depending on pesticides and their administered concentrations and existed for a relatively longer time span at lower temperatures. In most cases, the order of responses was moribundity, followed by intoxication and ataxia. Moribundity and intoxication were the most frequently observed symptoms for chlorpyriphos and bifenthrin-treated termite workers. In the case of fipronil, intoxication was the most pronounced symptom. Similarly, the maximum value of ataxia was recorded in the case of chlorantraniliprole. However, moribund symptoms lasted longer in all tested concentrations of chlorantraniliprole, followed by ataxia and intoxication. The overall order of toxicity was chlorantraniliprole > bifenthrin > fipronil > chlorpyrifos. These pesticides, at their low doses, did not exhibit any repellent action and were not detected by the foraging termite workers. Moreover, their slow action mechanism makes them a suitable candidate for infecting whole colonies away from treated surfaces. Therefore, these pesticides can be successfully incorporated into different integrated termite management programs to keep the plantation free from threatening underground pests.
... Therefore, R. speratus is a suitable candidate for the biochemical and molecular studies of termite queens that require several samples for multiple analyses. The lifespan of Reticulitermes termite queens is expected to be > 11 years (Long et al., 2007;Vargo & Husseneder, 2009;Korb & Thorne, 2017), and long-lived R. speratus queens exhibit lower oxidative damage and higher antioxidant activities than short-lived workers (Tasaki et al., 2017a;Tasaki et al., 2018). These findings suggest that termite queens can utilize the antioxidant system as one of the longevity mechanisms to support the evolution of extended lifespan. ...
Termite queens and kings live longer than nonreproductive workers. Several molecular mechanisms contributing to their long lifespan have been investigated; however, the underlying biochemical explanation remains unclear. Coenzyme Q (CoQ), a component of the mitochondrial electron transport chain, plays an essential role in the lipophilic antioxidant defense system. Its beneficial effects on health and longevity have been well studied in several organisms. Herein, we demonstrated that long-lived termite queens have significantly higher levels of the lipophilic antioxidant CoQ10 than workers. Liquid chromatography analysis revealed that the levels of the reduced form of CoQ10 were 4 fold higher in the queen's body than in the worker's body. In addition, queens showed 7 fold higher levels of vitamin E, which plays a role in antilipid peroxidation along with CoQ, than workers. Furthermore, the oral administration of CoQ10 to termites increased the CoQ10 redox state in the body and their survival rate under oxidative stress. These findings suggest that CoQ10 acts as an efficient lipophilic antioxidant along with vitamin E in long-lived termite queens. This study provides essential biochemical and evolutionary insights into the relationship between CoQ10 concentrations and termite lifespan extension.
... Reticulitermes is a well-studied termite genus in terms of its reproductive biology, oogenesis or ovarian development, and caste differentiation (Fig. 1C) [27][28][29][30][31], and the complete genome has recently been provided [32]. In R. speratus, most mature eld colonies contain tens to hundreds of neotenic queens [33,34], which are usually derived from nymphs [24]. ...
Full-text available
Tissue-specific endopolyploidy is widespread among plants and animals and its role in organ development and function has long been investigated. In insects, the fat body cells of sexually mature females produce substantial amounts of egg yolk precursor proteins (vitellogenins) and exhibit high polyploid levels, which is considered crucial for boosting egg production. Termites are social insects with a reproductive division of labor, and the fat bodies of mature termite queens exhibit higher ploidy levels than those of other females. The fat bodies of mature termite queens are known to be histologically and cytologically specialized in protein synthesis. However, the relationship between such modifications and polyploidization remains unknown. In this study, we investigated the relationship among cell type, queen maturation, and ploidy levels in the fat body of the termite Reticulitermes speratus . We first confirmed that the termite fat body consists of two types of cells, that is, adipocytes, metabolically active cells, and urocytes, urate-storing cells. Our ploidy analysis using flow cytometry has shown that the fat bodies of actively reproducing queens had more polyploid cells than those of newly emerged and pre-reproductive queens, regardless of the queen phenotype (adult or neotenic type). Using image-based analysis, we found that adipocytes became polyploid during queen differentiation and subsequent sexual maturation. These results suggest that polyploidization in the termite queen fat body is associated with sexual maturation and is regulated in a cell type-specific manner. Our study findings have provided novel insights into the development of insect fat bodies and provide a basis for future studies to understand the functional importance of polyploidy in the fat bodies of termite queens.
... In the single-site termite Incisitermes minor (Kalotermitidae), apparent daily feeding rhythms are largely driven by temperature (Lewis et al. 2013). Similar temperature-driven daily feeding rhythms have been observed in field colonies of termites of the genus Reticulitermes (Fuchikawa et al. 2012), which has features of single-site termites but with separatesite habitats; they nest and feed in the same substrate but also forage in nearby substrates (Vargo and Husseneder 2009). In a laboratory experiment, Reticulitermes workers showed no daily rhythmic behavior (T. ...
In insects, circadian clocks regulate daily rhythmicity in behavior (e.g., activity, feeding, mating, and oviposition), physiological processes, and developmental events such as hatching, pupariation, and eclosion. While the abiotic environment poses risks such as death or sterility due to extreme temperatures or desiccation, interactions with the biotic environment also give rise to other stressors such as energy expenditure, starvation, and predation risk. In this chapter, we discuss studies, mostly on drosophilid species, in laboratory as well as natural environments, highlighting the impact of rhythmic light and temperature on clock evolution. We also examine how clocks modulate life-history traits and, conversely, how selection on life-history traits may alter circadian clock properties. We also present a few studies emphasizing the vast diversity in clock function across different insect taxa. Last, we draw attention to the consequences of a rapidly changing climate on insect physiology, specifically rhythms.KeywordsAdaptationCircadian Drosophila EvolutionInsectRhythm
Full-text available
In insects, ecological competition has often resulted in phenotypic changes and modifications to foraging areas. In termites—and social insects as a whole—colonies cannot easily escape competition through the relocation of their colony. In these species, the outcomes of inter and intra-specific competition are influenced by different life history traits, such as colony size, breeding system (number and types of reproductives), food preference, tunneling patterns, nest site selection, and antagonism between colonies. Here, we investigated variation in breeding system and spatial distribution among colonies of a higher termite Amitermes parvulus and a subterranean termite Reticulitermes flavipes within an urban landscape. We first developed microsatellite markers as a tool to study these life history traits in A. parvulus. Second, we assessed competitive exclusion or tolerance of A. parvulus and R. flavipes colonies by determining their fine-scale distribution using monitoring stations on a grid site, and their large-scale distribution across an urban landscape. Third, we investigated the breeding system of A. parvulus colonies. We showed that the numerous colonies of R. flavipes inhabiting a restricted area contrast with the few, but spatially expansive colonies of A. parvulus, suggesting these species face different degrees of intra-specific competition. We showed that colonies of A. parvulus frequently merged together, and all of them were likely headed by inbred neotenic reproductives, two characteristics rarely observed in higher termites. Overall, our study revealed drastic differences in colony structure, breeding systems and foraging ranges between the two species. These differences may reflect differences in food preference and food availability between the two species allowing their co-existence within the same urban environment.
The highly developed sociality of insects has been well studied from the perspectives of animal behavior, physiology, and ecology. However, less effort has been devoted to examining the chronobiology of social insects, likely because the lifestyle of most insects involves dense cohabitation of many individuals within small, dark places. This chapter reviews the circadian behavioral rhythms of social insects such as bees, ants, and termites, focusing first on the general features of circadian patterns in social hymenopterans and termites and then on insect entrainment to environmental cycles such as light and social cues, which are fundamental properties of circadian rhythms. Finally, the ontogeny and plasticity of insect circadian rhythms are discussed.KeywordsCircadian behavioral rhythmsOntogeny of circadian rhythmsPlasticity of circadian rhythmsSocial entrainmentSocial insects
Full-text available
In eusocial termites, successful pairing is an essential element of dispersal and distribution after the departure of alates from natal colonies. Two situations could arise during the pairing process: mixed-sex pairs and same-sex pairs. However, most previous studies focused on mixed-sex pairs, overlooking groups formed by same-sex pairings, especially potential fecundity (the total number of oocytes or ovarioles), oogenesis and the development stage of oocytes of females in female-female pairs, and spermatogenesis and testis development of males in male-male pairs. In this study, through experimentation, we investigated the reproductive ability of virgin dealates based on various pairing types as mentioned above. We found that the life spans of virgin dealates can cover 1 yr or even more when they establish a nest with a partner, which is more than 10-fold longer than the life span of individuals establishing a colony alone. After 1 yr of pairing, the potential fecundity of virgin same sex dealates did not degenerate significantly compared with newly emerged dealates, including the number of ovarioles, size of testis, oogenesis, and the development stage of the oocytes. Moreover, when individuals of same-sex pairings experimentally changed into mixed-sex pairs after 1 yr, the eggs produced in the colony hatched into larvae. These findings suggest that dealates which through same-sex pairs retain fecundity after 1 yr have more reproductive potential than dealates that failed to pair with heterosexuals, shedding light on the ecological significance of homosexual behaviors in terms of the successful extension and fecundity of eusocial termites.
The book is a new compendium in which leading termite scientists review the advances of the last 30 years in our understanding of phylogeny, fossil records, relationships with cockroaches, social evolution, nesting, behaviour, mutualisms with archaea, protists, bacteria and fungi, nutrition, energy metabolism,population and community ecology, soil conditioning, greenhouse gas production and pest status.
We describe a model-based clustering method for using multilocus genotype data to infer population structure and assign individuals to populations. We assume a model in which there are K populations (where K may be unknown), each of which is characterized by a set of allele frequencies at each locus. Individuals in the sample are assigned (probabilistically) to populations, or jointly to two or more populations if their genotypes indicate that they are admixed. Our model does not assume a particular mutation process, and it can be applied to most of the commonly used genetic markers, provided that they are not closely linked. Applications of our method include demonstrating the presence of population structure, assigning individuals to populations, studying hybrid zones, and identifying migrants and admixed individuals. We show that the method can produce highly accurate assignments using modest numbers of loci—e.g., seven microsatellite loci in an example using genotype data from an endangered bird species. The software used for this article is available from
The spectrum of eusociality in termites. Social Competition and Cooperation in Insects and Arachnids. Cambridge: Cambridge University Press. pp. 52-93.