Jpn. J. Protozool. Vol. 45, No. 1, 2. (2012)

29

OriginalVariation and diversity of symbiotic protist
composition in the damp-wood termite Hodotermopsis
sjoestedti
Osamu KITADE1*, Yoshinobu HAYASHI2, Kaori TAKATSUTO1 and Tadao
MATSUMOTO3G
1

College of Science, Ibaraki University, Mito, Ibaraki 310-8512, JapanGG
School of Biological Sciences, The University of Sydney, Sydney, NSW 2006, AustraliaGG
3
Faculty of Liberal Arts, The Open University of Japan, Mihama, Chiba 261-8586 JapanG
2

SUMMARY
It is well recognized that composition of termite symbiotic protist community generally show hostspecies specificity at species-to-species level. On the other hand, studies focused on population or colonylevel variations of the protist composition are few, although such studies are necessary for understanding
the termite-protist mutualism. In this study we investigated symbiotic protist fauna of 34 Hodotermopsis
sjoestedti nests collected from five islands in the Ryukyu Archipelago, Taiwan Is., and southern part ofChinese continent. Thirteen parabasalid species and six oxymonad species, which were reported from thehost termite collected in Yakushima Is., were recognized in this study. Four parabasalids were identified
as recently described species from H. sjoestedti collected in Vietnam. The fauna was the most speciesrich among the termite hosts studied to date, possibly reflecting large host body size. The prevalence
rates of the symbiotic protist species are generally high, 100% in all populations for all protist species,
except Gen. A sp. and Hoplonympha sp. All host nests had identical protist species composition except
for the presence or absence of Gen. A sp. Two host populations lacked this species. In Yakushima Is.,
both types of termite nests were found, which exhibited mutually exclusive distribution. The distribution
pattern suggests that the host termite is a multiple-site nester and nest-budding occurs in the field.
Key words: Symbiosis, Parabasalia, Oxymonadida, Protist community

INTRODUCTION
Symbiotic protist community in hindguts oftermites is one of the textbook examples of wood*Corresponding author
Tel/Fax: +81-29-228-8375G
E-mail: kitade@mx.ibaraki.ac.jp
Received: 16 Mar. 2012; Accepted: 18 Oct. 2012.

degrading symbiosis (Cleveland, 1923; Inoue etal., 2000; Brune and Ohkuma, 2011; Ohkuma andBrune, 2011). The symbionts are consisted of two
lineages of anaerobic protists Parabasalia and Oxymonadida that lack mitochondria and can not survive outside the host digestive tracts (Brugerolle
and Radek, 2006). The host termites are social
insects and live in large family group called30

Symbiotic
protist composition of HodotermopsisG“colony”, making up spatially structured aggregation of community of the symbiotic protists. A new
host colony is founded by a pair of male and female alates (i.e., winged reproductive individuals,
called king and queen), and they succeed the protist symbionts of mother nests.GG
From the viewpoint of community ecology,
the termite symbiont community is unique among
symbiont (or parasite) communities in animal digestive tracts because the species composition
generally shows strong host-species specificity: acertain set of protist species are found from digestive tracts of a termite species (Kirby, 1934; Honigberg, 1970; Inoue et al., 2000; Kitade, 2004).
The mode of symbiont transmission through generations should lead to co-speciation between thehosts and the symbionts and thus the specificity of
the fauna. The co-speciation was verified for aparabasalid genus Pseudotrichonympha spp. andhost termites of the family Rhiontermitidae using
molecular phylogenetic analysis (Noda et al.,2007; Lo and Eggleton, 2011).GG
Although this species-to-species level hostspecificity is well recognized and described intaxonomic papers (Yamin, 1979), taxonomists also
noticed that sometimes a termite individuals or,rarely a whole colony, lack a particular protist species (Honigberg, 1970). However, most of the reports were fragmentary and ecological studies
were few that gave a fine description of colony- or
population-level variations of the protist species
composition. A detailed study was carried out forthe symbiont composition of Reticulitermes(Rhinotermitidae), a common termite genus in
Japan, based on the survey of the 84 field colonies
of six host species in the Japan Archipelago(Kitade and Matsumoto, 1993). The study revealed
that at species-to-species level, the host termites
certainly exhibited strict host specificity. However,the faunae in host individuals were not absolutely
uniform and the mean prevalence of each protist
species in a host species ranged from 0.68 to 1.0.
Each host species possessed species-specific“basic symbiont species composition”, and fromthis composition, a small fraction of individuals orcolonies lacked one or two symbiont species. For
other termite taxa, there is no reliable description
about the variation of the symbiont fauna, while
such ecological basis of the termite-symbiotic protist community is important for understanding theestablishment and maintenance processes of thesymbiotic protist community and evolution of mutualism.GG
In this study we investigated symbiotic protist fauna of Hodotermopsis sjoestedti Holmgren, asingle member of the genus Hodotermopsis in thefamily Termopsidae, which is distributed in East
Asia including southern part of Chinese continent,
Taiwan Is., and some islands in the northern Ryukyu Archipelago (Matsumoto and Hirono, 1985).
This species is one of the host insects of parabasalid and oxymonad protists with the largest bodysize. Like other members of the Termopsidae,
Hodotermopsis has been regarded as a “single-site
nester” whose colony nests in a single large deadlog or stump (Matsumoto and Hirono, 1985).
However, recent study of termite phylogeny basedon sequences of multiple genes did not support themonophyly of Termopsidae. The inferred phylogeny suggested that Hodotermopsis formed a cladewith the members of Hodotermitidae, althoughsupport of the topology is not strong (Inward et al.,2007a).GG
From H. sjoestedti in Japan, 19 species of thesymbiotic parabasalids and oxymonads were tentatively reported by Kitade et al. (1993). Brugerolleand Bordereau (2004) and Brugerolle (2005) observed ultrastructure of the parabasalid symbionts
and described five species from materials in Vietnam. Based on these preceding studies, we focused on investigation of the variations in symbiont species composition between termite colonies
and between regional populations using nests from
Ryukyu Archipelago, Taiwan Is., and Guandongprov., Continental China. To examine as many
fresh termite nests and individuals as possible andJpn. J. Protozool. Vol. 45, No. 1, 2. (2012)

to grasp characteristics of the field community, we
did not investigate population size of each symbiont species (i.e., community structure). The community structure is sensitive to changes in environmental conditions and requires much longer time
for the investigation.G
MATERIALS AND METHODS
Sample collection
We collected host termite nests during 19902010 from all the islands in the Ryukyu Archipelago, Japan, where H. sjoestedti was reported: 15
nests from Yakushima Is., two from TanegashimaIs., five from Nakanoshima Is., four from Amamioshima Is., and five from Tokunoshima Is.
These nests were collected from dead logs in laurel
forests, and in Yakushima Is., we mapped 14 nests
collected in Onoaida in Nov. 1991. The termites,
together with nest wood, were brought back to thelaboratory and maintained individually in plastic
boxes at 22 or 25ÛC under all dark condition until
investigation of the intestinal protists. We also
observed termite symbionts from two nests from
Nanshanxi, Nantou county, Taiwan Is., Republicof China and Shixhin, Guandong province, Continental China, just after they were collected in thefield. The host termite distributed in the Ryukyu
Archipelago and Shixing was formerly classified
as H. japonica and H. yui.
Examination of protist composition
Preceding the investigation of the protist
composition, we made and observed protargolstained specimens of the protists using one representative termite from each locality in Japan following Kitade et al. (1997). Based on the specimens, we listed the protist species and carefullycompared the morphology of them with living
materials in order to identify all the symbiont species in living state.GG
To investigate the variation of protist composition, for each termite nest, we examined presence31

or absence of the protist species for ten termites
individually. The examined termites were fifth- orlater-instar larvae and thought to function as main
workforce in the colony. We pulled out the intestine of the living insects with forceps, dissected it
in 0.6% NaCl solution, and suspended the intestinal contents. Then we dispensed intestinal fluid
onto several glass slides and observed all of themby differential interference microscope (BX-50,
Olympus).GG
For the samples of Taiwan Is. and Shixhin,
protsit composition was examined by observationof all intestinal contents using a portable phasecontrast microscope (DSM-II, Daiko Science). For
these samples, protargol specimens were examined
after the living samples were investigated.
G
Statistic analysis
Based on the protist composition data of ten
termites from each of termite nests, we calculated
mean prevalence value of each of seven populations. Standard deviations (SD) of the prevalencevalues between colonies were also calculated foreach population.
GWe carried out Mantel test (Mantel, 1967)
to examine whether the host nests of the different
symbiotic protist composition types exhibited mutually exclusive distribution in Onoaida, Yakushima Is. A matrix of geographical distance and thatof ‘distance of protist composition type’ were calculated between all termite nests mapped in Onoaida. As the distance of protist type, 0 and 1 wererespectively assigned for nest pairs of same anddifferent composition types (A and B, see results
and Table 1). Then a Mantel statistic ZM was calculated as the sum of cross products of the corresponding elements, x and y, of the two matrices:GG
Gn 1 nZM¦ ¦x yi 1 j i 1

ij

ij

where i and j are row and column indices and n is
number of the nests, respectively. Significance ofthe correlation was tested by comparing the origi-

32

Symbiotic
protist composition of HodotermopsisGnal ZM value with the frequency distribution of ZM
values calculated from 999 pairs of the matrices,which were produced by random element interchanges of the original matrices. The test was carried out with R ver. 2.9.2 (The R project for statistical computing, http://www.r-project.org/) and“vegan” program package.
RESULTS
All of the 13 parabasalid species and the six
oxymonad species, reported from H. sjoestedti
from Yakushima Is. in the Ryukyu Archipelago(Kitade et al., 1997), were recognized from thematerials of this study (Table 1).GG
Of these species, four parabasalids were recently described species from H. sjoestedti in Vi-

etnam by Brugerolle and Bordereau (2004: Holomastigotes lanceolata) and Brugerolle (2005: Microjoenia minima, Spirotrichonympha cincta,
Spironympha oblonga, and S. obtusa). Additionally, one Eucomonympha and three Trichonymphaspecies reported by Brugerolle and Bordereau(2004) corresponded well to the generic and specific composition of symbionts recognized in thisstudy.GG
The protist fauna found in this study includes
three parabasalid species that had similar morphology to Trichomonoides trypanoides (Duboscq and
Grassé), Holomastigotes elongatum Grassi and
Hoplonympha natator Light, recently reported
from H. sjoestedti in Vietnam (Brugerolle, 2005).
However, we tentatively did not assign these specific names to our materials: the latter three spe-

Table 1. Prevalence of each protist species
Population / Number of termites (nests) examinedGTN
20 (2)

NK
50 (5)

AM
40 (4)

TK
50 (5)

NSX
20 (2)

SHX
10 (1)

Total
340 (34)

Parabasalia
Trichomonoides sp. 1)G
1.00
Gen. A sp.G
0.55 ± 0.49G
Microjoenia minimaG
1.00
Spirotrichonympha cinctaG
1.00
Spironympha oblonga 2)G
1.00Spironympha obtusa 3)G
1.00Holomastigotes lanceolata 4)G
1.00Holomastigotes sp. 5)G
1.00
Hoplonympha sp.G
0.95 ± 0.18
Eucomonympha sp.G
1.00
Trichonympha sp. 1G
1.00
Trichonympha sp. 2G
1.00
Trichonympha sp. 3G
1.00
OxymonadidaG
Pyrsonympha sp. 1 6)G
1.00Pyrsonympha sp. 2 6)G
1.00Dinenympha sp. 1 7) 
1.00Dinenympha sp. 2 7)G
1.00Dinenympha sp. 3 7)G
1.00Gen. B sp. 8)G
1.00


1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00

1.00
1.00
1.00
1.00
1.00
1.00


1.00
-
1.00
1.00
1.00
1.00
1.00
1.00
0.82 ± 0.40
1.00
1.00
1.00
1.00

1.00
1.00
1.00
1.00
1.00
1.00


1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00

1.00
1.00
1.00
1.00
1.00
1.00


1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
0.92 ± 0.18
1.00
1.00
1.00
1.00

1.00
1.00
1.00
1.00
1.00
1.00


1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00

1.00
1.00
1.00
1.00
1.00
1.00


1.00
-
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00

1.00
1.00
1.00
1.00
1.00
1.00


1.00
0.66 ± 0.47
1.00
1.00
1.00
1.00
1.00
1.00
0.94 ± 0.20
1.00
1.00
1.00
1.00

1.00
1.00
1.00
1.00
1.00
1.00

Basic protist composition typeG A(8)*, B(7)*G

A

B

A

A

A

B



Symbiont SpeciesG

YK
150 (15)

Each value is represented by mean ± SD. YK: Yakushima Is.; TN: Tanegashima Is.; NK: Nakanoshima Is.; AM: Amamioshima Is.; TK: Tokunoshima Is.; NSX: Nanshanxi; SHX: Shixing. *: No. of colonies with each protist composition type. 1)8) corresponds to the species listed in Kitade et al. (1997), 1) : Trichomonas sp.; 2) : S. sp. 1; 3) : S. sp. 2; 4): H. sp. 1; 5): H. sp. 2;
6): Pyrsonympha (Pyrsonympha) sp. 1-2; 7): P. (Dinenypha) sp. 1-3; 8): P. (Subgen. A) sp.

Jpn. J. Protozool. Vol. 45, No. 1, 2. (2012)

cies were originally described as symbionts of
distantly related termites to Hodotermopsis,(Reticulitermes spp. and Paraneotermes simplicicornis), and Hoplonympha sp. found from H.
sjoestedti populations in this study often exhibitedmuch larger body length than H. natator.
Brugerolle and Bordereau (2004) reported Trichomitopsis termopsidis (Cleveland), a symbiontof termite genus Zootermopsis spp. (Termopsidae),from H. sjoestedti in Vietnam. In this study, however, T. termopsidis was not found but we recognized Gen A sp. (see Kitade et al., 1997). Examination of protargol specimens revealed that thisspecies had typical morphological character statesof genus Trichomitopsis and similar morphology
to T. termopsidis. On the other hand, Gen. A sp. is,besides a single nucleus and axostyle, equippedwith two karyomastigonts (Kitade et al., 1997)
which Trichomitopsis and other typical Trichomonadid species (sensu Brugerolle and Patterson,2001) have one.GG
Six oxymonad species reported by Kitade etal. (1997) were definitely recognized by morphology. For Dinenympha and Pyrsonympha, however,the fauna might include 1-2 unrecognized species.
Gen. B sp. could not be assigned to the any extant
genus (see Kitade et al., 1997).GG
At the level of termite nests (colonies), twotypes of basic protist compositions were recognized: the composition composed of the 19 protist
species (hereafter, composition type A) and thatlacked only one species, Gen. A sp., from the type
A composition (composition type B). All investigated nests in Amamioshima Is., Tokunoshima Is.
and Nanshanxi had type A and those in Nakanoshima Is. (N = 5) and Shixhin (N = 1) had type
B. In Yakushima Is., both nests with composition
type A (N = 8) and those with type B (N = 7) were
found. The prevalence rates of the symbiotic protist species were generally high, 100% in all populations for all protist species, except Gen. A sp.
and Hoplonympha sp. The prevalence of Gen. A
sp. was 100% in Tokunoshima Is., Amamioshima

33

Fig. 1. Distribution of H. sjoestedti nests found in 1991 in
the study site in Onoaida, Yakushima Is. Closed and open
circles represent nests with basic symbiont composition
type A and B, respectively (see Table 1).G

Is. and Nanshanxi, while it was much lower in
Nakanoshima Is. (0%), Shixhin (0%), and Yakushima Is. (55.3%). One nest was found in each of
three host populations containing termites without
Hoplonympha sp.: Yakushima Is. (prevalence:
95.3%), Nakanoshima Is. (82.0%), and Tokunoshima Is. (92.0%).GG
In the sampling site in Onoaida, YakushimaIs., both type of host nests with and without Gen.
A sp. were found (Fig. 1). The both type of nests
exhibited significantly mutually exclusive distribution (N = 14, Mantel test, P = 0.041).GG
GDISCUSSIONGThe high prevalence rate of each symbiotic
protist species in H. sjoestedti is the common feature with Reticulitermes host termites investigatedby Kitade and Matsumoto (1993), and probably
the general characteristic of termite protist community. As with Reticulitermes hosts, H. sjoestedti
has basic symbiont composition composed of 19
species, and from this composition, a particular
local population or individual lack one or two
symbiont species. Such high host specificity found34

Symbiotic
protist composition of HodotermopsisGin the termite protists is rare among the intestinal
parasite/symbiont communities of metazoans (e.g.
Esch et al., 1990). Together with the transmission
mode of protists, the specificity probably reflect
close mutualistic relationships between the hosts
and the multiple symbionts including intestinal
prokaryotes, through complex metabolic system
involved in wood degradation (Brune and Ohkuma, 2011).GG
The symbiotic protist fauna of H. sjoestedti
is the most species-rich among the termites studied
to date (Kitade et al., 1997; Yamin, 1979), except
for wood feeding cockroach genus Cryptocercus,
which is now recognized as sister taxon of termites
based on the molecular phylogenetic analyses (Loet al., 2000; Inward et al., 2007b). The prevalence
rates of the protist species constituting the basic
symbiont composition of H. sjoestedti, 100% except for two parabasalid species, are rather higher
than those of Reticulitermes spp. (Kitade andMatsumoto, 1993) sympatrically distributed in thesampling localities of this study and often coexisted in the same log (Kitade, 2004). Degrees of diversity and stability of the protist communities arelikely to be explained by host body size, as expected from the theory of island biogeography(MacArthur and Wilson, 1967). The much larger
body size and hindgut volume of Hodotermopsis(H. sjoestedti soldier mean head width: 4.69 mm,
N = 143, Huang et al., 2000) probably allow thelarger population size of each symbiont species
and thus diverse and stable symbiont community
structure than Reticulitermes (R. speratus speratus
soldier mean head width: 1.18 mm, N = 25, Takematsu, 1999). Similarly, large body size of Cryptocercus (C. punctulatus adult mean head width:
4.76 mm, N = 44, Nalepa et al., 2008) probably
enables the maintenance of the species-rich symbiont community (C. punctulatus: 23 species wererecognized by Cleveland et al., 1934).
GThe Nakanoshima and Shixhin populationsof H. sjoestedti lacked the symbiont species Gen A
sp. This population-level difference of the species

composition does not show correspondence to thephylogeny among the populations inferred frommitochondrial gene sequences (Maekawa et al.,1998). The most parsimonious explanation basedon the host phylogeny is that the common ancestorof H. sjoestedti harbored Gen. A sp. and in some
populations lack of the symbiont species occurred
independently. This symbiont species probably has
characteristics that tend to trigger colony- or population-level local extinction.GG
In Yakushima Is., both types of H. sjoestedti
nests coexist that harbor and lack Gen. A sp.,showing mutually exclusive distribution. These
facts lead following suggestions concerning ecology and reproductive mode of the host termite.
First, H. sjoestedti is not a single-site nester, but a“multiple-site nester” whose colony simultaneously utilizes multiple logs as nests and feeding sites.
It is presumable that neighboring host nests withsame protist composition type are owned by a single colony. Some reports of field studies that several nests of this termite species lacked reproductive castes (king and queen) (Matsumoto and Hirono, 1985; Miura et al., 2000) possibly support
our suggestion. Moreover, although all termites in
the family Termopsidae, including H. sjoestedti,
has been recognized as a single-site nester, a recent
molecular phylogenetic study suggests that
Hodotermopsis does not form monophyletic groupwith other Termopsid genera, but is closely related
to genera in the Hodotermitidae (Inward et al.,2007a).GG
Second, outbreeding by alate reproductive
pair (king and queen) may not be a dominant reproduction mode of H. sjoestedti. When an alate
pair establishes a new nest by outbreeding, thecolony members succeed the symbiotic protist
fauna of the mother colonies of the alates (Wakui,
unpublished data). In a normal termite population
where the outbreeding is dominant, even if a symbiont species disappeared in a termite colony, theincomplete symbiont fauna of the alates from thecolony must be complemented by their mates andJpn. J. Protozool. Vol. 45, No. 1, 2. (2012)

the alate pairs can produce new colonies with complete fauna. The high intra-populational variationand patterns of distribution of the two types offauna in Yakushima Is. suggest that H. sjoestedti
colonies mainly multiply through unusual mode of
reproduction, possibly by colony budding and inbreeding by neotenic reproductives. These possibilities should be verified by ecological genetic
studies of the host termite colonies using highresolution codominant DNA markers.
ACKNOWLEDGEMENTS
The authors thank Drs. Ping, Z.-M., Huang,
F.-S., Zhu, Y.-I., Terayama, M. for providing termite colonies or assist for the field study. Thanks
are also due to Drs. Wang, J.-S., Hirono, Y.,
Miura, T., Maekawa, K. for their help in field sampling and instruction. This work was supported by
Grant-in-Aid in for Scientific Research (Nos.
21310024, 22370008, 23657013).G
REFERENCES
Brugerolle, G. and Patterson, D. J. (2001) Ultrastructure of Joenia pulchella Grassi, 1917
(Protista, Parabasalia), a reassessment of
evolutionary trends in the parabasalids, and a
new order Cristamonadida for devescovinid,
calonymphid lophomonad flagellates. Org.
Divers. Evol., 1, 147–160.GG
Brugerolle, G. and Bordereau, C. (2004) The flagellates of the termite Hodotermopsis
sjoestedti with special reference to Hoplonympha, Holomastigotes and Trichomonoides trypanoides, n. comb. Eur. J. Protistol. 40, 163–174.
Brugerolle, G. (2005) The flagellates of the termite
Hodotermopsis sjoestedti: Immunologicaland ultrastructural characterization of four
new species in the genera Spirotrichonympha, Spironympha and Microjoenia. Eur. J.
Protistol., 41, 299–311.GG

35

Brugerolle, G. and Radek, R. (2006) Symbiotic
protozoa of termites. In: Intestinal Microorganisms of Termites and Other Invertebrates.
Konig, K. and Varma, A. (eds.). Springer,
Berlin Heiderberg, pp. 243–269.
Brune, A. and Ohkuma, M. (2011) Role of thetermite gut microbiota in symbiotic digestion. In: Biology of Termites: A Modern
Synthesis. Bignel, E. D., Roisin, Y. and Lo,
N. (eds.). Springer, Dordrechit Heiderberg,
pp. 439–475.GGG
Cleveland, L. R. (1923) Symbiosis between termites and their intestinal protozoa. Proc.
Natl. Acad. Sci. USA, 9, 424–428.GG
Cleveland, L. R., Hall, S. R., Sanders, E. P. andCollar, J. (1934) The wood feeding roach
Cryptocercus, its protozoa, and the symbiosis between protozoa and roach. Mem. Am.
Acad. Art. Sci., 17, 185–342.
Esch, G. W., Bush, A. O. and Aho, J. M. (1990)
Parasite Communities: Patterns and Processes. Chapman and Hall, London.GG
Honigberg, B. M. (1970) Protozoa associated withtermites and their role in digestion. In: The
Biology of Termites. Vol. II. Krishna, K. andWeesner, F. M. (eds.). Academic Press, New
York, pp. 1–36.GG
Huang, F., Zhu, S., Ping, Z., He, X., Li, G. andGao, D. (2000) Fauna Sinica. Insecta. Vol.
17 Isoptera. Science Press, Beijin.GG
Inoue, T., Kitade, O., Yoshimura, T. andYamaoka, I. (2000) Symbiotic associations
with protists. In: Termites: Evolution, Sociality, Symbioses, Ecology. Abe, T., Bignel,
D. E., and Higashi, M. (eds.). Kluwer, Dordrechit, pp. 275–288.
Inward, D. J. G., Voglera, A. P. and Eggleton, P.
(2007a) A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key
aspects of their evolutionary biology. Mol.
Phylogenet. Evol., 44, 953–967.GG
Inward, D. J. G., Beccaloni, G. and Eggleton, P.
(2007b) Death of an order: a comprehensive

36

Symbiotic
protist composition of HodotermopsisGmolecular phylogenetic study confirms thattermites are eusocial cockroaches. Biol.
Lett., 3, 331–335.GG
Kirby, H. (1934) Protozoa in termites. In: Termites
and Termite Control. Kofoid, C. A. (ed.).
University of California Press, Berkeley, pp.
84–93.
Kitade, O. (2004) Comparison of symbiotic flagellate faunae between termites and a woodfeeding cockroach of the genus Cryptocecus.
Microb. Environ. 19, 215–220.
Kitade, O. and Matsumoto, T. (1993) Symbiotic
protistan faunae of Reticulitermes (Isoptera:
Rhinotermitedae) in the Japan Archipelago.
Sociobiology, 23, 135–153.
Kitade, O., Maeyama, T. and Matsumoto, T.
(1997) Establishment of symbiotic flagellatefauna of Hodotermopsis (Isoptera: Termopsidae). Sociobiology, 30, 161–167.
Lo, N., Tokuda, G., Watanabe, H., Rose, H.,
Slator, M., Maekawa, K., Bandi, C. andNoda, H. (2000) Evidence of multiple genesequences indicates that termites evolved
from wood feeding cockroaches. Curr. Biol.,
10, B01–B04.GG
Lo, N. and Eggleton, P. (2011) Termitre phylogenetics and cocladogenesis with symbionts.
In: Biology of Termites: A Modern Synthesis. Bignel, E. D., Roisin, Y. and Lo, N.
(eds.). Springer, Dordrechit Heiderberg, pp.
27–50.GG
MacArthur, R. H. and Wilson, E. O. (1967) The
theory of Island Biogeography. Princeton
University Press, Princeton.
Maekawa, K., Miura, T., Kitade, O. and Matsumoto, T. (1998) Genetic variation and molecularphylogeny based on the mitochondrial genesof the damp-wood termite Hodotermopsis
japonica (Isoptera: Termopsidae). Entomol.
Sci., 1, 561–571.GG
Mantel, N. (1967) The detection of disease clustering and a generalized regression approach.
Cancer Res., 27, 209–220.

Matsumoto, T. and Hirono, Y. (1985) On the caste
composition of a primitive termite
Hodotermopsis
japonicus
Holmgren(Isoptera, Termopsidae). Sci. Pap. Coll. Arts
& Sci. Univ. Tokyo, 35, 211–216.GG
Miura, T., Hirono, Y., Machida, M., Kitade, O.
and Matsumoto, T. (2000) Caste developmental system of the Japanese damp-woodtermite Hodotermopsis japonica (Isoptera:
Termopsidae). Ecol. Res., 15, 83–92.GG
Nalepa, C. A., Maekawa, K., Shimada, K., Saito,
Y., Arellano, C. and Matsumoto, T. (2008)
Altrical development in subsocial woodfeeding cockroaches. Zool. Sci., 25, 1190–
1198.GG
Noda, S., Kitade, O., Inoue, T., Kawai, M.,
Kanuka, M., Hiroshima, K., Hongoh, Y.,
Constantino, R., Uys, V., Zhong, J., Kudo, T.
and Ohkuma, M. (2007) Identification andcharacterization in the triplex symbiosis oftermite gut protist (Pseudotrichonymphaspp.), their hosts, and their bacterial endosymbionts. Mol. Ecol., 16, 1257–1266.
Ohkuma, M. and Brune, A. (2011) Diversity,
structure, and evolution of the termite gut
microbial community. In: Biology of Termites: A Modern Synthesis. Bignel, E. D.,
Roisin, Y. and Lo, N. (eds.). Springer, Dordrechit Heiderberg, pp. 413–438.
Takematsu, Y. (1999) The genus Reticulitermes(Isoptera: Rhinotermitidae) in Japan, withdescription of a new species. Entomol. Sci.,
2, 231–243.GG
Yamin, M. A. (1979) Flagellates of the orders
Trichomonadida
Kirby,
Oxymonadida
Grassè, and Hypermastigida Grassi & Foá
reported from lower termites (Isoptera families
Mastotermitidae,
Kalotermitidae,
Hodotermitidae, Termopsidae, Rhinotermitidae and Serritermitidae) and from thewood-feedingroach
Cryptocercus(Dictyoptera: Cryptocercidae). Sociobiology,
4, 1–119.GG