Jpn. J. Protozool. Vol. 46, No. 1, 2. (2013)21

Regular Article

Symbiotic protist communities in the termite
Coptotermes formosanus in Japan and a comparisonof community structures between workers andsoldiers
Osamu KITADE1*, Yoshinobu HAYASHI2 and Satoko NODA3
1

College of Science, Ibaraki University, Mito, Ibaraki 310-8512, Japan
School of Biological Sciences, The University of Sydney, Sydney, NSW 2006, Australia
3
Interdisciplinary Graduate School of Medicine and Engineering, University of Yamanashi,
Kofu, Yamanashi 400-8510, Japan
2

SUMMARY
Termites harbor a host species-specific symbiotic community composed of excavate protist
species in their digestive tracts. Although termite-protist symbiosis is well known, our knowledge
concerning the variations in symbiont species compositions and variations in community structures
among individuals, colonies and host castes is very limited. Here we collected 11 colonies of the termite
Coptotermes formosanus in the Western Japan Archipelago and investigated the variations in the
protist species compositions. We investigated the symbiont community structures in three host colonies,
and for the first time, variations of the community structures were compared between worker andsoldier castes. Three parabasalian species, Pseudotrichonympha grassii, Holomastigotoides hartmanni
and Spirotrichonympha leidyi, were observed in all examined host individuals in the 11 colonies. One
small trichomonadid species was found in hosts obtained from Iriomote Island and Okinawa Island. The
mean symbiont community size in the workers was 30–50 times larger than that of the soldiers, and thehost caste had a significant effect on the protist community structure. A principal component analysis
revealed that the community structure was significantly more variable in the soldiers compared to theworkers. Differences in food quality and community size between these termite castes probably affect the
protist community structure and its variations.
Key words: Symbiosis, Parabasalia, Oxymonadida, Protist community*Corresponding author
Tel/Fax: +81-29-228-8375
E-mail: kitade@mx.ibaraki.ac.jp

Received: 2 May 2013; Accepted: 19 July 2013.

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Symbiotic protist of Coptotermes formosanus

INTRODUCTION
The symbiosis between host termites andprotist symbionts living in the host hindgut is themost well known type of mutualism mediated bywood degradation (Cleveland, 1923; Inoue et al.,
2000; Brugerolle and Radek, 2006; Brune and
Ohkuma, 2011; Ohkuma and Brune, 2011). The
anaerobic symbionts are assigned to two excavategroups, Parabasalia and Preaxostyleta (Adl et al.,2012), and usually a termite individual possesses
more than one symbiont species in its hindgut
making up a symbiont community. The symbiont
species composition in a host termite shows strong
host-specificity at the species-to-species level(Kirby, 1934; Honigberg, 1970; Inoue et al., 2000;
Kitade, 2004; Kitade et al., 2012). However, sometimes a fraction of termite individuals in a colonyor, rarely, a whole colony lacks a particular protist
species (Honigberg, 1970). Except for a few
host genera (Reticulitermes: Mannesmann, 1974;
Kitade and Matsumoto, 1993; Cook and Gold,
1998, 1999; Lewis and Forschler, 2004; Coptotermes: Yoshimura et al., 1994; Hodotermopsis:
Kitade et al., 2012), variations in symbiont species
compositions between individuals or among fieldcolonies have not been investigated. In addition,
the existing knowledge of the variations in symbiont community structures — i.e., the ratios of thenumbers of individuals of each symbiont species— is very limited, although it is important for the
study of the communities from the evolutionary
viewpoint.
Termites are well known as a social insectgroup, and a colony of most termite species
consists of many individuals, including a king anda queen as the ―reproductive caste‖ and theiroffspring, workers, and soldiers as the ―neuter
caste‖. Although most taxonomic and ecologicalstudies of termite protists have been conductedusing the symbionts in workers (which areavailable in high numbers), earlier studies notedthat termite soldiers also possess hindgut protists(Cleveland, 1925; Honigberg, 1970). Most of thestudies that focused on the differences in thesymbiont species compositions and/or community
structures between workers and other castes havebeen carried out for Reticulitermes host species(Cook and Gold, 1998; Lewis and Forschler, 2004;
Shimada et al., 2013).
The workers, the major decomposers ofwood material in a termite colony, possess
well-developed, swollen hindgut rumens, whereas
the soldiers specialize in colony defense; theirhindgut volumes are smaller than those of theworkers. The hindgut protists in the soldiers arethus expected to be much less abundant than in theworkers, although these two castes share identical
microenvironments in a colony. Comparisons of
the symbiont community structures and its variations among the workers and soldiers fromdifferent colonies and localities will therefore
help us identify the factors (e.g., host caste or
microenvironment) that affect the protist community structures. However, for the termite symbiotic
protists, comparative analysis of the community
structure variations has not been carried out.
Here we investigated the variations insymbiont species compositions and community
structures of the termite species Coptotermes

Fig. 1. Soldier (left) and worker (right) of C. formosanus.
Scale bar = 5 mm.

Jpn. J. Protozool. Vol. 46, No. 1, 2. (2013)

23

Fig. 3. Sampling localities of C. formosanus nests in thisstudy.

Fig. 2. Three symbiotic protist species of C. formosanus.
a: Pseudotrichonympha grassii, b: Holomastigotoides
hartmanni, c: Spirotrichonympha leidyi. Scale bars = 50µm.

formosanus (Fig. 1), a notorious pest species foundthroughout East Asia including the southern andwestern parts of the Japan Archipelago. A maturecolony of this species reaches 1,000,000 in number(Morimoto, 2000). Koidzumi (1921) described
three symbiont species in C. formosanus: Pseudotrichonympha grassii, Holomastigotoides hartmanni, and Spirotrichonympha leidyi (Fig. 2)
assigned in the class Trichonymphea in the phylum
Parabasalia (Cepicka et al., 2010). Lai et al. (1983)
investigated the protist species compositions of

this species using multiple castes from a single
colony. However, their method of microscopic
observation without a coverslip was not proper forthe specific identification, and their results need tobe reconfirmed. Yoshimura et al. (1994) havereported seasonal variations of the symbiont
communities using laboratory and field colonies.
In the present study, we first examined variationsin the symbiont species compositions among individuals, colonies and localities of C. formosanus
using worker termites from six localities in Japan.
Then, using three host colonies, we investigatedcommunity structures and its variations to comparethem between the worker and soldier castes andamong different colonies.
MATERIALS AND METHODS
Sample Collection and Observation of the Protist
Community
We collected 11 partial host termite colonies
in six localities in the Japan Archipelago (Fig. 3):
one colony from Cape Irago, Aichi Prefecture(IRG1) in October 2012, one from Kainan, Wakayama Prefecture (KN1) in October 1995, threecolonies from Hikari, Yamaguchi Prefecture (HK1–3) in September 2012, one from Okinawa Island

24

Symbiotic protist of Coptotermes formosanus(OK1) in May 1995, three from Miyako Island(MY1–3) in June 1995, and two from Iriomote
Island (IRO1–2) in September 2011. The partial
colonies were brought back to the laboratory withnest wood and maintained individually in plastic
boxes at 22–25°C until the investigation of thetermites’ intestinal protists.
Before investigating the protist composition,
we prepared and observed protargol-stained specimens of the intestinal contents following themethod by Kitade et al. (1997). The morphologyof the specimens and living materials were carefully compared in order to identify the symbiont
species in the living state.
To investigate the protist species composition, we determined the presence or absence of
the above three protist species in five worker
termites from each of the 11 termite colonies. The
examined workers were in fifth- or later instars.
Other protist species were also checked if present.
For the examination, we pulled out the intestineof the living insect with forceps, dissected it ina drop of 0.45% NaCl solution, and suspended
the intestinal contents. The intestinal fluid wasthen put onto a glass slide, and living protists
were observed with a differential interference
microscope (BX-50, Olympus, Tokyo). The investigations were carried out within 20 days after thecollection of the colonies.
The community structures of the protists inworkers and soldiers were investigated using ahost colony collected in Cape Irago and Hikari(IRG1, HK1 and 2) within 10 days after thecollection. To examine the symbionts in a worker
termite, the gut contents of a worker were suspended in 30 µl of 0.45% NaCl solution. The fluid wasdispensed onto five Thoma counting chambers,
and we counted the protists in 3.6 µl, 3.6 µl, and0.125 µl of the solution for P. grassii, H. hartmanni, and S. leidyi, respectively. To examine the symbionts in soldiers, the gut contents were suspended
in 20 µl of NaCl solution, and we counted thethree protist species in 3.6 µl of the solution.

Statistical Analyses
We analyzed the factors affecting thesymbiont community size in a termite by a Poisson
regression analysis, using the data of the host colonies HK1, HK2 and IRG1. Host castes (worker,
soldier) and colonies were assigned as explanatory
factors. Similarly, to evaluate the factors (castes
and colonies) affecting the population ratio of
the symbiont species, arcsin-transformed population ratio data were subjected to a two-way
multivariate analysis of variance (MANOVA).
Similarity patterns of the protist community structure between the host individuals were assessed bya principal component analysis (PCA) using arcsin-transformed protist population ratio data of thethree above-named host colonies. The first principal component (PC1) scores were then subjected toF-tests to compare the degrees of community
structure variation between the castes and thecolonies. All of the analyses and tests were carriedout with R ver. 2.9.2 (The R project for statisticalcomputing, http://www.r-project.org/). A function―princomp2‖ provided by S. Aoki (http://aoki2.si.
gunma-u.ac.jp/R/pca.html) was used for the PCA.
RESULTS
The three parabasalian species reported by
Koidzumi (1921), P. grassii, H. hartmanni and
S. leidyi, were observed in all host individuals
examined in all 11 colonies (Table 1). One small
parabasalian species in the order Trichomonadida
was found in host individuals from Iriomote Island
and Okinawa Island; the occurrence rates of thisspecies were not high (0.25 to 0.75), compared tothe three species mentioned above (1.0 for all
examined colonies) and the other parabasaliansymbionts reported from lower termites (Kitade
and Matsumoto, 1993; Kitade et al., 2012). The
population size of the trichomonadid species in thehost individuals was also small (less than 100,
Kitade, O., unpublished data). The taxonomic status of this species should be studied in the future.

Jpn. J. Protozool. Vol. 46, No. 1, 2. (2013)

Table 1. No. of host workers that harbored each symbiotic protist species (N = 5)
Protist Species

Host
ColonyP. grassii

H. hartmanni

S. leidyi

Trichomonadidae sp.

IRG1

5

5

5

0

KN1

5

5

5

0

HK1

5

5

5

0

HK2

5

5

5

0

HK3

5

5

5

0

OK1

5

5

5

2

MY1

5

5

5

0

MY2

5

5

5

0

MY3

5

5

5

0

IRO1

5

5

5

1

IRO2

5

5

5

4

All three of the described parabasalid species
were found in termites from the three colonies
in which the symbiont community structure wasinvestigated. The occurrence rates of these species
in worker termites were 1.0 for all of the examinedcolonies, whereas one soldier each in colonies
HK2 and IRG1 lacked P. grassii, and one incolony HK2 lacked both P. grassii and S. leidyi.
The arithmetic mean symbiont community sizes of
the workers in each colony ranged from 8207 to
9207, which was approx. 30–50 times larger thanthe mean symbiont community sizes of the soldiers(range 156 to 229; Table 2). The Poisson regression analysis revealed that both host caste (z =−31.70, P < 0.001) and the host colony (HK1-25

HK2: z = 8.10, P < 0.001; HK1-IRG1: z = 11.13,
P < 0.001) had a significant effect on the community size.
In the worker termites, S. leidyi was the mostdominant in number, followed by H. hartmanni
and then P. grassii in all 11 colonies (Table 2).
The population size difference between the lattertwo species was small, and at the host individuallevel, P. grassii was more abundant than H. hartmanni in 4 of the 15 workers examined. In thesoldiers, the relative abundance of S. leidyi wasmarkedly low, and the relative abundance of thethree symbiont species varied among individuals.
The relative abundance of the three species was
significantly affected by the host caste (two-way
MANOVA, F = 28.28, df = 1, P < 0.001), but
it was not affected by the host colony (F = 0.97,
df = 2, P = 0.45) or the interaction between casteand colony (F = 0.65, df = 2, P = 0.69).
The 1st and 2nd principal components (PC1and PC2) obtained from the PCA based on therelative abundance data of the three protist species
explained 68.9% and 31.1% of the total variance,
respectively. The scatterplot of the PC scores ofeach termite individual shows clear aggregationsof workers (Fig. 4), indicating that the workers had
similar symbiont community structures. In contrast, the variation in PC scores was larger in thesoldiers, showing greater variations in the symbiont community structures. Individuals in the same

Table 2. Mean no. (SE) of estimated symbiotic protist species in workers (N = 5) and soldiers (N = 5) of three hostcolonies
Host Caste /ColonyProtist Species
Total

P. grassii

H. hartmanni

S. leidyi

IRG1

563 (74)580 (82)

8,060 (1,420)HK1495 (197)

532 (130)

7,870 (2,050)

8,900 (2,200)

HK2

193 (37)382 (117)

7,630 (1,470)

8,210 (1,520)

IRG1

74 (43)142 (63)

82 (16)299 (100)HK1

31 (15)83 (64)64 (42)179 (59)HK2

41 (6)

33 (9)133 (87)

207 (85)

Worker9,210 (1,310)

Soldier

26

Symbiotic protist of Coptotermes formosanusFig. 4. Scatterplot of principal component scores (PC1
and 2) of each termite individuals based on the protist
community structures. Different symbols and colors indicate castes (worker and soldier) and colonies (IRG1 andHK1-2).

colony did not exhibit a clear tendency to aggregate. These results correspond well to the results of
the MANOVA. An F-test showed that the variation in the soldier PC1 scores was significantly
larger than that of the workers (F = 0.10, df = 14,
P < 0.001). Host colony did not have a significant
effect on the variances of PC1 scores (F-test with
Bonferroni correction, HK1-HK2, F = 0.63, df = 9,
P > 0.05; HK1-IRG1, F = 1.17, df = 9, P > 0.05;
HK2-IRG1, F = 1.85, df = 9, P > 0.05).
DISCUSSION
The high occurrence rates of the threedescribed symbiotic protist species in C. formosanus workers observed in the present study are
similar to those of hindgut protists of other East
Asian termite taxa, e.g., Reticulitermes spp.
(Kitade et al., 1993) and Hodotermopsis sjostedti(Kitade et al., 2012), and perhaps with those oflower termites in general. The unusual, lower
infection rate of the other tiny trichomonadid

species, together with its small population size,
suggest that this species is an opportunistic parasite and does not take part in wood degradation.
Except for this species, the symbiont species
composition of the worker hindgut community
identified in the present study is identical to that of
the C. formosanus in Taiwan (Koidzumi, 1921)
and Miyazaki, Japan (Yoshimura et al., 1993,
1994). The host-species specificity is the generaltrend of termite protist communities (Honigberg,
1970; Inoue et al., 2000). Symbiont fauna composed of species belonging to Pseudotrichonympha, Holomastigotoides, and Spirotrichonympha
are a characteristic of Coptotermes hosts (Yamin,
1979; Kitade and Matsumoto, 1998) and Pseudotrichonympha, at least, was inherited from thecommon ancestor of the host family Rhinotermitidae (Noda et al., 2007).
The community size in the worker termites
estimated for the three colonies (IRG1, HK1 and
2) did not show remarkable differences from thatof three field colonies in Miyazaki (mean 7,280,
range 3,750–11,140, n = 15 individuals) investigated by Yoshimura et al. (1994). The population
size of H. hartmanni (382–580) was considerably
smaller than that of the Miyazaki colonies (mean2,160, range 1,160–3,350, n = 15 individuals),possibly because our investigation was carried out
from late October to late November, while thelatter data were collected year-round except in mid-winter. In laboratory colonies of the termite Reticulitermes speratus, the breeding temperature
affected the symbiont community structures(Takayanagi, M. and Nemoto, M., unpublisheddata).
In Reticulitermes hosts, the relative symbiont
species abundance was similar between workers
and soldiers (Cook and Gold 1998; Lewis andForschler 2004). Here we first indicated clear differences of the symbiont community structures
between these castes of C. formosanus. The resultsof the MANOVA indicated that the differences inhost-symbiont relationships between these castes

Jpn. J. Protozool. Vol. 46, No. 1, 2. (2013)

had stronger effects on the community structure
than the differences in non-biological physicalenvironments between the colonies. It is likely thatthe host caste affects not only the carrying capacity
for the populations of community members but
also the quality of their microhabitats. Workers
can take undegraded wood fragments into theirguts by masticating the wood and digesting it, but
the soldiers depend on partially degraded wood
received from nestmate workers as their food
(Cleveland 1925; Cook and Gold 1998), throughproctodeal and stomodeal trophallaxis. These differences in food sources would be expected tochange the community structure of the hindgut
symbionts.
Yoshimura et al. (1993) showed that P.
grassii disappeared quickly when C. formosanus
workers were fed low-molecular-weight cellulose.
The absence of this symbiont species in three ofthe 15 soldiers examined in our study may be theresult of a shortage of undegraded cellulose in thesoldiers’ food. To test this idea, comparisonsshould be conducted of the symbiont community
structures between young and old workers, which
possess hindgut lumens with different sizes
although they have similar food sources.
To the best of our knowledge, this study isthe first to reveal that the variation in protist
species compositions and community structures
are much larger in termite soldiers than workers.
The generality of this finding should be further
tested using multiple host species. The differencein the community stability between castes, whichshare the same physical environment in a host nest,
may reflect the community size, i.e., the population size of each component species. In general, an
organism with a small population size is likely to
be extinguished (MacArthur and Wilson, 1967).
Our recent study (Kitade et al., 2012) showed thatthe variations in species compositions of symbiotic
protist communities were much smaller in a hosttermite with a larger body size and symbiont
community size, Hodotermopsis sjostedti, than in27

host termites with smaller body and community
sizes, Reticulitermes spp., even though the twohost groups are distributed sympatrically.
ACKNOWLEDGEMENTS
We thank Dr. M. Hojo for providing termitecolonies and K. Urayama for help in termite
sampling. This work was supported by Grants-inAid for Scientific Research (Nos. 21310024,
22370008 to OK, No. 23657013 to OK and SN).
REFERENCES
Adl, S. M., Simpson, A. G. B., Lane, C. E., Lukes,
J., Bass, D., Bowser, S. S., Brown M. W.,
Burki, F., Dunthorn, M., Hample V., Heiss,A., Hoppenrath, M., Lara, E., Gall, L. L.,
Lynn, D., McManus, H., Mitchel, E. A. D.,
Mozley-Standridge, S. E., Parfrey, L. W.,
Pawlowski, J., Rueckert, S., Shadwick, L.,
Schoch, C. L., Smirnov, A. and Spiegel, F.
W. (2012) The revised classification of eukaryotes. J. Eukaryot. Microbiol., 59, 429–
493.
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.
Cepicka, I., Hampl, V. and Kulda, J. (2010) Critical Taxonomic revision of parabasalids withdescription of one new genus and three new
species. Protist, 161, 400–433.
Cleveland, L. R. (1923) Symbiosis between termites and their intestinal protozoa. Proc.
Natl. Acad. Sci. U S A, 9, 424–428.

28

Symbiotic protist of Coptotermes formosanus

Cleveland, L. R. (1925) The feeding habit of termite castes and its relation to their intestinal
flagellates. Biol. Bull., 48, 295–308.
Cook, T. J. and Gold, R. E. G. (1998) Organizationof the symbiotic flagellate community inthree castes of the Eastern subterranean termite, Reticulitermes flavipes. Sociobiology,
31, 25–69.
Cook, T. J. and Gold, R. E. G. (1999) Symbiotic
hindgut flagellate communities of the subterranean termites Reticulitermes virginicus andReticulitermes flavipes in Texas (Isoptera:
Rhinotermitidae). Sociobiology, 34, 533–
543.
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.
Inoue, T., Kitade, O., Yoshimura, T. andYamaoka, I. (2000) Symbiotic associations
with protists. In: Termites: Evolution, Sociality, Symbioses, Ecology. Abe, T., Bignell,
D. E., and Higashi, M. (eds.). Kluwer, Dordrechit, pp. 275–288.
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., Hayashi, Y., Takatsuto, K. and Matsumoto, T. (2012) Variation and diversity ofsymbiotic protist composition in the dampwood termite Hodotermopsis sjoestedti. Jpn.
J. Protozool., 45, 29–36.
Kitade, O., Maeyama, T. and Matsumoto, T.
(1997) Establishment of symbiotic flagellatefauna of Hodotermopsis (Isoptera: Termopsidae). Sociobiology, 30, 161–167.

Kitade, O. and Matsumoto, T. (1993) Symbiotic
protistan faunae of Reticulitermes (Isoptera:
Rhinotermitedae) in the Japan Archipelago.
Sociobiology, 23, 135–153.
Kitade, O. and Matsumoto, T. (1998) Characteristics of the symbiotic flagellate composition
within the termite family Rhinotermitidae(Isoptera). Symbiosis, 25, 271–278.
Koidzumi, M. (1921) Studies on the intestinal protozoa found in the termites of Japan. Parasitology, 13, 235–309.
Lai, P. Y., Tamashiro, M. and Fujii, J. K. (1983)
Abundance and distribution of the three species of symbiotic protozoa in the hindgut of
Coptotermes formosanus. Proc. Hawaii. Ent.
Soc. 24, 271–276.
Lewis, J. L. and Forschler, B. T. (2004) Protist
communities from four castes and three species of Reticulitermes (Isoptera: Rhinotermitidae). Ann. Ent. Soc. Am., 97, 1242–
1251.
MacArthur, R. H. and Wilson, E. O. (1967) The
theory of Island Biogeography. Princeton
University Press, Princeton.
Mannesmann, R. (1974) Qualitative und quantitative Unterschung der Darmfaunen mehrerer
Populationen von Reticulitermes (Isopt., Rhinotermitidae). Z. ang. Ent. 76, 86–97.
Morimoto, K. (2000) Termites. In: Termites andcontrol policy. The Japan Termite Control
Association (ed.). The Japan Termite Control
Association, Tokyo, pp. 1–126 (in Japanese).
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 Ter-

Jpn. J. Protozool. Vol. 46, No. 1, 2. (2013)

mites: A Modern Synthesis. Bignell, E. D.,
Roisin, Y. and Lo, N. (eds.). Springer, Dordrechit Heiderberg, pp. 413–438.
Shimada, K., Lo, N., Kitade, O., Wakui, A. andMaekawa, K. (2013) Cellulolytic protist
numbers rise and fall dramatically in termite
queens and kings during colony foundation.
Eukaryot. Cell, 2, 545–550.
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-feeding roach Cryptocercus (Dictyop-

29

tera: Cryptocercidae). Sociobiology, 4, 1–
119.
Yoshimura, T., Azuma, J.-I., Tsunoda, K. andTakahashi, M. (1993) Cellulose metabolismof the symbiotic protozoa in termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae): I. Effect of degree of polymerization of cellulose. Mokuzai Gakkaishi, 39,
221–226.
Yoshimura, T., Tsunoda, K. and Takahashi, M.
(1994) Cellulose metabolism of the symbiotic protozoa in termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae):IV. Seasonal changes of the protozoan fauna
and its relation to wood-attacking activity.
Mokuzai Gakkaishi, 40, 853–859.