Ecological Research (1998) 13, 377±387

Use of carbon and nitrogen isotope ratios in termite

research
ICHIRO TAYASU*
Laboratory of Forest Ecology, Division of Environmental Science and Technology, Graduate School of
Agriculture, Kyoto University, Kyoto 606±8502, Japan

In this paper, I review carbon and nitrogen isotopic (natural abundance levels) studies of termites. The
carbon isotope ratio of CH4 emitted from termites, together with the emission rates of CO2, CH4 and
H2, showed several trends corresponding to the kinds of symbiotic microbes and feeding habits. The
fraction of methane oxidized in the nest structure was estimated by comparing carbon isotope ratio of
CH4 emitted from the nest with that produced by termites in the nest. Symbiotic nitrogen ®xation in
the gut of termites has been shown to have a signi®cant contribution to the nitrogen economy in some
wood-feeding termites. The carbon isotope ratio distinguishes between C4 from C3 plants, and the
fractional contribution of grass in the diet can thereby be estimated. The carbon and nitrogen isotope
ratios in termites are discernible among soil-feeders, fungus cultivators and wood-feeders. Wood/soil-
interface feeders have intermediate values between wood- and soil-feeders, and thus carbon and
nitrogen stable isotope ratios are assumed to characterize the degree of humi®cation of the material
consumed by termites. It is suggested that carbon and nitrogen isotope ratios are useful indicators of
the functional position of termites in the decomposition process. A similar isotope pattern has been
obtained in earthworms, suggesting that isotope signatures might be useful parameters in investigating
detritivorous animals in general.

Key words: decomposition; detritivore; humi¢cation; Isoptera; trophic enrichment.

INTRODUCTION where R in d13C and d15N denotes 13C/12C and

Stable carbon and nitrogen isotope ratios have
been widely applied in ecological studies. Natural
abundance isotopic signatures can be used to ®nd
patterns and mechanisms at the single organism
level as well as to trace food webs, understand
palaeodiets and follow whole ecosystem cycling
in both terrestrial and marine ecosystems (Pe-
terson & Fry 1987; Wada et al. 1991). Since
variation in stable isotope ratios is so small, the
natural abundance of 13C and 15N is expressed
per mil (&) deviation from international stan-
dards, as de®ned by the following equation:
d13 C; d15 N ˆ …Rsample =Rstandard ÿ 1†  1000;
*Email: <tayasu@kais.kyoto-u.ac.jp>
Received 14 January 1998.
Accepted 3 March 1998.
15
N/14N, respectively. Pee Dee Belemnite and
atmospheric nitrogen are used as the standards.
In this paper, I use the term `trophic enrichment'
as the difference in isotope ratio between an
animal and its putative diet, expressed as DdX
( ˆ dXanimalÿdXdiet, where dX denotes d13C and
d15N).
The carbon isotope ratio has been used as a
dietary indicator. In a review paper, Deines
(1980) reported that d13C values are separated by
bimodal distribution (i.e. ÿ20 to ÿ35& for C3
plants [woody forms] and ÿ9 to ÿ14& for C4
plants [grasses]). In contrast, trophic enrichment
of carbon isotopes is small, mostly within 1&
(DeNiro & Epstein 1978; Fry & Sherr 1984).
Therefore, it has been possible to characterize the
carbon ¯ow of a food chain based on woody
and/or herbaceous materials.
Trophic enrichment of nitrogen isotopes is
usually positive, averaging 3.4& (DeNiro &
378 I. Tayasu
Epstein 1981; Minagawa & Wada 1984). Since the
ratio is assumed to re¯ect the trophic position,
the nitrogen isotope ratio has been used as a food
web indicator for animals in various ecosystems
(Schoeninger & DeNiro 1984; Ambrose & De
Niro 1986; Sealy et al. 1987; Wada et al. 1987a,
1987b; Fry 1988; Hobson & Welch 1992). The
excretion of low d15N as urea or ammonium
seems to account for the 15N-enriched nitrogen
that is incorporated into animal tissues, presum-
ably due to isotopic processes occurring during
amino acid metabolism in the reaction of urea
cycle (Steele & Daniel 1978; Minagawa & Wada
1984). Several authors have reported some
modi®cation of the relationships. For example, a
slightly smaller enrichment (Dd15N » 2.4&) has
been reported in birds (Mizutani et al. 1991). In
another case, a negative correlation was found
between d15N and the annual amount of pre-
cipitation for a variety of different species in
southern Africa (Heaton et al. 1986; Sealy et al.
1987). Drought-tolerant species (mostly brows-
ers) were further found to have d15N values 2±
4& higher than obligate drinkers (mostly grazers;
Ambrose & DeNiro 1986), but the tendency to
high d15N occurred only in combination with a
high C4 diet (Cormie & Schwarcz 1996). They
suggested that an increase of d15N might result
from combined effects from excretion of con-
centrated urine (to conserve water) and increased
internal recycling of nitrogen (to conserve nitro-
gen), corresponding with the consumption of
grasses (Cormie & Schwarcz 1996). Recent pa-
pers repeatedly have called for reconsideration of
the assumption and appealed for laboratory ex-
periments to determine the trophic enrichment in
reference to food quality (Cormie & Schwarcz
1996; Gannes et al. 1997).
Termites (Isoptera) are dominant soil animals in
the tropics, which feed on a range of organic
materials in the decomposition process. They are
divided into two large groups: the lower termites
(six families) and the higher termites (one family,
Termitidae; Wood & Johnson 1986). The lower
termites, which harbor associated protozoa in
their gut, mainly consume wood, whereas the
higher termites that lack protozoa and constitute
75% of all species, consume various kinds of dead
organic material including wood, dry grass, bark,
lichens, fallen leaves and soil (Wood & Sands
1978). Their highly developed social organization
and symbiosis with microorganisms have per-
mitted remarkable developments in adaptive ra-
diation of their feeding habits (Higashi & Abe
1996).
Fungus-growing termites (subfamily Macro-
termitinae), which cultivate symbiotic fungi in the
nest and feed on the fungus garden (comb), are a
successful group especially in dry areas of Africa
and Asia. Soil-feeding is also widely represented
with 51% of all genera of the Isoptera and 62%
of the Termitidae (Noirot 1992) occurring in
three subfamilies: Apicotermitinae, Termitinae
and Nasutitermitinae. The majority of soil-feed-
ing species belong to two subfamilies (Apico-
termitinae and Termitinae) and constitute a major
trend in higher termite diversi®cation (Wood &
Johnson 1986; Noirot 1992; Bignell 1994). Al-
though soil-feeding represents a major trophic
habit within the Isoptera, it is still unclear which
components in the soil organic matter are in-
volved during ingestion. There is a conspicuous
variation among soil-feeding species in gut mor-
phology and pH regimes, suggesting that the
biochemistry of digestion and/or the intestinal
micro¯ora may vary among species (Bignell &
Eggleton 1995). In addition, a number of higher
termites feed on very highly decayed wood,
which is in an advanced stage of humi®cation.
These are currently known as wood/soil-inter-
face feeders (Eggleton et al. 1995).
This paper reviews the literature relating to
stable isotope studies of termite-symbiont sys-
tems with particular emphasis on carbon and
nitrogen isotope ratios and suggests a possibility
of application to general detritivorous animals.
SYMBIOSIS WITH MICROORGANISMS
Methane and acetate production
Methane production by termites is an important
source in the global budget (Cicerone & Oremland
1988), but the absolute contribution is dif®cult to
quantify. In order to explain the variation in
methane emission rates between species and col-
onies (Bignell et al. 1997), it is important to ex-
amine pattern and mechanisms of hydrogen sink in
the intestinal process. Brauman et al. (1992)

pointed out that acetogenesis occurred in wood-
feeders, whereas methanogenesis is favored in
fungus-growers and soil-feeders. Sugimoto et al.
(1998) compared methane and hydrogen produc-
tion among various kinds of feeding habit. They
pointed out that the variation in emission rates in
lower termites is extremely large, ranging from the
detectable limit to a very high level. In higher ter-
mites, they also suggested that two types of sym-
biosis, wood-feeding and soil-feeding, have
different ef®ciencies of interspecies transfer of H2.
Although nothing is known of the mechanisms,
these differences may relate to the observed d13C
of emitted CH4: greater than ÿ80& for lower
termites, ÿ100 to ÿ82& for higher termites ex-
cept for Macrotermes, and ÿ79 to ÿ41& for Mac-
rotermes (fungus-growing termites). The CH4
emitted from termites is oxidized by methane-
oxidizing bacteria inhabiting the nest material
(Bignell et al. 1997). Sugimoto et al. (in press) esti-
mated the emission factor (17±47%), de®ned as
proportion of CH4 emitted from the nest mound
to CH4 produced by termites in the mound, by
using fractionation factor of methane oxidation by
nests, which was obtained by the incubation ex-
periments. Using this factor, they concluded that
the contribution of termites to the global methane
budget is reduced to 0.3±1.3% of the total source.
Anaerobic acetogenesis from CO2/H2 in the
gut possibly lowers d13C of termites (A. Sugi-
moto & I. Tayasu, pers. comm.). In the gut of
termites, cellulose is decomposed into glucose
and then fermented into CO2, H2 and acetate.
The CO2 and H2 produced are converted into
CH4 and/or acetate by bacteria in the hindgut.
Acetate is absorbed and utilized by the host
termite as an energy source (Odelson & Breznak
1983). Since isotope fractionation during CH4
(Krzycki et al. 1987) and acetate (Gelwicks et al.
1989) production is very large, the d13C value of
the CH4 and acetate produced is 45±60& lower
than that of CO2. The produced CH4 leaves the
termite body, whereas acetate is absorbed by
termites. This difference may affect d13C of
termites (A. Sugimoto & I. Tayasu, pers.
comm.), especially in wood-feeders where aceto-
genesis is predominant (Brauman et al. 1992).
This is consistent with the fact that the Dd13C of
wood-feeding species was negative (Tayasu et al.
1997).
Stable isotopic studies of termites 379
Symbiosis and nitrogen economy
Xylophagous termites must cope with the low
levels of nitrogen in wood. Tayasu et al. (1994)
have shown that the fraction of nitrogen derived
from the atmosphere (%Ndfa) is given by the
following equation (two source model),
ÿ 15

d Nwood ‡ Ddig ÿ d15 Ntermite
%Ndfa ˆ ÿ 15
 100
d Nwood ‡ Ddig ÿ Dfix
where Ddig (d15Ntermite ÿ d15Nwood) is the isotope
discrimination during the digestion of wood, D®x
is that occurring as a result of nitrogen ®xation,
and d15Ntermite is the isotope ratio of the termite.
This expression is analogous to the widely ac-
cepted estimation of the contribution of atmo-
spheric nitrogen in nitrogen-®xing plants (Shearer
& Kohl 1986). Tayasu et al. (1994) estimated that
at least 30±60% of the nitrogen present in workers
of Neotermes koshuensis came from the atmosphere,
with the assumption of Ddig > 0 and
ÿ2 < D®x < 0. This method is useful in obtaining
an in situ estimation of nitrogen ®xation in ter-
mites, which are very sensitive to manipulation
(Prestwich & Bentley 1981). However, (i) Ddig and
D®x should be con®rmed experimentally before
being applied in general and (ii) this method can be
used only when the dietary material is identi®ed.
Although there are uncertainties in the parame-
terization, it is suggested that nitrogen ®xation is
an important source of nitrogen for wood-feeding
one-piece type (sensu Abe 1987; termites that
consume only the nesting wood) termites, while
not important in other termite species especially in
soil-feeding termites (Tayasu 1997).
Nitrogen recycling is another process which
minimizes nitrogen de®ciency problem in ter-
mites. Termites store uric acid in their body fat
tissue (Potrikus & Breznak 1981). Since uric acid-
degrading bacteria are found in the gut of ter-
mites, they may recycle stored uric acid though
necrophagy and cannibalism (Slaytor & Chappell
1994). If they recycle nitrogen through uric acid
preservation, the Dd15N value might be different
from organisms that are unable to recycle meta-
bolic wastes.
A study of ruminants suggested that an intestinal
interaction may in¯uence trophic enrichment.
Sealy et al. (1987) suggested that d15N might be
enriched if nitrogen was recycled among microbes
380 I. Tayasu

in the rumen. Sutoh et al. (1987) reported 2.8±

5.6& enrichment of d15N between protozoa and
bacteria, where the former were assumed to digest
the latter, in the rumen of cattle.

FEEDING HABITS OF TERMITES

Dietary preferences
Boutton et al. (1983) introduced the stable isotope
technique to termite research and successfully
characterized dietary preference of a fungus-
growing termite (Macrotermes michaelseni ) between
woody and herbaceous materials. Lepage et al.
(1993) examined the d13C of fungus combs and
found a seasonal change in feeding habit. They also
pointed out the dominance of C3 plants of diet in
fungus-growing termites (Macrotermitinae), much
higher than the contribution of total aboveground
production. They suggested that the nitrogen
content could explain the preference for woody
(C3) litter. Soil modi®cation through termite-
feeding can also be studied by the d13C relationship
between termites and their nests if there is both C3
and C4 vegetation in a habitat (Spain & Reddell
1996; Tayasu et al. 1998).
Fungus comb is 3±4& enriched in d13C relative
to the stored litter in the nest, thereby explaining
13
C enrichment in termites compared with wood
feeders (Tayasu 1997). The enrichment of d13C in
the symbiotic fungi is consistent with the fact that
decomposing fungi are enriched by 4& relative to
their substances in wood (Gleixner et al. 1993).
Relationships in d15N among castes in the fungus-
grower are complicated (Tayasu 1997), probably
due to the highly complicated nutritional caste
differentiation, including division of labour
(Badertscher et al. 1983).
From wood- to soil-feeding termites
The idea of trophic enrichment is mainly based on
the species in the grazing food chain (Minagawa &
Wada 1984); however, recent studies have sug-
gested that the trophic enrichment is different at
the bottom of the detritus food chain. Tayasu et al.
(1997, 1998) found that the d15N of termite tissues
was gradually enriched along a spectrum of species
representing a trophic gradient from wood- to soil-
Fig. 1. Plot of mean d15N against mean d13C for the
tissues of worker caste termites, collected in a typical C3
plant-dominated forest in Cameroon. Soil-feeding spe-
cies (colonies of eight species, d) cluster in the top right
and colonies of the wood-feeding Microcerotermes parvus
(n) cluster in the lower left. Others include: h, wood-
feeders, wood/soil-interface feeders; and m, the fungus-
grower Acanthoterms acanthothorax. The isotopic relation-
ships of termites, which are categorized as wood-feeders,
soil-feeders and fungus-growers, are represented sche-
matically in the ®gure as large circles (Tayasu et al. 1997).
feeding, which was consistent with the results of
gut content analysis (Sleaford et al. 1996). They
proposed d15N as a possible indicator of the
functional position of feeding habit in the humi-
®cation process. The wide ranges of carbon and
nitrogen isotope ratios suggest a high diversity of
nutrient acquisition in termites: from plant debris
in the wood to humus in the soil (Fig. 1; Tayasu
et al. 1997). Carbon and nitrogen isotope ratios
relating to the feeding habit appear to be inde-
pendent of phylogenetic relationships and might
also be applicable to general detritivores (Tayasu
et al. 1998).
Trophic enrichment in deposit feeders and
insects
Trophic enrichment of nitrogen isotopes has
been reported for several detritivorous animals.
Kikuchi and Wada (1996) reported 5 ‹ 1& for
the deposit feeder Neanthes japonica (Polychaeta,

Annelida). They suggested that large trophic en-
richment may result from selective assimilation of
bacterial N or bacterially altered compounds in
the diet. Owens and Law (1989) also suggested
that detrital organic matter is gradually enriched
in d15N due to microbial transformation of nitro-
gen in sediments. In contrast, Hobson and Welch
(1995) reported a small enrichment in d15N in
detritivorous chironomids. They speculated
that the diet may be comprised of an unknown
fraction of isotopically light nitrogen including
bacteria which utilize nitrogen depleted in d15N
as part of microbial loop. It is obvious that more
isotopic investigation is required for deposit-
feeders.
Some papers have suggested that 3.4& of
Dd15N is not necessarily appropriate for insects
due to the difference in physiology, although
Dd15N is still non-negative (e.g. DeNiro & Ep-
stein 1981). For example, Scrimgeour et al. (1995)
observed unexpectedly elevated d15N values
(Dd15N » 10&) in adult raspberry beetles (By-
turus tomentosus) collected shortly after emergence
from overwintering sites. d15N of feeding larvae
was, however, close to that of the food plant
(Dd15N ˆ 1±2&), red raspberry (Rubus idaeus).
The elevated d15N values in overwintered larvae
and adults of the raspberry beetle were consistent
with an hypothesis of extensive amino acid ni-
trogen recycling during prolonged fasting (Hob-
son et al. 1993).
STUDY OF DETRITIVOROUS ANIMALS
Soil organic matter
15
N natural abundance of organic N and inor-
ganic N in forest ecosystems vary in accordance
with pedogenic process (Nadelhoffer & Fry 1994;
Handley & Scrimgeour 1997; HoÈgberg 1997).
Nitrogen in plant tissue typically has d15N values
ranging from about ÿ5±2& (Fry 1991) but is
dependent on local nitrogen cycling. For exam-
ple, ÿ10& of d15N was reported for foliage in
very young soils in Hawaiian forests (Vitousek
et al. 1989) and +10& in foliage of desert
woodland (Virginia et al. 1989). Nitrogen input to
the soil is mainly by nitrate and ammonia depo-
sition and by biological nitrogen ®xation. d15N of
Stable isotopic studies of termites 381
ammonia and nitrate are depleted (typically ÿ10±
0&) on average, and those of nitrogen by N2-
®xation are slightly negative (typically ÿ2±0&;
Yoneyama 1996).
In general, tree tissues and fresh litter are
slightly depleted in 15N relative to soils and d15N
values increase with depth in soil pro®les to
about +8 ‹ 2& at a depth of 20±40 cm (LeÂtolle
1980; Ledgard et al. 1984; Wada et al. 1984;
Nadelhoffer & Fry 1994). Ammonia volatilization
(HoÈgberg 1990) and denitri®cation (Mariotti et al.
1981, 1982, 1988) accounts for the evolution of
d15N in the decomposition process. Experiments
with incorporated plant litter con®rmed the in-
crease of the d15N value of soils, caused by the
partial loss of 15N-depleted volatile N com-
pounds (amine and ammonia, Turner & Berger-
sen 1983) and by leaching of 15N-depleted
compounds including by denitri®cation
(Nadelhoffer & Fry 1988). These processes occur
in relatively short time courses and are followed
by the recalcitrant phase caused by microbial
and/or chemical stabilization (HoÈgberg 1997).
Various physicochemical approaches have been
applied in separating the properties of complex
soil organic matter.
Particle-size fractionation allows the separa-
tion, in a ®rst approximation, of three types of
organic compartments: (i) the plant debris frac-
tion (>20 lm); (ii) the organo-silt complex
(2±20 lm) composed of humi®ed plant and
fungi debris and of very stable microaggregates;
and (iii) the organoclay fraction (<2 lm) domi-
nated by amorphous organic matter of partly
microbial origin (Feller et al. 1996). Tiessen et al.
(1984) studied the natural nitrogen isotope ratio
of soil organic matter associated with organo-
mineral particle size fractions of two cultivated
and two native grassland soils. They reported
that ®ne clay (<0.2 lm) had about 7& more
d15N than total nitrogen. The technique was
based on soil fractionation by ultrasoni®cation
and centrifugation/decantation (Anderson et al.
1981; Tiessen & Stewart 1983; Ledgard et al.
1984; Balesdent et al. 1991). Mineralization of
relatively 15N-depleted nitrogen and reassimila-
tion of relatively 15N-enriched nitrogen during
microbial N turnover may result in 15N enrich-
ment in acid hydrolysable fractions, representing
labile N (proteinous) materials, compared to
382 I. Tayasu
non-hydrolysable fractions resistant to microbial
cycles (Cheng et al. 1964; Selles et al. 1984). The
mechanisms and fractionation of 15N along the
pedogenic process is, however, scarcely known
(Handley & Scrimgeour 1997).
Factors controlling d13 C and d15 N of termites
The d13C and d15N of termites can be utilized in
identifying feeding habits of termites (Tayasu
1997; Tayasu et al. 1997, 1998). In comparing
values between different habitats, d13C and d15N
of the background (nesting wood, nest construct
and soil organic matter) must also be considered.
Feeding habits of termites are schematically
shown in Fig. 1, which is superimposed on the
empirical data obtained from Cameroon (Tayasu
et al. 1997), where C3 plants dominated
(d15N ˆ 3±6&; d13C ˆ ÿ29±ÿ27& in wood
tissue). d13C and d15N of wood-feeders are lower
and similar to those of woods (not shown).
Fungus-growing termites are higher in d13C but
similar in d15N compared to the levels in stored
food. Soil-feeders are, however, high in both d13C
and d15N. In fact, wood/soil-interface feeders
have intermediate values between wood- and soil-
feeders, possibly representing a trophic gradient
from wood- to soil-feeding (Fig. 1). Based on the
literature mentioned above, factors which may
have an affect on the isotope ratios are as follows.
The d13C of termite tissue is determined by
three main factors; (i) the ratio of C4
(d13C ˆ ÿ13&) to C3 (d13C ˆ ÿ28&; typical
value from Peterson & Fry 1987) plants of food
source (Boutton et al. 1983; Lepage et al. 1993);
(ii) the ratio of assimilation of cellulose to mi-
crobial-mediated substances (enrichment up to
3±4&; Tayasu et al. 1997, 1998); and (iii) aceto-
genesis to methanogenesis ratio (ranges are not
determined; A. Sugimoto & I. Tayasu, pers.
comm.). In contrast, d15N value is determined by
another set of factors: (i) the ratio of assimilation
of plant nitrogen (presumably cytoplasm-N in
plant material) to microbially mediated (including
intestinal microbes) substances in soil (presum-
ably microbially concentrated N and polyphenol-
bound N; enrichment up to 8.8&; Tayasu et al.
1997); (ii) nitrogen ®xation in the gut (slightly
negative discrimination; Tayasu et al. 1994); and
(iii) trophallaxis among castes (not uniform;
Tayasu 1997; Tayasu et al. 1997). The carbon-to-
nitrogen ratio of diets is very different between
wood tissue and soil organic matter; part of these
factors may be considered as co-occurring effect.
Other factors, which might also in¯uence d15N
of termites, are as follows. The extremely alkaline
conditions present in termite guts may allow the
decomposition of recalcitrant materials (Bignell
1994; Bignell & Eggleton 1995; Brune & KuÈhl
1996). When soil particles containing protein are
consumed by termites (Bignell 1994), one might
therefore expect the enrichment of d15N to oc-
cur. HoÈgberg et al. (1996) demonstrated that
fungal sheath stripped from roots colonized by
ectomycorrhiza were 2.4±6.4& enriched in d15N
relative to the remaining root core. Taylor et al.
(1997) also reported that proteins and amino
acids were enriched by 9.7 ‹ 0.4& relative to
chitin in fruit bodies of ectomycorrhizal fungi.
These studies may be important for the estima-
tion of fungal contribution to the diet of termites,
especially to the soil-feeding species. Nitrogen
emitted as N2O might enrich d15N in the termite
body by the emission of N2O, which has lighter
d15N in general (reviewed by Wada & Ueda
1996). N2O production of termites is very low
(Khalil et al. 1990) in wood-feeders, but has not
been determined in soil-feeders.
Termites and earthworms as macrofauna
Termites and earthworms are classi®ed as
macrofauna (Lavelle 1997), and they have been
described by some researchers as ecosystem
engineers for their ability to profoundly affect the
soil structure and hence major soil processes via
the structures that they build (Jones et al. 1994).
Termites are abundant in the tropics and it is
well known that their activity in¯uences the
chemical properties of soil (e.g. Coventry et al.
1988). However, the isotopic signature of ter-
mites in plant nutrition has not been demon-
strated except for the tree species Combretum molle,
which is found exclusively in association with
termite mounds in African miombo woodland
(HoÈgberg & Alexander 1995). They reported that
the species was more than 3& enriched in d15N
relative to other non-N2-®xing species.
Finally, studies on earthworms are compared
with those of termites. Earthworms are divided

Fig. 2. d13C and d15N plot in plants and earthworms
from a wheat (solid symbols) and a wheat-clover (hollow
symbols) ®eld. Aporrectodea caliginosa, Allolobophora chloro-
tica and Aporrectodea rosea, endogeic species; Aporrectodea
longa, anecic species; Lumbricus spp., epigeic/anecic spe-
cies. d and s, A. caliginosa/A. chlorotica; j and h,
Lumbricus spp.; r and e, A. longa; ,, A. rosea; and ,
wheat; , white clover (Schmidt et al. 1997).
into three ecological categories (Lavelle 1997).
Epigeic species are small, pigmented and live in
the litter, while anecic species are larger, partly
pigmented species, and live in deep soil burrows.
Both groups feed on litter. Endogeic species,
however, are medium-sized, unpigmented and
live in temporary soil channels; they have a geo-
phagous diet. Martin et al. (1992b) pointed out
that young Millsonia anomala (geophagous tropical
earthworm) were able to assimilate young organic
matter (fresh organic matter, coarse soil organic
matter) as well as ®ne soil organic matter using
d13C incorporation. They separated soil into ®ve
fractions (250±2000, 100±250, 50±100, 20±50,
and 0±20 lm) in C4-dominated vegetation and
substituted each fraction for that of C3-domi-
nated soil. Martin & Lavelle (1992) and Martin
et al. (1992a) showed that earthworms mainly
feed on recent soil organic pools, with a mean
turnover time of a few years. They made use of
the character of the study sites where the vege-
tation shifted from a C3 type to a C4 type and
vice versa.
Stable isotopic studies of termites 383
Schmidt et al. (1997) compared isotope ratios
of earthworms from a wheat and a wheat-clo-
ver cropping system and demonstrated the
d15N signature of legumes can in¯uence those
of soil invertebrates. They also reported that
d15N of earthworm species are positively cor-
related with the feeding habit along a gradient
from plant litter to decomposed organic mate-
rials (Fig. 2), similar to termites. These data
suggest that the isotopic approach may be
useful in studying the feeding relationships of
general detritivorous animals as well as termites
(Tayasu et al. 1997, 1998) and earthworms
(Schmidt et al. 1997).
CONCLUSIONS
This brief review illustrates how stable isotope
ratios of termites are useful both in studying
intestinal symbiosis with microbes and in
elucidating their ecological position in an
ecosystem. However, it is still unclear why wide
ranges of d13C and d15N are observed in
termites. Microbial dynamics in soil as well as
in the termite-symbiont system must be con-
sidered.
The use of stable isotope ratios in the study of
detritivorous animals has some potential for
elucidating complex relationships occurring in the
detritus food web. Experimental studies of ter-
mites and earthworms, particularly those with
reference to quality of food, should be an im-
portant step in the application to general de-
titivores.
ACKNOWLEDGEMENTS
I am grateful to Dr T. Abe for providing me with
an opportunity to write this review for Ecological
Research, and to Dr A. Sugimoto for permission to
use the unpublished data. I also thank Drs L. L.
Handley, E. Hobbie and A. V. Spain for valuable
comments on the manuscript. The author is a
research fellow of the Japan Society for the
Promotion of Science and a guest scientist of
Center for Ecological Research, Kyoto Univer-
sity.
384 I. Tayasu
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