Present address: Frontier Research Center for Global Change, 3173–25, Showamachi, Kanagawaga, 236–0001, Japan.
Estimation of the longevity of C in terrestrial detrital food webs using radiocarbon (14C): how old are diets in termites?
Article first published online: 19 APR 2006
Volume 20, Issue 2, pages 385–393, April 2006
How to Cite
HYODO, F., TAYASU, I. and WADA, E. (2006), Estimation of the longevity of C in terrestrial detrital food webs using radiocarbon (14C): how old are diets in termites?. Functional Ecology, 20: 385–393. doi: 10.1111/j.1365-2435.2006.01081.x
- Issue published online: 19 APR 2006
- Article first published online: 19 APR 2006
- Received 15 June 2005; revised 9 September 2005; accepted 20 September 2005 Editor: S. L. Chown
- Diet age;
- food web;
- stable carbon and nitrogen isotope ratios;
- Top of page
- Materials and methods
- 1We propose that diets of consumers in a food web have various ages, where age is defined as the time elapsed since carbon (C) in the diet was fixed from atmospheric CO2 by primary producers. To examine the diet ages for primary consumers in a detrital food web, we measured the radiocarbon (14C) content of termites collected in Thailand in 1998 and 2004. Diet ages were estimated by comparing the 14C content of samples with records of atmospheric 14CO2, which doubled in the early 1960s as a result of nuclear weapons tests and decreased after the nuclear test ban treaty. For comparison, we measured the 14C content of bees as primary consumers in a grazing web at the same study site. Stable carbon and nitrogen (N) isotope ratios were also analysed.
- 2The 14C contents of the same species of termites decreased during the sampling interval, indicating that they used organic matter produced after the peak in atmospheric 14CO2. The diet ages were estimated to be 12–18, 7–13 and 5–9 years for the wood-feeder (Microcerotermes crassus), the soil-feeders (Dicuspiditermes makhamensis and Termes comis) and the fungus-grower (Macrotermes carbonarius), respectively. One colony of soil-feeder (T. comis), which nested in a fallen tree trunk, had exceptionally low 14C content, and its diet age was estimated to be around 50 years. The two bee species had lower 14C contents compared with the termites, and their diet ages were estimated to be 0 (Apis florea) and 2–4 years (Trigona sp.).
- 3Stable C and N isotope ratios of termites showed similar patterns as previously reported, and no clear difference was observed between 1998 and 2004. Although the bees and the fungus-growing termite had similar stable C and N isotope ratios, their diet ages differed.
- 4Our study suggests that radiocarbon can be used to estimate the diet ages of consumers in terrestrial food webs. Diet age should provide new insight into the trophic positions of organisms in grazing and detrital food webs and the interactions between these two webs.
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- Materials and methods
In terrestrial ecosystems, most net primary production enters the detrital food web without being consumed in the grazing food web (Swift, Heal & Anderson 1979; Begon, Harper & Townsend 1996). The detrital food web can affect the quantity and quality of primary production through the decomposition of organic matter and the cycling of nutrients, thereby supporting the grazing food web, which in turn affects the primary production entering the detrital web (Wardle et al. 2004). In addition to these indirect interactions between the two food webs via primary producers, the grazing food web is often sustained directly by energy and material from the detrital food web (Polis & Strong 1996).
It is important to know the precise trophic position of a consumer in a grazing or detrital food web because the position represents its functional role (e.g. predator, herbivore or decomposer; Eggers & Jones 2000). However, it is difficult to determine the trophic position of a consumer using only natural history observations because it is time-consuming and all trophic links may not be of equal importance (Post 2002); it is especially difficult for detrital organisms because of their cryptic behaviour and taxonomic diversity. Furthermore, considering the ubiquity of detrital infusion and omnivory in terrestrial food webs (Polis & Strong 1996), it is also difficult to assign arbitrary consumers to either grazing and/or detrital food webs and to estimate to what extent a consumer in a grazing food web is dependent on the detrital subsidy without field experiments (e.g. Miyashita, Takada & Shimazaki 2003).
Stable isotope techniques can provide time-integrated measurements of trophic position, and thus have been used to disentangle complex food webs, and to investigate the trophic position of organisms in both terrestrial grazing and detrital food webs (e.g. Ostrom, Colunga-Garcia & Gage 1997; Ponsard & Arditi 2000). Most of these studies were based on the finding that stable carbon (C) isotope ratios of animals are similar to those of their diets (DeNiro & Epstein 1978), and that stable nitrogen (N) isotope ratios of animals are about 3·4 higher than those of their diets (Minagawa & Wada 1984). In the detrital food web, stable N isotope ratios of detritivores also increase along with the humification gradient of their food substrates, although the underlying mechanisms of the 15N enrichment remain unclear (Tayasu 1998).
These isotopic studies provide a ‘snapshot’ of a food web in terms of transfer of energy and material through prey and predator interactions. In the snapshot, all consumers are placed in trophic positions that are connected by various amounts of energy and material flows originating from primary producers. In addition to their amounts, energy and material flows have another important dimension, i.e. the time axis. Although energy and material flows begin with primary production, the time of production (i.e. photosynthesis) is not always the same, and can be quite diverse in a food web. In other words, the diets of consumers can be considered to have various ‘ages’. The diet age of a consumer can be defined as the time elapsed since C in its diet was fixed from atmospheric CO2 by primary producers. This definition of diet age is the same as that previously termed ‘lag time’ (Druffel & Griffin 1995, Beavan & Sparks 1998) or ‘sample age’ (Hobbie et al. 2002).
Diet age should be relatively young in grazing food webs and older in detrital food webs. If so, diet age may allow the estimation of the relative dependence of a consumer on grazing and detrital food webs, and the placement of consumer trophic positions along the longevity of C (turnover times) that they use from the ‘whole’ food web. Recent studies have investigated the food web effects of changes in primary production caused by high CO2 concentrations and modified plant species composition to understand how anthropogenic activities affect ecosystem properties (e.g. Jones et al. 1998; Wardle et al. 1999). Diet age should allow the prediction of the response of consumers, especially consumers of the detrital food web, to these changes because a consumer with a young diet age should respond more quickly to changes in primary production than one with an older diet age. However, diet age has rarely been examined.
In practice, however, it would be difficult to measure the diet age in a food web based on field observations, even with stable isotope techniques. In addition to its ‘stable’ isotopes, carbon also has a ‘radioactive’ isotope, i.e. radiocarbon (14C). The 14C content of atmospheric CO2 drastically increased in the 1950s and early 1960s as a result of nuclear weapons tests (Fig. 1). Since the nuclear test ban treaty of 1962, the ‘bomb’-14C of atmospheric CO2 has exponentially decreased through exchange with oceans and terrestrial biota (Levin & Hesshaimer 2000).
Given that the 14C content of organic matter synthesized by primary producers is the same as that of atmospheric CO2 at the time (Burchuladze et al. 1989; Druffel & Griffin 1995; Hua et al. 2000), the trend in the decline in 14CO2 allows us to estimate the time when the organic matter was produced by a primary producer, such that we can estimate the diet age by measuring the 14C content of a consumer, and then comparing it with the known 14CO2 trend. As the recent yearly change is comparable to the analytical error of 14C measurement using accelerator mass spectrometry (AMS), we can estimate the diet age with a precision of 1–2 years.
The 14CO2 trend has been used to examine the feeding habits of rats (Beavan & Sparks 1998), the mycorrhizal and saprotrophic status of fungi (Hobbie et al. 2002), and the feeding behaviour of enchytraeids (Briones & Ineson 2002). The diet age does not distinguish in which form the fixed C spent its time, e.g. as stored or structural C in plants, dead plant debris, root exudates, soil organic matter or prey organisms. Furthermore, consumers may use various types of organic matter with different ages; thus, the estimated diet age should be regarded as a weighted mean.
To verify the validity of radiocarbon in estimating diet age and examining the variation in the diet ages of a detrital food web, we examined the 14C content of termites (Isoptera) with different feeding habits in a dry evergreen forest in Thailand. Termites are one of the most abundant detritivores in tropical ecosystems (Wood & Sands 1978), and have diversified to use various stages of organic matter ranging from fresh plant materials to humified organic matter (soil organic matter; Noirot 1992; Bignell & Eggleton 1995). Relatively substantial data of stable C and N isotope ratios, as well as preliminary data on 14C content, are available for termites. Tayasu et al. (2002b) reported that wood-feeding termites had a higher 14C content than did soil-feeding termites for samples collected in both Cameroon, 1994, and Thailand, 1998, and termites with the same feeding habits had a higher 14C content in 1994 than in 1998, suggesting that soil-feeding termites use younger diets than do wood-feeders.
We compared the 14C contents of the same species of wood- and soil-feeders collected in 1998 and 2004 at the same sampling site to confirm that termites use organic matter produced after the peak of 14CO2. Such confirmation is required because a lower 14C content may indicate an older diet if the organic matter used was produced before the peak of atmospheric 14CO2. We evaluated the 14C content of a fungus-growing termite collected in 1998, which cultivates symbiotic fungi on fungus garden made from plant materials in the nest and feeds on the fungus garden degraded by the symbiotic fungi (Rouland-Lefèvre 2000). To compare diet ages between grazing and detrital food webs, we collected two bee species (Apidae) in 2004 as representatives of primary consumers in the grazing food web. The bee diet consists of nectar and pollen (Roubik 1989), which have expected ages of 0–1 years because their labile carbohydrates are mainly formed in the current year of production (Hobbie et al. 2002). In addition to 14C contents, we also measured stable C and N isotope ratios. We discuss diet age in relation to these stable isotope ratios and the known feeding habits and biology of the study species, and its importance for further studies of terrestrial food webs.
Materials and methods
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- Materials and methods
study sites and sample collection
The study site was in a dry evergreen forest within the Sakaerat Environmental Research Station in Nakhon Ratchashima, Thailand (14°30′ N, 101°56′ E; mean annual temperature: 26 °C; mean annual precipitation: 1240 mm).
The following termite species were collected both in January 1998 and January 2004: Microcerotermes crassus Snyder (wood-feeder), Dicuspiditermes makhamensis Ahamd, and Termes comis Haviland (soil-feeders). Macrotermes carbonarius (Hagen) (fungus-grower) was collected only in January 1998. Two bee species (Apidae), Apis florea Fabricius and Trigona sp., were also collected in January 2004. Additionally, leaf litter (L layer) was collected in January of 1998 and 2004, and the samples were ground with a ball mill. The samples were dried at 60 °C for over 24 h in an air-dryer.
radiocarbon and stable isotope analyses
For the isotope analyses, we used head capsules of termites where possible to exclude the influence of the gut contents (wood and soil) on stable C and N isotope ratios and radiocarbon. However, when there were not enough individuals (c. 30) to collect head capsules, we used whole bodies (including gut contents), because we found no significant difference in the isotopes between head capsules and whole bodies (see Results).
For radiocarbon analysis, samples (estimated to produce about 2 mg C) were combusted in evacuated and sealed Vycor tubes with CuO, Cu, and Ag wire at 850 °C for 2 h. After cooling, the Vycor tubes were cracked on a vacuum line, and the CO2 was cryogenically purified. The purified CO2 was graphitized under Fe catalysis at 650 °C for 6 h (Kitagawa et al. 1993). The graphite samples were sent to the Rafter Radiocarbon Laboratory, Institute of Geological and Nuclear Sciences, New Zealand, for accelerator mass spectrometry measurements of radiocarbon. Radiocarbon values were reported as Δ14C (), which is the part per thousand deviation from the activity of nineteenth century wood, and corrected for the fractionation using stable C isotope ratios of the samples (Stuiver & Polach 1977). The average analytical error was ±5·5.
For stable C and N isotope analyses, the samples were folded into tin capsules. Stable C and N isotope ratios were measured using a mass spectrometer (Finnigan MAT Delta S or Delta plus XP, Bremen, Germany) coupled with an elemental analyser. The precision of the on-line procedure was better than ±0·2 for both isotope ratios. The natural abundances of 13C and 15N are expressed in per mil () deviation from international standards: δ13C or δ15N = (Rsample/Rstandard − 1) × 1000, where R in δ13C or δ15N is 13C/12C or 15N/14N, respectively. Pee Dee Belemnite and atmospheric nitrogen were used as the international standards for carbon and nitrogen, respectively. δ13C and δ15N values of whole bodies of termites collected in 1998 were reported by Tayasu, Hyodo & Abe (2002a) and Tayasu et al. (2002b).
diet age estimation
To estimate diet age in termites and bees, we compared Δ14C values of samples with those of atmospheric CO2 recorded at Schauinsland, Germany, for 1976–97 (Levin & Kromer 1997). We estimated the Δ14C values of atmospheric CO2 after 1997 by extrapolation of the exponential function: Δ14C(t) = 417 × exp(–t/16·0), where t is the year after 1974 (Levin & Kromer 1997). For comparison, the ages after litter production were also estimated as diet ages in the same manner.
To our knowledge, no data are available on the Δ14C trend of atmospheric CO2 in Thailand. It may be possible that there is a difference in Δ14C values of atmospheric CO2 between temperate northern hemisphere (Germany) and tropical (Thailand) regions. Hua et al. (2000) investigated the Δ14C values from 1952 to 1975 in three-leaf pine tree rings in north-western Thailand and found a large depletion of Δ14C values of atmospheric CO2 in 1953/54, which may be due to upwelling in the tropical Indian Ocean. However, the overall trend in Δ14C of atmospheric CO2 in Thailand was similar to that in Germany, and there is a time delay of approximately 1 year between these regions (Hua et al. 2000). Because 1 year was within our analytical error, we did not correct for the difference in latitude.
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- Materials and methods
differences in Δ14c, δ13c and δ15n between head capsules and whole bodies of termites
The differences in the Δ14C values between head capsules and whole bodies of termites from the same colonies were within our analytical error (see Appendix). δ13C and δ15N values showed slight differences between the head capsule and the body, but the greatest differences were 1·4 for T. comis colony 6 and 0·9 for D. makhamensis colonies 4 and 6, which were small enough not to influence our interpretation of the results (see Appendix). The small differences mean the contribution of organic matter of gut contents to these isotopic values is modest relative to that of body tissue. Therefore, we did not distinguish between head capsules and whole bodies in terms of isotopic values.
variation in Δ14c, δ13c and δ15n of termites and bees
For Δ14C values of samples collected in 1998, the wood-feeding termite M. crassus had higher 14C content relative to the other termites, although M. crassus showed high variation in Δ14C values (Fig. 2). Δ14C values of the soil-feeder T. comis appeared higher than those of the soil-feeder D. makhamensis and the fungus-grower M. carbonarius, both of which showed similar Δ14C values. Litter was the most depleted in 14C content among the samples in 1998. Δ14C values of termites collected in 2004 showed a pattern similar to that in 1998, except that the variation in 14C content in M. crassus was relatively small, while T. comis showed a large variation in 14C content. One colony (colony 4) of T. comis had the lowest Δ14C values (47 ± 7·4) among the organisms examined in this study. In contrast to termites, A. florea had a 14C content similar to the estimated value of atmospheric CO2 (63·9) in 2004, and Δ14C values of Trigona sp. were higher than those of A. florea and litter collected in 2004.
We compared the 14C contents in the same species and litter collected in 1998 with those in 2004 and found that the Δ14C values of the samples in 1998 were higher than those in 2004. The differences (mean ± SD) in 14C content between 1998 and 2004 were 81·0 ± 36, 31·6 ± 6·7, 77·1 ± 36·9 (53·5 ± 11·3) and 40·9 for M. crassus, D. makhamensis, T. comis (excluding colony 4), and litter, respectively.
The δ13C and δ15N values of D. makhamensis and T. comis were higher than those of M. crassus, but we found no clear difference in the δ13C and δ15N values between D. makhamensis and T. comis (Fig. 3a). M. carbonarius had higher δ13C values, and similar δ15N values compared with M. crassus. This pattern was consistent with the results of Tayasu et al. (2002a,b). The two bee species showed δ13C and δ15N values similar to those of M. carbonarius. Trigona sp. had higher δ13C and δ15N values than did A. florea. The δ15N values of litter were close to M. crassus, but the δ13C values were more depleted. Comparing δ13C and δ15N values of termites collected in 1998 with those collected in 2004, we observed no clear difference in these values, although δ15N values of M. crassus were higher in 2004 than in 1998.
diet ages in termites and bees
The diet age of the wood-feeder M. crassus ranged from 12 to 18 years, which is older than the age of litter (0–4 years) (Table 1). The diet age of M. crassus was older than that of the soil-feeder D. makhamensis (7–12 years). Except for colony 4, the soil-feeder T. comis had a diet age (8–13 years) that was similar to that of D. makhamensis, and higher than that of the fungus-grower M. carbonarius (5–9 years). We collected colony 4 of T. comis from a nest on a fallen tree trunk, and by comparing the 14C content with that of the 14C content tree rings in Thailand (Hua et al. 2000), we estimated the diet age of colony 4 to be about 50 years.
|Taxa or sample type||Colony no.||Collected in||Body parts used for age estimation||Diet age (year)|
|M. crassus||1||Jan. 98||Head capsule||12–13|
|2||Jan. 98||Head capsule||17–18|
|3||Jan. 98||Head capsule||16–17|
|4||Jan. 04||Head capsule||13–15|
|5||Jan. 04||Head capsule||13–14|
|6||Jan. 04||Head capsule||14–17|
|D. makhamensis||1||Jan. 98||Head capsule||7–9|
|2||Jan. 98||Head capsule||7–9|
|3||Jan. 98||Whole body||8–10|
|4||Jan. 04||Head capsule||9–12|
|5||Jan. 04||Head capsule||9–12|
|6||Jan. 04||Head capsule||9–12|
|T. comis||1||Jan. 98||Whole body||8–10|
|2||Jan. 98||Whole body||10–12|
|3||Jan. 98||Whole body||10–13|
|4||Jan. 04||Head capsule||47*|
|5||Jan. 04||Head capsule||8–11|
|6||Jan. 04||Head capsule||10–12|
|M. carbonarius||1||Jan. 98||Whole body||8–9|
|2||Jan. 98||Whole body||5–8|
|3||Jan. 98||Whole body||6–8|
|Trigona sp.||Jan. 04||Whole body||2–4|
|A. florea||Jan. 04||Whole body||0|
The two bee species, A. florea and Trigona sp., had diet ages that were apparently younger than those of termites, and the diet age of the latter species was older than that of the former, and that of litter. Noticeably, the diet age of A. florea was estimated to be 0 years, indicating that this species feeds only on current-year products.
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- Materials and methods
We demonstrated that Δ14C values of termites differ based on their feeding habits. The wood-feeder M. crassus had Δ14C values that were higher than those of the soil-feeders D. makhamensis and T. comis, which is generally consistent with the preliminary results reported by Tayasu et al. (2002b). We also showed that Δ14C values of the same species of termites and litter decreased during the sampling interval (1998–2004), although we found no significant difference in the pattern of stable C and N isotope ratios. This depletion in the 14C content in both termites and the litter should reflect the decline in atmospheric 14CO2, and therefore indicate that these termites, which were collected in 1998 and 2004, fed on organic matter that had been produced by photosynthesis after the peak of bomb-14C (1962–63; Levin & Hesshaimer 2000). However, an exception was that T. comis colony 4, collected in 2004, fed on a fallen tree trunk, had a highly depleted Δ14C value (47 ± 7·4), and should have used organic matter produced before the bomb-14C peak.
Using the decreased 14C content of atmospheric CO2 after the peak of bomb-14C, we estimated the diet ages of termites, bees and plant litter. The two soil-feeders D. makhamensis and T. comis showed similar diet ages, which were younger than that of the wood-feeder M. crassus. As Tayasu et al. (2002b) pointed out, there was no significant difference in diet ages or stable C and N isotope ratios between T. comis and D. makhamensis, except for the diet age of T. comis colony 4.
Among termites, different species specialize in the use of organic material as food across the whole humification gradient. The range is from live plant tissues at one extreme, to soil organic matter at the other (Bignell & Eggleton 2000). Tayasu et al. (1997) proposed that stable N isotope ratios of termites reflect the degree of the humification of their food source. From the perspective of the humification gradient, it may be expected that the soil-feeding termites feed on older organic matter because humification progresses over time through the activity of microorganisms. However, we propose that the soil-feeders use diets that are younger than those of wood-feeders. This discrepancy between the humification process and the diet age may be explained by whether wood tissue, in which C passes a lot of time without humification, is used by the termites. Therefore, it is suggested that most soil-feeders should use organic matter in soil that originates, not from woody tissues, but from root exudates and/or leaf and root litters (Tayasu et al. 2002b). On the other hand, colony 4 of the soil-feeder T. comis used organic matter, which was apparently derived from woody tissue, and was humified to a similar extent as the soil organic matter used by the other soil-feeders; this colony had the oldest diet age among the termites examined in this study.
As with variation in the diet ages of wood-feeders, M. crassus showed a very small range of diet age (12–18 years), despite the presence of variously aged organic matter ranging from 0 to >1000 years in the lifetime of tropical trees (Chambers, Higuchi & Schimel 1998). This small range of diet ages could be attributed to the fact that M. crassus tends to feed on dead wood with a relatively small diameter (<5 cm; Yamada et al. 2003).
The fungus-growing termite M. carbonarius had a diet age that was younger than that of the wood-feeder M. crassus. This is in agreement with its known feeding habits; this species is rarely found in dead wood, and consumes fresh leaves, as well as very small branches <3 cm in diameter (Abe 1979). Our study demonstrated that litter was relatively young (0–4 years), suggesting that the fungus-grower uses small branches to a significant extent in its diet.
Several studies on the response of termite assemblages to anthropogenic disturbances in tropical forests have been undertaken, and they have indicated that soil-feeders are more vulnerable to disturbance than are wood-feeders (e.g. Eggleton et al. 2002; Jones et al. 2003). Eggleton et al. (2002) suggested that this trend is mainly caused by abiotic environmental changes (e.g. drought) and the fragile bodies and severe requirements for stable habitat conditions of soil-feeders. In addition, we suggest that this trend may reflect that soil-feeders with younger diet ages respond more quickly to disturbance of primary production than do wood-feeders with older diet ages.
In addition to these termites, we measured the 14C contents of two bee species as representatives of the grazing food web. A. florea showed a 14C value as expected from the extrapolation and, thus, was determined to have a diet age of zero, while the stingless bee Trigona sp. showed an older diet age (2–4 years) than A. florea. The reason why these two bee species showed differences in their diet ages is unknown, and it is also uncertain if these ages are typical for each species, since there was no replication. However, the difference may be explained by their nesting and foraging habits. A. florea builds open nests and relocates its nests in response to seasonal changes (Wongsiri et al. 1996). In contrast, Trigona sp. constructs well-built nests, and queens are unable to fly (Roubik 1989; Wille 1983); thus, Trigona sp. should seldom move their nest location. The difference in mobility may affect the age of the diet storage, i.e. Trigona sp. use nectar and pollen that have been stored longer than those used by A. florea. Some species of Trigona consume carcasses (Roubik 1989), which may also be older than nectar and pollen.
Diet ages clearly reflect the differences in food sources between the fungus-growing termites and the bees, even though they had similar δ15N and δ13C values. Relatively low δ15N values indicate that both use non-humified diets, while the high δ13C value may reflect differences in their food sources. Since basidiomycetes are generally more enriched in 13C relative to their substrates (Gleixner et al. 1993; Kohzu et al. 1999), the high δ13C values in fungus-growers may indicate that they acquire food source to some extent from the symbiotic fungi, grown in fungus gardens, which are made from plant materials (Hyodo et al. 2003). This explanation may be partly applicable to soil-feeders with high δ13C values (Tayasu et al. 1998), because it is suggested that soil-feeders use microorganisms, as well as plant materials, in their diets (Ji & Brune 2001). On the other hand, the high δ13C values in bees may reflect that they use sucrose in nectar, which should have higher δ13C values than do bulk plant materials through metabolic branching effects (Gleixner et al. 1993).
Increasing numbers of studies examine how the effects of changes in primary production manifest in consumers of grazing and detrital food webs, as well as the interactions between the webs, based on field and laboratory experiments (Wardle 2002). The estimation of diet age using radiocarbon, which measures energy and material flow in nature, should provide additional information; however, little information is currently available on the diet ages of consumers (e.g. mycorrhizal fungi: 0–2 years (Hobbie et al. 2002), saprotrophic fungi: 6 to >50 years (Hobbie et al. 2002), and enchytraeids: 5–10 years (Briones & Ineson 2002)). Further studies using radiocarbon and stable C and N isotope ratios should be helpful in understanding both terrestrial grazing and detrital food webs and their interactions, which regulate terrestrial ecosystem processes.
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We are grateful to the National Research Council of Thailand for permission to conduct this research. We also thank Dr H. Takeda, Dr W. Decha, Dr R. Ishii and the staff of Sakaerat Environmental Station for various kinds of help, Dr R. Sparks and Dr N. Beavan-Athfield for valuable information on radiocarbon analysis, Dr H. Samejima for helpful discussion on biology of tropical bees, and two anonymous reviewers for invaluable comments on an earlier version of this manuscript. This study was supported by Research Institute for Humanity and Nature (Project 3–1) and partly by the Grant for the Biodiversity Research of the 21st Century COE (A14). F.H. is currently supported by the Research Fellowship of Japan Society for the Promotion of Science for Young Scientists.
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- Top of page
- Materials and methods
|Taxa or sample type||Colony no.||Collected in||Analysed parts||δ13C ()||δ15Ν ()||Δ14C ()||Lab code NZA no.|
|M. crassus||1||Jan. 98||WB*||−28·1||2·8||173·8 ± 10·4||**|
|1||Jan. 98||HC||−28·7||3·5||188·4 ± 5·9||20 559|
|2||Jan. 98||HC||−28·3||2·1||265·2 ± 5·4||20 551|
|3||Jan. 98||HC||−27·8||3·7||244·9 ± 5·8||20 552|
|4||Jan. 04||WB||−27·5||6·0||153·7 ± 5·4||20 022|
|4||Jan. 04||HC||−27·9||6·4||147·5 ± 5·1||20 023|
|5||Jan. 04||WB||−28·0||4·2||134 ± 5||19 676|
|5||Jan. 04||HC||−27·9||4·4||142·8 ± 5·1||19 677|
|6||Jan. 04||WB||−28·2||4·7||167 ± 5·5||19 678|
|6||Jan. 04||HC||−28·3||4·7||165·2 ± 5·7||19 679|
|D. makhamensis||1||Jan. 98||WB*||−24·6||11·0||146·6 ± 10||**|
|1||Jan. 98||HC||−23·9||11·3||143·4 ± 5·2||20 553|
|2||Jan. 98||HC||−23·1||10·6||152·1 ± 4·6||20 554|
|3||Jan. 98||WB*||−23·8||9·7||158·2 ± 4·6||20 560|
|4||Jan. 04||WB||−24·2||10·7||115·1 ± 5·4||19 681|
|4||Jan. 04||HC||−23·5||11·6||118·8 ± 5||19 682|
|5||Jan. 04||WB||−24·5||10·9||122·6 ± 6||19 683|
|5||Jan. 04||HC||−23·6||11·5||118·1 ± 5·3||19 684|
|6||Jan. 04||WB||−24·9||9·8||113 ± 6·2||19 685|
|6||Jan. 04||HC||−23·7||10·7||121·9 ± 5||19 686|
|T. comis||1||Jan. 98||WB*||−23·0||11·1||160·2 ± 5·1||20 561|
|2||Jan. 98||WB*||−24·5||12·3||173·5 ± 4·7||20 562|
|3||Jan. 98||WB*||−23·8||11·6||180·5 ± 5·1||20 563|
|4||Jan. 04||WB||−23·5||9·4||54·3 ± 7·2||19 688|
|4||Jan. 04||HC||−22·3||9·5||47 ± 7·4||19 689|
|5||Jan. 04||WB||−23·2||11·4||116 ± 5·8||19 690|
|5||Jan. 04||HC||−22·6||10·8||112 ± 5·3||19 691|
|6||Jan. 04||WB||−24·8||9·8||123·5 ± 6||19 692|
|6||Jan. 04||HC||−23·4||10·3||123·9 ± 5||19 693|
|M. carbonarius||1||Jan. 98||WB*||−24·9||2·6||154·2 ± 4·7||20 564|
|2||Jan. 98||WB||−23·7||6·2||133·2 ± 3·8||21 463|
|3||Jan. 98||WB*||−25·5||2·7||136·6 ± 4·3||21 464|
|Trigona sp.||Jan. 04||WB||−24·3||2·9||79·6 ± 4·4||20 555|
|A. florea||Jan. 04||WB||−26·0||1·2||60·4 ± 4·7||20 539|
|Litter||Jan. 98||–||−29·8||5·3||111·8 ± 4·9||20 545|
|Jan. 04||–||−29·1||2·7||70·9 ± 4·3||20 540|