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Keywords:

  • earthworms;
  • radiocarbon;
  • stable nitrogen isotope;
  • termites

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
  • 1
    Stable nitrogen (N) isotope has been widely used to disentangle food webs and to infer trophic positions of organisms based on an assumption that the stepwise enrichment occurs along trophic levels. The enrichment of 15N in soil organisms with diet humification has also been reported, but the underlying mechanism has not been fully examined.
  • 2
    To examine the effect of diet humification on 15N, we estimated the stable N isotope ratios and diet ages of earthworms and termites. These organisms feed on organic matter with various degrees of humification, ranging from undecomposed plant materials to humified organic matter (soil organic matter), in a gallery forest and a savanna in the Ivory Coast. We defined diet age as the time elapsed since carbon (C) in the diet of earthworms and termites was fixed from atmospheric CO2 by photosynthesis; it was estimated by comparing the radiocarbon (14C) content of these organisms to atmospheric 14CO2 records.
  • 3
    Stable N isotope ratios increased along the humification gradient of diets, and values for earthworms and termites varied from 1·8‰ to 9·9‰ and from –1·5‰ to 15·9‰, respectively. Epigeic (litter-feeding) earthworms had younger diet ages (2–4 years), whereas endogeic (soil-feeding) earthworms generally exhibited older diet ages (5–9 years). Grass-feeding termites had young diet ages (2 years), and wood/soil-feeding termites had the oldest diet ages (c. 50 years). Soil-feeding termites were similar in diet age (7–12 years) to wood feeders (8–11 years), with the exception of one species (18–21 years) that consumes large-diameter wood.
  • 4
    A significant positive relationship was found between diet ages and stable N isotope ratios of the two groups in the savanna. This relationship held in the gallery forest when termites feeding on woody tissues were not considered. These results show that the stable N isotope ratios of organisms can increase with diet age, unless C in the diet has been stored as organic matter, such as woody tissue, that is able to age without being subject to humification processes.
  • 5
    Given that above-ground food webs are often sustained directly by material and energy flow from below-ground food webs, in addition to trophic interactions, gradual enrichment of 15N with the humification of below-ground diets should be considered when interpreting stable N isotope ratios of terrestrial food webs.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

An increasing number of studies have revealed that below-ground food webs affect above-ground food webs through the release of nutrients by decomposition, as well as the direct provision of material and energy (e.g. Wardle 2002; Moore et al. 2004; Wardle et al. 2004). The linkage between below- and above-ground food webs influences the stability of entire food webs and thus terrestrial ecosystem function (Hooper et al. 2000; Rooney et al. 2006).

An organism's position in a particular food web reflects its function in the ecosystem (Eggers & Jones 2000). Stable nitrogen isotope ratios (δ15N) have been measured in soil animals to investigate feeding habits and positions in below-ground food webs (Schmidt, Scrimgeour & Handley 1997; Tayasu et al. 1997; Ponsard & Arditii 2000; Scheu & Falca 2000). The stable isotope method has advantages that make it possible to examine time-integrated measurements of food sources and trophic positions in food webs (Post 2002). Previous studies have shown that species of diverse taxonomic groups (e.g. earthworms, termites and Collembola) that feed on more humified organic matter have higher values of δ15N. Thus, the level of δ15N increases along a humification gradient of diets (Schmidt et al. 1997; Tayasu et al. 1997; Hishi et al. 2007).

The gradual enrichment of 15N along a humification gradient (e.g. up to 12‰ in the case of termites) contrasts markedly with the pattern typical of aquatic and above-ground food webs, in which it is assumed that a stepwise enrichment of 15N (e.g. 3·4‰) occurs with increases in trophic level (Minagawa & Wada 1984). The mechanisms underlying trophic enrichment of 15N have been investigated using experiments and meta-analyses (e.g. McCutchan et al. 2003; Vanderklift & Ponsard 2003; Dalerum & Angerbjorn 2005). However, 15N enrichment with humification has not been fully examined, even though it may be a confounding factor in determining the δ15N values of organisms in below-ground food webs (Bardgett 2005).

The degree of humification of diets has been primarily estimated from gut contents, as well as the site and soil depth of the habitat of each taxonomic group (e.g. Takeda 1978; Lavelle 1979; Sleaford, Bignell & Eggleton 1996). However, because of the technical difficulty involved, there has been little quantitative estimation of the degree of humification of diets. Such measurements would elucidate both the effects of humification on the δ15N value of various taxonomic groups of detritivores and the unique enrichment patterns in below-ground food webs. Because the humification process should proceed over time through the activity of micro-organisms, soil organisms with higher values of δ15N are thought to feed on more aged organic matter (Tayasu 1998). Indeed, soil organic matter that has older fractions and is more affected by microbial processing exhibits relatively higher isotopic signatures of N (Nadelhoffer & Fry 1988; Kramer et al. 2003; Billings & Richter 2006).

The radioactive carbon isotope radiocarbon (14C) has been used to investigate the feeding habits of rats, enchytraeids, earthworms and termites, and the mycorrhizal status of fungi (Beavan & Sparks 1998; Briones & Ineson 2002; Hobbie et al. 2002; Tayasu et al. 2002; Briones, Garnett & Piearce 2005). It has been proposed that in addition to trophic level, the time axis (i.e. the approximate age of the food web) is an important factor in terrestrial food webs (Tayasu et al. 2002; Hyodo, Tayasu & Wada 2006). Hyodo et al. (2006) estimated the time axis as the ‘diet ages’ of organisms with a precision of 1–2 years by comparing organismal 14C contents to known records of atmospheric 14CO2, which was doubled by atmospheric nuclear tests and has been decreasing rapidly since the ban treaty of 1962 (Levin & Hesshaimer 2000). Diet age was defined as the mean time elapsed since C in diets of termites was fixed from the atmosphere by photosynthesis (Hyodo et al. 2006). Thus, the effect of diet humification on the δ15N value can be quantitatively examined by investigating the relationship between δ15N value and diet age of soil organisms determined using 14C.

To examine this relationship, we measured the δ15N and radiocarbon values of earthworms and termites with various feeding habits along a humification gradient in an African humid tropic gallery forest and savanna in the Ivory Coast. Because of the importance of their activities in the soil, both earthworms and termites have been referred to as ‘ecosystem engineers’ (Jones, Lawton & Schachak 1994; Lavelle & Spain 2005). These organisms occur in our study site (Josens 1972; Lavelle 1979) and belong to taxonomic groups for which the N isotopic signatures have been well examined. We demonstrate that trophic level is not the only factor determining the δ15N values of terrestrial organisms, resulting in a more complete understanding of terrestrial food web structure based on the stable N isotope and radiocarbon.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

study site and sample collection

Sampling was conducted at the Lamto Ecological Station, Ivory Coast (6°13′N, 5°02′W), at the end of the rainy season in July 2001. The research station is located in the forest–savanna boundary region of the Ivory Coast and is surrounded by a 2500-ha natural reserve characterized by a mosaic of grass and shrub savanna and gallery forest. The average annual temperature (1986–1996) is 28·4 °C, and the average annual precipitation is 1138 mm (Tondoh & Lavelle 2005).

Earthworms and termites were collected in gallery forests and savanna. Five species of earthworm and unidentified taxa in the family Eudrilidae and 10 species of termites were examined (see Table 1). Organisms were collected at three sites (each 1 km apart) in each vegetation type (forest and savanna). The feeding habits of earthworms were classified as epigeic (i.e. feed on litter), epi-endogeic (i.e. feed on litter and soil organic matter) or endogeic (i.e. feed on soil organic matter), whereas termites were classified as grass, wood, soil or wood/soil (i.e. feed at the interface of decomposing logs and the soil or within highly-decayed wood) feeders (Lavelle & Spain 2005; Tondoh & Lavelle 2005). Collected earthworms were kept in Petri dishes containing tap water in the dark (24 h) and allowed to empty their gut contents. Grass, leaf litter and soil (0–10 cm) were also collected at both sites. These samples were dried at 60 °C for over 24 h in an oven, and the soil and plant materials were air-dried at Lamto Ecological Station. Grass and leaf litter were ground to powder using a ball mill. Soils were passed through a 2-mm sieve and treated with 0·5 mol L−1 HCl overnight to remove inorganic C.

Table 1.  δ15N and diet age of earthworms, termites, soil organic matter, litter and grass. Sampling site and feeding habits of the two groups were also listed
Taxa or sample typeSampling siteFeeding habitsnδ15N (‰)Diet age (year)
MeanRangeMeanRange
  • Abbreviations: GF, gallery forest; S, savanna; EP, epigeic; ED, endogeic; EP/ED, epi/endogeic; GF, grass-feeder; WF, wood-feeder; WS, wood/soil feeder; SF, soil feeder.

  • Number of colonies for termites and individuals for earthworms except for Eudrilidae spp., which were measured by pooling several individuals.

  • One colony which showed 44 years was excluded to estimate the mean age.

Earthworm
 Dichogastor agilisGFEP26·16·1–6·13 2–4
 Hyperiodrilus africanusGFEP/ED17·0 6 
 Eudrilidae spp.GFED29·59·4–9·78 7–9
 Millsonia annomalaGFED19·2 5 
 Dichogastor terrae-nigreaGFED18·3 7 
 Dichogastor baeriSEP32·01·8–2·33 2–4
 Eudrilidae spp.SED36·46·2–6·65 2–6
 Millsonia annomalaSED36·25·9–6·75 5–6
 Dichogastor terrae-nigreaSED19·9 8 
Termite
 Microcerotermes parvusGFWF32·00·6–3·110 8–11
 Cryptotermes brevisGFWF2–1·0–1·5–0·52018–21
 Nasutitermes latifronsGFWF13·9 8 
 Amitermes evunciferGFWS?45·95·0–6·84 3–44
 Termes hospesGFWS25·75·1–6·34544–46
 Noditermes aburiensisGFSF314·813·2–15·99 7–11
 Euchilotermes tensusGFSF212·812·3–13·31111–12
 Procapritermes holmgreniGFSF19·5 9 
 Trinervitermes geminatusSGF30·1–0·6–0·22 2–2
 Microcerotermes sp.SWF1–0·9 3 
 Amitermes evunciferSWS?33·43·2–3·64 3–4
Soil organic matters
 Soil 0–10 cmGF 36·05·5–6·97 4–8
 Soil 0–10 cmS 34·23·5–5·09 8–10
 LitterGF 13·0 5 
 GrassS 2–0·5–0·5−−0·51 0–2

stable and radio isotope analyses

For the isotope analyses, we used adult earthworms with empty intestines and head capsules of termites to exclude the influence of gut contents on isotopic values. For radiocarbon analysis, samples (estimated to produce about 2 mg C: one to several earthworms and c. 30 termites from one colony) 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 Rafter Radiocarbon Laboratory, Institute of Geological and Nuclear Sciences, New Zealand, for accelerator mass spectrometry measurements of radiocarbon. Radiocarbon values are reported as D14C (‰), which is the part per thousand deviation from the activity of 19th century wood, and corrected for 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 contained in folded tin capsules. Stable C and N isotope ratios were measured using a mass spectrometer (Finnigan MAT Delta S or Deltaplus XP, Thermo Electron, Erlangen, Germany) coupled with an elemental analyzer (EA 1108 Fisons Instruments, Italy, or Flash EA 1112, Thermo Electron, Erlangen, Germany). The precision of the on-line procedure was better than ±0·2‰ for both isotope ratios. 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. All isotopic data are listed in the Appendix S1 of Supplementary material.

diet age determination

We estimated the diet age unambiguously from the difference between the sample collection year (2001) and the year (t) when the D14C value of a sample matched that of atmospheric CO2. The year (t) was calculated using a regression curve, year (t) = 2074 – 16·71 ln(D14C) (r2 = 0·997, P < 0·0001), which we estimated based on 14CO2 data for the northern hemisphere, including our study site, from 1977 to 1999 (Hua & Barbetti 2004; Supplementary Figure S1). The diet age of Termes hospes and one colony of Amitermes evuncifer was estimated by comparison to the D14C values of wines that had been collected prior to the 14C-bomb peak (Burchuladze et al. 1989) because their ages apparently exhibited 14C contents prior to the peak, and therefore we could not use the above equation. For comparison, the times elapsed since the organic soil layer, litter and grass were produced were also estimated as diet age.

statistical analyses

Variation in δ15N values was analyzed for each vegetation type using ancova with diet age as a covariate and taxonomic group as a class variable. In the gallery forest, where large variation in diet age of the wood- and wood/soil-feeding termites was found (see Results), simple regression analysis was also used to assess the effect of diet age on δ15N values of the earthworms and the soil-feeding termites.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

In both the gallery forest and savanna, the δ15N values of both earthworms and termites gradually increased from species feeding on plants (wood and grass) to those feeding on soil organic matter (Table 1). The δ15N values of earthworms ranged from 6·1‰ to 9·7‰ in the gallery forest and from 1·8‰ to 9·9‰ in the savanna, whereas those of termites ranged from –1·5‰ to 15·9‰ in the gallery forest and from −0·9‰ to 3·6‰ in the savanna. The δ15N values were higher in the gallery forest soil than in the savanna soil (P = 0·0505, t-test). This difference was also reflected in the values for litter and grass.

The diet age of earthworms varied from 2 to 9 years (Table 1). Epigeic earthworms exhibited the youngest diet ages (2–4 years), whereas endogeic earthworms had older diet ages (5–9 years), with the exception of one sample of Eudrilidae (2 years; Table 1). Litter and grass samples exhibited similar ages to those of epigeic and epi/endogeic earthworms and grass-feeding termites, respectively. Because of the large variation in values from the gallery forest, there were no significant differences in the diet ages of soils between the gallery forest and the savanna.

In contrast, the diet ages of termites varied much more than those of earthworms because of the presence of wood-feeding and wood/soil-feeding termites. Grass-feeding termites, Trinervitermes geminatus, exhibited the youngest diet age (2 years), and wood/soil-feeding termites, T. hospes, had the oldest diet age (c. 50 years), reflecting their respective feeding habits: T. geminatus feeds on current-year grasses, whereas T. hospes feeds and nests on humified dead trees. Soil feeders exhibited diet ages (7–12 years) similar to those of wood feeders (8–11 years), with the exception of one species, Cryptotermes brevis (18–21 years), which nests in and consumes only large-diameter wood (Abe 1987). A wood-feeding termite (Microcerotermes sp.) in the savanna had a young diet age (3 years), indicating that it consumed dead grasses or grass roots, or both, as reflected in the high δ13C value (see Supplementary Appendix S1).

In the gallery forest, no significant effect of diet age (F1,21 = 0·2849, P = 0·599), taxonomic group (F1,21 = 0·5305, P = 0·4744) or their interaction (F1,21 = 0·4577, P = 0·5061) was found on δ15N values (Fig. 1a). In the savanna, taxonomic group and the interaction had no significant effect (F1,13 = 2·5368, P = 0·1352; F1,13 = 1·0202, P = 0·331, respectively), while diet age had a significant effect on δ15N values (F1,13 = 12·6171, P = 0·0035; Fig. 1b). Simple linear regression analysis showed that diet age had a significant effect on δ15N values when wood- and wood/soil-feeding termites were removed and the rest of the detritivores were pooled together (r2 = 0·5465, P = 0·0039).

image

Figure 1. Relationship between the δ15N values and diet ages of earthworms and termites in the gallery forest (a) and the savanna (b). Closed and open circles, respectively, indicate earthworms and termites, except for wood feeders and wood/soil feeders, which are represented by open squares. Diet ages of some samples were slightly altered for clarity. The scale of diet age in the gallery forest changes at a break at 15-years-old.

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Stable isotopes have been widely used to understand food web structure and the trophic positions of organisms in food webs (Fry 2006). In contrast to aquatic and above-ground food webs, below-ground food webs exhibit a gradual increase in δ15N values among various organisms (Ponsard & Arditii 2000; Scheu & Falca 2000), as well as within a single taxon (earthworms, termites, mites and Collembola; Schmidt et al. 1997; Tayasu et al. 1997; Schneider et al. 2004; Chahartaghi et al. 2005; Hishi et al. 2007; but see Grey, Kelly & Jones 2004). It has been suggested that these patterns reflect the complex food web structure and the dominance of omnivory in the soil through direct prey–predator interactions (Eggers & Jones 2000).

Both earthworms and termites do indeed have increasing δ15N values along a humification gradient at a given site. Assuming the typical relationship between the δ15N of an animal and its diet (3·4‰; Minagawa & Wada 1984), the largest variation in the δ15N of earthworms and termites in a vegetation type corresponded to two and five trophic levels, respectively. Such variation could be a confounding factor in determining the trophic position of predators feeding on these detritivores, particularly because these soil organisms are common prey for various predators (Lavelle & Spain 2005).

In addition, the δ15N values were strongly positively correlated with diet age, regardless of taxonomic group in the savanna. In contrast, δ15N values were not significantly correlated with diet age in the gallery forest, apparently because of the large variety of wood- and wood/soil-feeding termites. Furthermore the relationship between δ15N and diet age held in the gallery forest when the wood- and wood/soil-feeding termites were not considered. Thus, these results show that the δ15N values of soil organisms increase with the age of diets in the soil, if the dietary C has not been stored in organic matter, such as wood tissue, that can age without being exposed to humification processes. The relationship observed in the gallery forest suggests that termites as well as earthworms using soil organic matter in tropical forest soils are dependent on organic matter derived from leaf/grass litter, roots and root exudates, but not from woody tissues, as carbon sources (Tayasu et al. 2002; Hyodo et al. 2006). Investigating variability in diet ages of these soil-feeding animals may provide insights into the contribution of woody debris to the soil organic matter and to the diet of soil organisms.

The increase in the δ15N values of organisms with diet age confirms the gradual enrichment of 15N with the humification of diets in the below-ground food web. This probably explains the variation in δ15N values of decomposers, which was previously thought to show a continuum from primary to secondary decomposers (Scheu & Falca 2000; Schmidt et al. 2004). The enrichment of 15N of organisms should correspond to the enrichment of the δ15N of organic matter in the soil. Although mechanisms of 15N enrichment in the soil are not yet well understood, several factors have been proposed: (i) ammonia volatilization (Högberg 1990); (ii) denitrification (Mariotti, Germon & Hubert 1981); (iii) fractionation associated with the mineralization of organic N by microbes (Nadelhoffer & Fry 1988); (iv) mycorrhizal transfer of 15N-depleted compounds from the soil to vegetation (Kohzu et al. 2000); and (v) accumulation of 15N-enriched compounds derived by microbial cells in the soil (Billings & Richter 2006). As a result of these complex processes, the δ15N of soil organic matter increases with soil depth (Nadelhoffer & Fry 1988) and with decreasing particle size of soil organic matter (Tiessen et al. 1984). Thus, further research at our study site examining the 14C content and δ15N values of soil organic matter at different soil depths and particle sizes will provide key information regarding the preferred particle size and feeding depths of soil detritivores.

Diet age is an important ecological trait that can provide information regarding the extent to which an organism depends on grazing and/or detrital food webs, an organism's position along turnover times of C used in a food web, and the timing of the manifestation of effects on primary producers in food webs (Hyodo et al. 2006). The diet age of termites has also been reported from a dry evergreen forest in Thailand (Hyodo et al. 2006). The diet ages of soil feeders (7–12 years) and wood/soil feeders (c. 50 years) are comparable to our results for the gallery forest in the Ivory Coast. However, a wood-feeding termite (Microcerotermes parvus) in the Ivory Coast had a younger diet age than a wood-feeding congener in Thailand (M. crassus: 12–18 years), presumably reflecting a difference in the distribution of available food sources (wood diameter) or in the preference of wood size by these two species of termites.

Briones et al. (2005) reported the 14C content of both epigeic and endogeic earthworms at a woodland in the United Kingdom. Considering the differences in latitude and the resulting C turnover time (decomposition rates; see Vogt, Grier & Vogt 1986; Aerts 1997), one might expect that the diet ages of earthworms with the same feeding habits in the United Kingdom would be older than those in the Ivory Coast. Interestingly, the diet age is similar between the two regions: epigeic earthworm diets are 0 to 3-years-old and endogeic earthworm diets are 5 to 8-years-old in the United Kingdom. This result suggests that diet age is not necessarily affected by the overall C turnover time of an ecosystem. Clearly, additional 14C measurements of organisms in various ecosystems should be conducted to better understand the factors that determine the 14C content and diet age of organisms across ecosystems.

In conclusion, based on the relationship between δ15N values and diet age, we demonstrated that the δ15N of soil organisms can increase with humification of diets and not just with trophic level. This relationship may allow the elimination of the effect of humification on the δ15N of terrestrial organisms and the correction of the trophic position of terrestrial predators based on 14C measurements. This correction may be required not only in below-ground but also in above-ground food webs, because the δ15N values of above-ground predators would reflect their consumption of prey from both food webs (Polis & Strong 1996; Rooney et al. 2006). We suggest that researchers who use stable isotope techniques to understand terrestrial food webs should consider the gradual enrichment of 15N with the humification of diets in soil. Stable N isotope and radiocarbon should be useful in determining the trophic position of an organism in terrestrial food webs.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

We thank people in Lamto Ecological Station and Dr K. Kawamura for various help, Drs P. Eggleton and G. Josens for identification of termites, and two anonymous reviewers for their invaluable comments on earlier version of this manuscript. This study was supported by the Ministry of Education, Culture, Sports, Science and Technology Grant in Aid for No. 09NP1501 and partly No. 19681002 and Research Institute for Humanity and Nature, Japan (P3-1). F.H. and I.T. were supported by the Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists and Research Abroad.

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  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
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Supporting Information

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Appendix S1. δ15N, δ13C, δ14C values and diet ages of earthworms, termites, soil, litter and grass collected in Ivory Coast in July 2001

Fig. S1. Regression curve between Δ14C values of atmospheric CO2 and its sampling year using the data of Hua and Bartetti (2004, Radiocarbon46: 1273–1298).

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