Ecological Research

, Volume 24, Issue 6, pp 1351–1359 | Cite as

Vertical heterogeneity of a forest floor invertebrate food web as indicated by stable-isotope analysis

  • Yutaka Okuzaki
  • Ichiro Tayasu
  • Noboru Okuda
  • Teiji Sota
Original Article


Diverse populations of invertebrates constitute the food web in detritus layers of a forest floor. Heterogeneity in trophic interactions within such a species-rich community food web may affect the dynamic properties of biological communities such as stability. To examine the vertical heterogeneity in trophic interactions among invertebrates in litter and humus layers, we studied differences in species composition and variations in carbon and nitrogen stable-isotope ratios (δ13C and δ15N) using community-wide metrics of the forest floors of temperate broadleaf forests in Japan. The species composition differed between the two layers, and the invertebrates in the litter layer were generally larger than those in the humus layer, suggesting that these layers harbored separate food webs based on different basal resources. However, the δ13C of invertebrates, an indicator of differences in the basal resources of community food webs, did not provide evidence for separate food webs between layers even though plant-derived organic matter showed differences in stable-isotope ratios according to decomposition state. The minimum δ15N of invertebrates also did not differ between layers, suggesting sharing of food by detritivores from the two layers at lower trophic levels. The maximum and range of δ15N were greater in the humus layer, suggesting more trophic transfers (probably involving microorganisms) than in the litter layer and providing circumstantial evidence for weak trophic interactions between layers at higher trophic levels. Thus, the invertebrate community food web was not clearly compartmentalized between the detrital layers but still showed a conspicuous spatial (vertical) heterogeneity in trophic interactions.


Compartment Food web structure Microhabitat 



We thank Y. Takami, Y. Takeuchi and H. Nakagawa for statistics, M. Yoshida, M. Ito, H. Takeda, S. Saito, T. Tanigaki, H. Nishi, S. Yamamoto, S. Gotou for taxonomy, C. Hori, T. Takeyama and N. Nagata for technical assistance, and D. Gustafson for English text assistance. We also thank Prof. M. Hori and the members of the Laboratory of Animal Ecology, Kyoto University, for advice and discussion. This research was supported in part by grants-in-aid for Biodiversity Research of 21st Century COE (A14) and Global COE Program “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem” from the Ministry of Education, Culture, Sports and Technology, Japan, and a grant-in-aid from the Japan Society for the Promotion of Science (No. 2037011 to TS and No. 19681002 to IT).

Supplementary material

11284_2009_619_MOESM1_ESM.doc (104 kb)
Supplementary material (DOC 109 kb)


  1. Balesdent J, Girardin C, Mariotti A (1993) Site-related 13C of tree leaves and soil organic matter in a temperate forest. Ecology 74:1713–1721. doi: 10.2307/1939930 CrossRefGoogle Scholar
  2. Billing SA, Richter DD (2006) Changes in stable isotope signatures of soil nitrogen and carbon during 40 years of forest development. Oecologia 148:325–333. doi: 10.1007/s00442-006-0366-7 CrossRefGoogle Scholar
  3. Briand F, Cohen JE (1984) Community food webs have scale-invariant structure. Nature 307:264–267. doi: 10.1038/307264a0 CrossRefGoogle Scholar
  4. Caner L, Zeller B, Dambrine E, Ponge JF, Chauvat M, Lianque C (2004) Origin of the nitrogen assimilated by soil fauna living in decomposing beech litter. Soil Biol Biochem 36:1861–1872. doi: 10.1016/j.soilbio.2004.05.007 CrossRefGoogle Scholar
  5. Chahartaghi M, Langel R, Scheu S, Ruess L (2005) Feeding guilds in Collembola based on nitrogen stable isotope ratios. Soil Biol Biochem 37:1718–1725. doi: 10.1016/j.soilbio.2005.02.006 CrossRefGoogle Scholar
  6. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. doi: 10.1111/j.1442-9993.1993.tb00438.x CrossRefGoogle Scholar
  7. De Ruiter PC, Neutel AM, Moore JC (1995) Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269:1257–1260. doi: 10.1126/science.269.5228.1257 CrossRefPubMedGoogle Scholar
  8. De Ruiter PC, Neutel AM, Moore JC (1998) Biodiversity in soil ecosystems: the role of energy flow and community stability. Appl Soil Ecol 10:217–228. doi: 10.1016/S0929-1393(98)00121-8 CrossRefGoogle Scholar
  9. Dicks LV, Corbet SA, Pywell RF (2002) Compartmentalization in plant-insect flower visitor webs. J Anim Ecol 71:32–43. doi: 10.1046/j.0021-8790.2001.00572.x CrossRefGoogle Scholar
  10. Dijkstra P, Ishizu A, Doucett R, Hart SC, Schwartz E, Menyailo OV, Hungate BA (2006) 13C and 15N natural abundance of the soil microbial biomass. Soil Biol Biochem 38:3257–3266. doi: 10.1016/j.soilbio.2006.04.005 CrossRefGoogle Scholar
  11. Ehleringer JR, Buchmann N, Flanagan LB (2000) Carbon isotope ratios in belowground carbon cycle processes. Ecol Appl 10:412–422. doi: 10.1890/1051-0761(2000)010[0412:CIRIBC]2.0.CO;2 CrossRefGoogle Scholar
  12. Fonseca CR, Ganade G (1996) Asymmetries, compartments and null interactions in an Amazonian ant-plant community. J Anim Ecol 65:339–347. doi: 10.2307/5880 CrossRefGoogle Scholar
  13. Halaj J, Peck RW, Niwa CG (2005) Trophic structure of a macroarthropod litter food web in managed coniferous forest stands: a stable isotope analysis with δ15N and δ13C. Pedobiologia (Jena) 49:109–118. doi: 10.1016/j.pedobi.2004.09.002 CrossRefGoogle Scholar
  14. Hart SC, Gehring CA, Selmants PC, Deckert RJ (2006) Carbon and nitrogen elemental and isotopic patterns in macrofungal sporocarps and trees in semiarid forests of the south-western USA. Funct Ecol 20:42–51. doi: 10.1111/j.1365-2435.2005.01058.x CrossRefGoogle Scholar
  15. Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218. doi: 10.1146/annurev.ecolsys.36.112904.151932 CrossRefGoogle Scholar
  16. Hishi T, Hyodo F, Saitoh S, Takeda H (2007) The feeding habits of collembolan along decomposition gradients using stable carbon and nitrogen isotope analyses. Soil Biol Biochem 39:1820–1823. doi: 10.1016/j.soilbio.2007.01.028 CrossRefGoogle Scholar
  17. Högberg P (1997) Tansley review No. 95 15N natural abundance in soil-plant systems. New Phytol 137:179–203. doi: 10.1046/j.1469-8137.1997.00808.x CrossRefGoogle Scholar
  18. Hyodo F, Tayasu I, Konaté S, Tondoh JE, Lavelle P, Wada E (2008) Gradual enrichment of 15N with humification of diets in a below-ground food web: relationship between 15Nand diet age determined using 14C. Funct Ecol 22:516–522. doi: 10.1111/j.1365-2435.2008.01386.x CrossRefGoogle Scholar
  19. Ikeda H, Kubota K, Kagaya T, Abe T (2007) Flight capabilities and feeding habits of silphine beetles: are flightless species really “carrion beetles”? Ecol Res 22:237–241. doi: 10.1007/s11284-006-0012-1 CrossRefGoogle Scholar
  20. Ingham ER, Coleman DC, Moore JC (1989) An analysis of food-web structure and function in a shortgrass prairie, a mountain meadow, and a lodgepole pine forest. Biol Fertil Soils 8:29–37. doi: 10.1007/BF00260513 CrossRefGoogle Scholar
  21. Kohzu A, Yoshioka T, Ando T, Takahashi M, Koba K, Wada E (1999) Natural 13C and 15N abundance of field-collected fungi and their ecological implications. New Phytol 144:323–330. doi: 10.1046/j.1469-8137.1999.00508.x CrossRefGoogle Scholar
  22. Krause AE, Frank KA, Mason DM, Ulanowicz RE, Taylor WW (2003) Compartments revealed in food-web structure. Nature 426:282–285. doi: 10.1038/nature02115 CrossRefPubMedGoogle Scholar
  23. Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48. doi: 10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2 CrossRefPubMedGoogle Scholar
  24. May RM (1972) Will a large complex system be stable? Nature 238:413–414. doi: 10.1038/238413a0 CrossRefPubMedGoogle Scholar
  25. May RM (1973) Stability and complexity in model ecosystems. Princeton University Press, PrincetonGoogle Scholar
  26. McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798. doi: 10.1038/27427 CrossRefGoogle Scholar
  27. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390. doi: 10.1034/j.1600-0706.2003.12098.x CrossRefGoogle Scholar
  28. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140. doi: 10.1016/0016-7037(84)90204-7 CrossRefGoogle Scholar
  29. Moore JC, Walter DE, Hunt HW (1988) Arthropod regulation of micro- and mesobiota in below-ground detrital food webs. Annu Rev Entomol 33:419–439Google Scholar
  30. Paine RT (1980) Food webs: linkage, interaction strength and community infrastructure. J Anim Ecol 49:667–685. doi: 10.2307/4220 Google Scholar
  31. Petersen H, Luxton M (1982) A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 39:288–388. doi: 10.2307/3544689 CrossRefGoogle Scholar
  32. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320. doi: 10.1146/ CrossRefGoogle Scholar
  33. Pimm SL (1979) The structure of food webs. Theor Popul Biol 16:144–158. doi: 10.1016/0040-5809(79)90010-8 CrossRefPubMedGoogle Scholar
  34. Pimm SL, Lawton JH (1980) Are food webs divided into compartments? J Anim Ecol 49:879–898. doi: 10.2307/4233 CrossRefGoogle Scholar
  35. Ponge JF (2003) Humus forms in terrestrial ecosystems: a framework to biodiversity. Soil Biol Biochem 35:935–945. doi: 10.1016/S0038-0717(03)00149-4 CrossRefGoogle Scholar
  36. Ponsard S, Arditi R (2000) What can stable isotopes (delta N-15 and delta C-13) tell about the food web of soil macro-invertebrates? Ecology 81:852–864Google Scholar
  37. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718Google Scholar
  38. Post DM, Conners ME, Goldberg DS (2000) Prey preference by a top predator and the stability of linked food chains. Ecology 81:8–14Google Scholar
  39. Raffaelli D, Hall SJ (1992) Compartments and predation in an estuarine food web. J Anim Ecol 61:551–560. doi: 10.2307/5610 CrossRefGoogle Scholar
  40. Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature 442:265–269. doi: 10.1038/nature04887 CrossRefPubMedGoogle Scholar
  41. Scheu S (2002) The soil food web: structure and perspectives. Eur J Soil Biol 38:11–20. doi: 10.1016/S1164-5563(01)01117-7 CrossRefGoogle Scholar
  42. Scheu S, Falca M (2000) The soil food web of two beech forests (Fagus sylvatica) of contrasting humus type: stable isotope analysis of a macro- and mesofauna-dominated community. Oecologia 123:285–296. doi: 10.1007/s004420051015 CrossRefGoogle Scholar
  43. Scheu S, Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone: manipulation of food resources. Ecology 79:1573–1585CrossRefGoogle Scholar
  44. Schneider K, Migge S, Norton RA, Scheu S, Langel R, Reineking A, Maraun M (2004) Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15N/14N). Soil Biol Biochem 36:1769–1774. doi: 10.1016/j.soilbio.2004.04.033 CrossRefGoogle Scholar
  45. Schröter D, Wolters V, De Ruiter PC (2003) C and N mineralisation in the decomposer food webs of a European forest transect. Oikos 102:294–308. doi: 10.1034/j.1600-0579.2003.12064.x CrossRefGoogle Scholar
  46. Setälä H, Aarnio T (2002) Vertical stratification and trophic interactions among organisms of a soil decomposer food web—a field experiment using 15N as a tool. Eur J Soil Biol 38:29–34. doi: 10.1016/S1164-5563(01)01119-0 CrossRefGoogle Scholar
  47. Sota T (1985) Activity patterns, diets and interspecific interactions of coexisting spring and autumn breeding carabids: Carabus yaconinus and Leptocarabus kumagaii (Coleoptera, Carabidae). Ecol Entomol 10:315–324. doi: 10.1111/j.1365-2311.1985.tb00728.x CrossRefGoogle Scholar
  48. Sticht C, Schrader S, Giesemann A (2006) Influence of chemical agents commonly used for soil fauna investigations on the stable C-isotopic signature of soil animals. Eur J Soil Biol 42:S326–S330. doi: 10.1016/j.ejsobi.2006.07.009 CrossRefGoogle Scholar
  49. Tayasu I, Abe T, Eggleton P, Bignell DE (1997) Nitrogen and carbon isotope ratios in termites: an indicator of trophic habit along the gradient from wood-feeding to soil-feeding. Ecol Entomol 22:343–351. doi: 10.1046/j.1365-2311.1997.00070.x CrossRefGoogle Scholar
  50. Tiunov AV (2007) Stable isotopes of carbon and nitrogen in soil ecological studies. Biol Bull 34:395–407. doi: 10.1134/S1062359007040127 CrossRefGoogle Scholar
  51. Uchida T, Kaneko N, Ito MT, Futagami K, Sasaki T, Sugimoto A (2004) Analysis of the feeding ecology of earthworms (Megascolecidae) in Japanese forests using gut content fractionation and δ15N and δ13C stable isotope natural abundances. Appl Soil Ecol 27:153–163. doi: 10.1016/j.apsoil.2004.04.003 CrossRefGoogle Scholar
  52. Van Veen FJF, Müller CB, Pell JK, Godfray HCJ (2008) Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids. J Anim Ecol 77:191–200. doi: 10.1111/j.1365-2656.2007.01325.x CrossRefPubMedGoogle Scholar
  53. Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066Google Scholar
  54. Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182. doi: 10.1007/s00442-003-1270-z CrossRefPubMedGoogle Scholar

Copyright information

© The Ecological Society of Japan 2009

Authors and Affiliations

  • Yutaka Okuzaki
    • 1
  • Ichiro Tayasu
    • 2
  • Noboru Okuda
    • 2
  • Teiji Sota
    • 1
  1. 1.Department of Zoology, Graduate School of ScienceKyoto UniversityKyotoJapan
  2. 2.Center for Ecological ResearchKyoto UniversityOtsuJapan

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