Abstract
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.
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References
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
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
Briand F, Cohen JE (1984) Community food webs have scale-invariant structure. Nature 307:264–267. doi:10.1038/307264a0
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
May RM (1972) Will a large complex system be stable? Nature 238:413–414. doi:10.1038/238413a0
May RM (1973) Stability and complexity in model ecosystems. Princeton University Press, Princeton
McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798. doi:10.1038/27427
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
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
Moore JC, Walter DE, Hunt HW (1988) Arthropod regulation of micro- and mesobiota in below-ground detrital food webs. Annu Rev Entomol 33:419–439
Paine RT (1980) Food webs: linkage, interaction strength and community infrastructure. J Anim Ecol 49:667–685. doi:10.2307/4220
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
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320. doi:10.1146/annurev.es.18.110187.001453
Pimm SL (1979) The structure of food webs. Theor Popul Biol 16:144–158. doi:10.1016/0040-5809(79)90010-8
Pimm SL, Lawton JH (1980) Are food webs divided into compartments? J Anim Ecol 49:879–898. doi:10.2307/4233
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
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 81:852–864
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718
Post DM, Conners ME, Goldberg DS (2000) Prey preference by a top predator and the stability of linked food chains. Ecology 81:8–14
Raffaelli D, Hall SJ (1992) Compartments and predation in an estuarine food web. J Anim Ecol 61:551–560. doi:10.2307/5610
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
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
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
Scheu S, Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone: manipulation of food resources. Ecology 79:1573–1585
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
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
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
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
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
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
Tiunov AV (2007) Stable isotopes of carbon and nitrogen in soil ecological studies. Biol Bull 34:395–407. doi:10.1134/S1062359007040127
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
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
Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066
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
Acknowledgments
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).
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Okuzaki, Y., Tayasu, I., Okuda, N. et al. Vertical heterogeneity of a forest floor invertebrate food web as indicated by stable-isotope analysis. Ecol Res 24, 1351–1359 (2009). https://doi.org/10.1007/s11284-009-0619-0
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DOI: https://doi.org/10.1007/s11284-009-0619-0