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The structure of a food web in a tropical rain forest in Malaysia based on carbon and nitrogen stable isotope ratios

Published online by Cambridge University Press:  29 January 2010

Fujio Hyodo*
Affiliation:
Research Core for Interdisciplinary Sciences, Okayama University, 3-1-1, Tsushimanaka, Okayama, 700-8530, Japan
Takashi Matsumoto
Affiliation:
Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu, Sakyo-ku, Kyoto 606-8501, Japan
Yoko Takematsu
Affiliation:
Department of Biological Environmental Sciences, Yamaguchi University, 1677-1, Yoshida, Yamaguchi, 735-5838, Japan
Tamaki Kamoi
Affiliation:
Faculty of Agriculture, Ehime University, 3-5-7. Tarumi, Matsuyama 790-8566, Japan
Daisuke Fukuda
Affiliation:
Center for Ecological Research, Kyoto University, 2-509-3, Hirano, Otsu, Shiga, 520-2113, Japan
Michiko Nakagawa
Affiliation:
Graduate School of Agricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
Takao Itioka
Affiliation:
Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu, Sakyo-ku, Kyoto 606-8501, Japan
*
1Corresponding author. Email: [email protected]

Abstract:

Carbon and nitrogen stable isotope ratios (δ13C and δ15N) have been used to study the structure of food webs. However, few studies have examined how a terrestrial food web can be depicted by this technique. We measured δ13C and δ15N in various consumers of four trophic groups (detritivores, herbivores, omnivores and predators), including vertebrates and invertebrates (14 orders, ≥24 families), as well as canopy and understorey leaves in a tropical rain forest in Malaysia. We found that δ13C and δ15N of the consumers differed significantly among the trophic groups. The predators had significantly higher δ13C than the herbivores, and were similar in δ13C to the detritivores, suggesting that most predators examined depend largely on below-ground food webs. δ15N was higher in predators than detritivores by about 3‰. The comparison of δ13C in plant materials and herbivores suggests that most herbivores are dependent on C fixed in the canopy layers. The vertebrates had significantly higher δ15N and δ13C than the invertebrates of the same trophic group, likely reflecting differences in the physiological processes and/or feeding habits. This study indicates that stable isotope techniques can help better understanding of the terrestrial food webs in terms of both trophic level and the linkage of above- and below-ground systems.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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References

LITERATURE CITED

AMBROSE, S. H. & DENIRO, M. J. 1986. The isotopic ecology of East-African mammals. Oecologia 69:395406.CrossRefGoogle ScholarPubMed
BIRKHOFER, K., WISE, D. H. & SCHEU, S. 2008. Subsidy from the detrital food web, but not microhabitat complexity, affects the role of generalist predators in an aboveground herbivore food web. Oikos 117:494500.CrossRefGoogle Scholar
BOCHERENS, H. & DRUCKER, D. 2003. Trophic level isotopic enrichment of carbon and nitrogen in bone collagen: case studies from recent and ancient terrestrial ecosystems. International Journal of Osteoarchaeology 13:4653.CrossRefGoogle Scholar
BOURGUIGNON, T., SABOTNIK, J., LEPOINT, G., MARTIN, J. M. & ROISIN, Y. 2009. Niche differentiation among neotropical soldierless soil-feeding termites revealed by stable isotope ratios. Soil Biology & Biochemistry 41:20382043.CrossRefGoogle Scholar
BRIONES, M. J. I., BOL, R., SLEEP, D., SAMPEDRO, L. & ALLEN, D. 1999. A dynamic study of earthworm feeding ecology using stable isotopes. Rapid Communications in Mass Spectrometry 13:13001304.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
DAVIDSON, D. W., COOK, S. C., SNELLING, R. R. & CHUA, T. H. 2003. Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969972.CrossRefGoogle ScholarPubMed
DAVIES, R. G. 1988. Outlines of entomology (Seventh edition). Chapman and Hall, London. 408 pp.Google Scholar
DAWSON, T. E., MAMBELLI, S., PLAMBOECK, A. H., TEMPLER, P. H. & TU, K. P. 2002. Stable isotopes in plant ecology. Annual Review of Ecology and Systematics 33:507559.CrossRefGoogle Scholar
DENIRO, M. J. & EPSTEIN, S. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42:495506.CrossRefGoogle Scholar
DOI, H., KIKUCHI, E., TAKAGI, S. & SHIKANO, S. 2007. Changes in carbon and nitrogen stable isotopes of chironomid larvae during growth, starvation and metamorphosis. Rapid Communications in Mass Spectrometry 21:9971002.CrossRefGoogle ScholarPubMed
DUFFY, J. E., CARINALE, B. J., FRANCE, K. E., MCINTYRE, P. B., THEBAULT, E. & LOREAU, M. 2007. The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecology Letters 10:522538.CrossRefGoogle ScholarPubMed
FRY, B. 2006. Stable isotope ecology. Springer, New York. 308 pp.CrossRefGoogle Scholar
FUKUDA, D., TISEN, O. B., MOMOSE, K. & SAKAI, S. 2009. Bat diversity in the vegetation mosaic around a lowland dipterocarp forest of Borneo. Raffles Bulletin of Zoology 57:213221.Google Scholar
GARTEN, C. T. & TAYLOR, G. E. 1992. Foliar δ13C within a temperature deciduous forest – spatial, temporal, and species sources of variation. Oecologia 90:17.CrossRefGoogle ScholarPubMed
GRAFEN, A. & HAILS, R. 2002. Modern statistics for life sciences. Oxford University Press, Oxford. 368 pp.Google Scholar
GREY, J. & JONES, R. I. 2001. Seasonal changes in the importance of the source of organic matter to the diet of zooplankton in Loch Ness, as indicated by stable isotope analysis. Limnology and Oceanography 46:505513.CrossRefGoogle Scholar
HAIRSTON, N. G., SMITH, F. E. & SLOBODKIN, L. B. 1960. Community structure, population control, and competition. American Naturalist 94:421425.CrossRefGoogle Scholar
HALAJ, J. & WISE, D. H. 2002. Impact of a detrital subsidy on trophic cascades in a terrestrial grazing food web. Ecology 83:31413151.CrossRefGoogle Scholar
HANBA, Y. T., MORI, S., LEI, T. T., KOIKE, T. & WADA, E. 1997. Variations in leaf δ13C along a vertical profile of irradiance in a temperate Japanese forest. Oecologia 110:253261.CrossRefGoogle Scholar
HERRERA, L. G., GUTIERRES, E., HOBSON, K. A., ALTUBE, B., GIAZ, W. G. & SANCHEZ-CORDERO, V. 2002. Sources of assimilated protein in five species of New World frugivorous bats. Oecologia 133:280287.CrossRefGoogle ScholarPubMed
HISHI, T., HYODO, F., SAITOH, S. & TAKEDA, H. 2007. The feeding habits of collembola along decomposition gradients using stable carbon and nitrogen isotope analyses. Soil Biology and Biochemistry 39:18201823.CrossRefGoogle Scholar
HOBBIE, E. A., MACKO, S. A. & SHUGART, H. H. 1999. Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118:353360.CrossRefGoogle ScholarPubMed
HOBSON, K. A., SCHELL, D. M., RENOUF, D. & NOSEWORTHY, E. 1996. Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Canadian Journal of Fisheries and Aquatic Sciences 53:528533.CrossRefGoogle Scholar
HYODO, F., TAYASU, I., INOUE, T., AZUMA, J.-I. & KUDO, T. 2003. Differential role of symbiotic fungi in lignin degradation and food provision for fungus-growing termites (Macrotermitinae: Isoptera). Functional Ecology 17:186193.CrossRefGoogle Scholar
HYODO, F., TAYASU, I. & 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 20:385393.CrossRefGoogle Scholar
HYODO, F., TAYASU, I., KONATE, S., TONDOH, J. E., LAVELLE, P. & WADA, E. 2008. Gradual enrichment of 15N with humification of diets in a below-ground food web: relationship between 15N and diet age determined using 14C. Functional Ecology 22:516522.CrossRefGoogle Scholar
ILLIG, J., LANGEL, R., NORTON, R. A., SCHEU, S. & MARAUN, M. 2005. Where are the decomposers? Uncovering the soil food web of a tropical montane rain forest in southern Ecuador using stable isotopes (N-15). Journal of Tropical Ecology 21:589593.CrossRefGoogle Scholar
KAMOI, T. 2007. Reproductive ecology of tropical pioneer plants. Masters thesis of Graduate School of Agriculture, Ehime University.Google Scholar
KOHZU, A., MIYAJIMA, T., TATEISHI, T., WATANABE, T., TAKAHASHI, M. & WADA, E. 2005. Dynamics of 13C natural abundance in wood decomposing fungi and their ecophysiological implications. Soil Biology & Biochemistry 37:15981607.CrossRefGoogle Scholar
KUPFER, A., LANGEL, R., SCHEU, S., HIMSTEDT, W. & MARAUN, M. 2006. Trophic ecology of a tropical aquatic and terrestrial food web: insights from stable isotopes (15N). Journal of Tropical Ecology 22:469476.CrossRefGoogle Scholar
MCCUTCHAN, J. H., LEWIS, W. M., KENDALL, C. & MCGRATH, C. C. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378390.CrossRefGoogle Scholar
MINAGAWA, M. & WADA, E. 1984. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48:11351140.CrossRefGoogle Scholar
MIYASHITA, T., TAKADA, M. & SHIMAZAKI, A. 2003. Experimental evidence that aboveground predators are sustained by underground detritivores. Oikos 103:3136.CrossRefGoogle Scholar
NADELHOFFER, K. J. & FRY, B. 1988. Controls on natural nitrogen-15 and carbon-13 abundances in forest soil organic matter. Soil Science Society of America Journal 52:16331640.CrossRefGoogle Scholar
NAKAGAWA, M., TANAKA, K., NAKASHIZUKA, T., OHKUBO, T., KATO, T., MAEDA, T., SATO, K., MIGUCHI, H., NAGAMASU, H., OGINO, K., TEO, S., HAMID, A. A. & LEE, H.S. 2000. Impact of severe drought associated with the 1997–1998 El Nino in a tropical forest in Sarawak. Journal of Tropical Ecology 16:355367.CrossRefGoogle Scholar
NAKAGAWA, M., HYODO, F. & NAKASHIZUKA, T. 2007. Effect of forest use on trophic levels of small mammals: an analysis using stable isotopes. Canadian Journal of Zoology 85:472478.CrossRefGoogle Scholar
ODUM, E. P. 1969. Strategy of ecosystem development. Science 164:262270.CrossRefGoogle ScholarPubMed
OELBERMANN, K. & SCHEU, S. 2002. Stable isotope enrichment (δ15N and δ13C) in a generalist predator (Pardosa lugubris, Araneae: Lycosidae): effects of prey quality. Oecologia 130:337344.CrossRefGoogle Scholar
OKSANEN, L. 1997. Outlines of food webs in a low arctic tundra landscape in relation to three theories on trophic dynamics. Pp. 351373 in Gange, A. C. & Brown, V. K. (eds.). Multitrophic interactions in terrestrial systems. Blackwell, Oxford.Google Scholar
OSADA, N., TAKEDA, H., FURUKAWA, A. & AWANG, M. 2001. Leaf dynamics and maintenance of tree crowns in a Malaysian rain forest stand. Journal of Ecology 89:774782.CrossRefGoogle Scholar
OSTROM, P. H., COLUNGA-GARCIA, M. & GAGE, S. H. 1997. Establishing pathways of energy flow for insect predators using stable isotope ratios: field and laboratory evidence. Oecologia 109:108113.CrossRefGoogle Scholar
PARK, H. H. & LEE, J. H. 2006. Arthropod trophic relationships in a temperate rice ecosystem: a stable isotope analysis with δ13C and δ15N. Environmental Entomology 35:684693.CrossRefGoogle Scholar
PAYNE, J., FRANCIS, C. M. & PHILLIPS, K. 1985. A field guide to the mammals of Borneo. The Sabah Society, Kota Kinabalu. 332 pp.Google Scholar
POLIS, G. & STRONG, D. R. 1996. Food web complexity and community dynamics. American Naturalist 147:813846.CrossRefGoogle Scholar
POLLIERER, M. M., LANGEL, R., SCHEU, S. & MARAUN, M. 2009. Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (15N/14N and 13C/12C). Soil Biology & Biochemistry 41:12211226.CrossRefGoogle Scholar
PONSARD, S. & ARDITI, R. 2000. What can stable isotopes (δ15N and δ13C) tell about the food web of soil macro-invertebrates? Ecology 81:852864.Google Scholar
POST, D. M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703718.CrossRefGoogle Scholar
PRICE, P. W. 1997. Insect ecology. Wiley, New York. 874 pp.Google Scholar
REAGAN, D. P., CAMILO, G. R. & WAIDE, R. B. 1996. The community food web: major properties and patterns of organization. Pp. 461510 in Reagan, D. P. & Waide, R. B. (eds.). The food web of a tropical rain forest. The University of Chicago Press, Chicago.Google Scholar
SCHEU, S. 2001. Plants and generalist predators as links between the below-ground and above-ground system. Basic and Applied Ecology 2:313.CrossRefGoogle Scholar
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 a mesofauna-dominated community. Oecologia 123:285296.CrossRefGoogle Scholar
SCHMIDT, O., CURRY, J. P., DYCKMANS, J., ROTA, E. & SCRIMGEOUR, C. M. 2004. Dual stable isotope analysis (δ13C and δ15N) of soil invertebrates and their food sources. Pedobiologia 48:171180.CrossRefGoogle Scholar
SETTLE, W. H., ARIAWAN, H., ASTUTI, E. T., CAHYANA, W., HAKIM, A. L., HINDAYANA, D., LESTARI, A. S., PAJARNINGSIH, & SARTANTO, . 1996. Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77:19751988.CrossRefGoogle Scholar
SMYTHIES, B. E. 1999. Birds of Borneo. (Fourth edition). Natural History Publications (Borneo), Kota Kinabalu. 853 pp.Google Scholar
SPAIN, A. V. & REDDELL, P. 1996. δ13C values of selected termites (Isoptera) and termite-modified materials. Soil Biology & Biochemistry 28:15851593.CrossRefGoogle Scholar
SPENCE, K. O. & ROSENTHEIM, J. A. 2005. Isotopic enrichment in herbiorous insects: a comparative field-based study of variation. Oecologia 146:8997.CrossRefGoogle ScholarPubMed
SWIFT, M. J., HEAL, O. W. & ANDERSON, J. M. 1979. Decomposition in terrestrial ecosystems. Blackwell Scientific Publications, Oxford. 372 pp.CrossRefGoogle Scholar
TAYASU, I., ABE, T., EGGLETON, P. & BIGNELL, D. E. 1997. Nitrogen and carbon isotope ratios in termites: an indicator of trophic habit along the gradient from wood-feeding to soil-feeding. Ecological Entomology 22:343351.CrossRefGoogle Scholar
THEBAULT, E. & LOREAU, M. 2003. Food-web constraints on biodiversity-ecosystem functioning relationships. Proceedings of the National Academy of Sciences USA 100:1494914954.CrossRefGoogle ScholarPubMed
TIESZEN, L. L. & BOUTTON, T. W. 1989. Stable carbon isotopes in terrestrial ecosystem research. Pp. 167195 in Rundel, P. W., Ehleringer, J. R. & Nagy, K. A. (eds.). Stable isotopes in ecological research. Springer-Verlag, New York.CrossRefGoogle Scholar
TIESZEN, L. L., BOUTTON, T. W., TESDAHL, K. G. & SLADE, N. A. 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:3237.CrossRefGoogle ScholarPubMed
VANDERKLIFT, M. A. & PONSARD, S. 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169182.CrossRefGoogle ScholarPubMed
WARDLE, D. A. 2002. Communities and ecosystems: linking the aboveground and belowground components. Princeton University Press, Oxford. 392 pp.Google Scholar
WHITMORE, T. C. 1984. Tropical rain forests of the Far East. Clarendon Press, Oxford. 352 pp.Google Scholar
WISE, D. H., MOLDENHAUER, D. M. & HALAJ, J. 2006. Using stable isotopes to reveal shifts in prey consumption by generalist predators. Ecological Applications 16:865876.CrossRefGoogle ScholarPubMed
YOSHII, K., MELNIK, N. G., TIMOSHKIN, O. A., BONDARENKO, N. A., ANOSHKO, P. N., YOSHIOKA, T. & WADA, E. 1999. Stable isotope analyses of the pelagic food web in Lake Baikal. Limnology and Oceanography 44:502511.CrossRefGoogle Scholar
YUMOTO, T. & NAKASHIZUKA, T. 2005. The canopy biology program in Sarawak: scope, methods, and merit. Pp. 1321 in Roubik, D. W., Sakai, S. & Hamid, A. A. (eds.). Pollination ecology and the rain forest. Springer, New York.CrossRefGoogle Scholar