Abstract
Despite the recognition of the functional role of Hymenoptera (ants, bees and wasps) and Isoptera (termites) in tropical ecosystems, their detailed feeding habits are not well known. To examine the feeding habits of these groups, we measured nitrogen (N) and carbon (C) stable isotope ratios (δ15N and δ13C) of hymenopterans (12 families, ≥16 genera and ≥32 species) and isopterans (one family and 10 species) collected in a tropical rain forest, Sarawak, Malaysia. We compared the isotopic signatures of these insects to those previously reported for other consumers collected in the same forest. The δ15N and δ13C values of these insects overlapped with those of the other consumers, indicating that they have access to diverse C and N sources in the forest. The δ15N values of ants and termites indicated that their feeding habits range along a continuum from herbivory (i.e. dependent on honeydew and nectar) to predation and from wood-feeders to soil-feeders, respectively. In addition, the δ15N values of wasps varied greatly from −0.1‰ (Braconidae sp.) to 8.6‰ (Bembix sp.), suggesting that their feeding habits also range from omnivory to predation. The ant species Camponotus gigas had δ13C values similar to those of invertebrate detritivores and omnivores rather than to those of invertebrate herbivores, although the diet of this species consists mostly of honeydew. This discrepancy suggests that the ant uses carbohydrates as an energy source, the isotopic signatures of which are not well retained in the body tissues. Values of both δ15N and δ13C of the predatory army ant Leptogenys diminuta and the soil-feeding termite Dicuspiditermes nemorosus did not differ significantly, indicating that both trophic level and the humification of feeding substrates can increase the isotopic signatures of terrestrial consumers.
Similar content being viewed by others
References
Abe T. 1979. Studies on the distribution and ecological role of termites in a lowland rain forest of West Malaysia (2) Food and feeding habits of termites in Pasoh Forest Reserve. Jap. J. Ecol. 29: 121-135
Abe T., Bignell D.E. and Higashi M. 2000. Termites: Evolution, Sociality, Symbiosis, Ecology. Kluwer Academic Publishers, Dordrecht. 488 pp
Ambrose S.H. and Norr L. 1993. Carbon isotopic evidence for routing of dietary protein to bone collagen, and whole diet to bone apatite carbonate: purified diet growth experiments. In: Molecular Archaeology of Prehistoric Human Bone (Lambert J. and Grupe G., Eds). Springer-Verlag, Berlin, Germany. pp 1-37
Baker H. and Baker I. 1986. The occurrence and significance of amino acids in floral nectar. Plant Syst. Evol. 151: 175-186
Bignell D.E. and Eggleton P. 2000. Termites in ecosystems. In: Termites: Evolution, Sociality, Symbiosis, Ecology (Abe T., Bignell D.E. and Higashi M., Eds). Kluwer Academic Publishers, Dordrecht. pp 363-387
Blüthgen N. and Fiedler K. 2002. Interactions between weaver ants Oecophylla smaragdina, homopterans, trees and lianas in an Australian rain forest canopy. J. Anim. Ecol. 71: 793-801
Blüthgen N., Gebauer G. and Fiedler K. 2003. Disentangling a rainforest food web using stable isotopes: dietary diversity in a species-rich ant community. Oecologia 137: 426-435
Blüthgen N., Gottsberger G. and Fiedler K. 2004. Sugar and amino acid composition of ant-attended nectar and honeydew sources from an Australian rainforest. Austral Ecol. 29: 418-429
Bohart R.M. and Menke A.S. 1976. Sphecid Wasps of the World. University of California Press, Berkeley. 600 pp
Bourguignon T., Šobotník J., Lepoint G., Martin J.M. and Roisin Y. 2009. Niche differentiation among neotropical soldierless soil-feeding termites revealed by stable isotope ratios. Soil Biol. Biochem. 41: 2038-2043
Breznak J.A. and Brune A. 1994. Role of microorganisms in the digestion of lignocellulose by termites. Annu. Rev. Entomol. 39: 453-487
Brian M.V. 1978. Production Ecology of Ants and Termites. Cambridge University Press, Cambridge. 409 pp
Buschinger A., Klein R.W. and Maschwitz U. 1994. Colony structure of a bamboo-dwelling Tetraponera sp. (Hymenoptera: Formicidae: Pseudomyrmecinae) from Malaysia. Insect. Soc. 41: 29-41
Davidson D.W., Cook S.C., Snelling R.R. and Chua T.H. 2003. Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300: 969-972
DeNiro M.J. and Epstein S. 1977. Mechanism of carbon isotope fractionation associated with lipid-synthesis. Science 197: 261-263
DeNiro M.J. and Epstein S. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 42: 495-506
Eggleton P., Homathevi R., Jones D.T., MacDonald J.A., Jeeva D., Bignell D.E., Davies R.G. and Maryati M. 1999. Termite assemblages, forest disturbance and greenhouse gas fluxes in Sabah, East Malaysia. Phil. Trans. R. Soc. B 354: 1791-1802
Feldhaar H., Gebauer G. and Blüthgen N. 2010. Stable isotopes: past and future in exposing secrets of ant nutrition (Hymenoptera: Formicidae). Myrmecol. News 13: 3-13
Fiala B., Maschwitz U., Tho Y.P. and Helbig A.J. 1989. Studies of a South East Asian ant-plant association - protection of Macaranga trees by Crematogaster borneensis. Oecologia 79: 463-470
Fittkau E.J. and Klinge H. 1973. On biomass and trophic structure of the central Amazonian rain forest ecosystem. Biotropica 5: 2-14
Fry B. 2006. Stable Isotope Ecology. Springer, New York. 308 pp
Gadagkar R. 1991. Belonogaster, Mischocyttarus, Parapolybia, and independent-founding Ropalidia. In: The Social Biology of Wasps (Ross K.G. and Matthews R.W., Eds). Cornell University Press, Ithaca and London. pp 149-190
Gannes L.Z., O’Brien D.M. and Martínez del Rio C. 1997. Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78: 1271-1276
Grimaldi D. and Engel M.S. 2005. Evolution of the Insects. Cambridge University Press, Cambridge, U.K. 755 pp
Heil M., Fiala B., Kaiser W. and Linsenmair K.E. 1998. Chemical contents of Macaranga food bodies: adaptations to their role in ant attraction and nutrition. Funct. Ecol. 12: 117-122
Higashi M. and Abe T. 1996. Global diversification of termites driven by the evolution of symbiosis and sociality. In: Biodiversity: An Ecological Perspective (Abe T., Levin S.A. and Higashi M., Eds). Springer-Verlag, New York. pp 83-112
Hobbie E.A. and Werner R.A. 2004. Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis. New Phytol. 161: 371-385
Hölldobler B. and Wilson E.O. 1990. The Ants. Belknap Press of Harvard University Press, Cambridge. 732 pp
Hyodo F., Kohzu A. and Tayasu I. 2010a. Linking aboveground and belowground food webs through carbon and nitrogen stable isotope analyses. Ecol. Res. 25: 745-756
Hyodo F., Matsumoto T., Takematsu Y., Kamoi T., Fukuda D., Nakagawa M. and Itioka T. 2010b. The structure of a food web in a tropical rain forest in Malaysia based on carbon and nitrogen stable isotope ratios. J. Trop. Ecol. 26: 205-214
Hyodo F., Tayasu I., Inoue T., Azuma J.-I. and Kudo T. 2003. Differential role of symbiotic fungi in lignin degradation and food provision for fungus-growing termites (Macrotermitinae: Isoptera). Funct. Ecol. 17: 186-193
Hyodo F., Tayasu I., Konate S., Tondoh J.E., Lavelle P. and 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. Funct. Ecol. 22: 516-522
Inui Y., Tanaka H.O., Hyodo F. and Itioka T. 2009. Within-nest abundance of a tropical cockroach Pseudoanaplectinia yumotoi associated with Crematogaster ants inhabiting epiphytic fern domatia in a Bornean dipterocarp forest. J. Nat. Hist. 43: 1139-1145
Itino T., Davies S.J., Tada H., Hieda O., Inoguchi M., Itioka T., Yamane S. and Inoue T. 2001. Cospeciation of ants and plants. Ecol. Res. 16: 787-793
Jeeva D., Bignell D.E., Eggleton P. and Maryati M. 1999. Respiratory gas exchanges of termites from the Sabah (Borneo) assemblage. Physiol. Entomol. 24: 11-17
Jones D.T. and Gathorne-Hardy F.J. 1995. Foraging activity of the processional termite Hospitalitermes hospitalis (Termitidae, Nasutitermitinae) in the rain-forest of Brunei, North-West Borneo. Insect. Soc. 42: 359-369
Jones D.T. and Praestyo A.H. 2002. A survey of the termites (Insecta: Isoptera) of Tabalong District, south Kalimantan, Indonesia. Raffles Bull. Zool. 50: 117-128
Jones D.T., Rahman H., Bignell D.E. and Prasetyo A.H. 2010. Forests on ultramafic-derived soils in Borneo have very depauperate termite assemblages. J. Trop. Ecol. 26: 103-114
Klein A.M., Steffan-Dewenter I. and Tscharntke T. 2004. Foraging trip duration and density of megachilid bees, eumenid wasps and pompilid wasps in tropical agroforestry systems. J. Anim. Ecol. 73: 517-525
Lindeman R.L. 1942. The trophic-dynamic aspect of ecology. Ecology 23: 399-417
Martin S.J. 1995. Hornets (Hymenoptera: Vespinae) of Malaysia. Malay. Nat. J. 49: 71-82
Maschwitz U. and Mühlenberg M. 1975. Strategy of predation in some oriental Leptogenys species (Formicidae-Ponerinae). Oecologia 20: 65-83
Matsuura K. 1991. Vespa and Provespa. In: The Social Biology of Wasps (Ross K.G. and Matthews R.W., Eds). Cornell University Press, Ithaca. pp 232-262
McCutchan J.H., Lewis W.M., Kendall C. and McGrath C.C. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378-390
Michener C.D. 2000. The Bees of the World. The Johns Hopkins University Press, Baltimore, Md. 913 pp
Minagawa M. and 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
Momose K., Yumoto T., Nagamitsu T., Kato M., Nagamasu H., Sakai S., Harrison R.D., Itioka T., Hamid A.A. and Inoue T. 1998. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Am. J. Bot. 85: 1477-1501
Nadelhoffer K. and Fry B. 1994. Nitrogen isotope studies in forest ecosystems. In: Stable Isotopes in Ecology and Environmental Science (Lajtha K. and Michener R.H., Eds). Blackwell Scientific Publications, Oxford. pp 22-44
O’Neil K.M. 2001. Solitary Wasps: Behavior and Natural History. Cornell University Press, Ithaca. 406 pp
Pfeiffer M. and Linsenmair K.E. 2000. Contributions to the life history of the Malaysian giant ant Camponotus gigas (Hymenoptera, Formicidae). Insect. Soc. 47: 123-132
Pollierer M.M., Langel R., Scheu S. and 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 Biol. Biochem. 41: 1221-1226
Post D.M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703-718
Richter M.R. 2000. Social wasp (Hymenoptera: Vespidae) foraging behavior. Annu. Rev. Entomol. 45: 121-150
Roubik D.W. 1989. Ecology and Natural History of Tropical Bees. Cambridge University Press, New York. 514 pp
Tanaka H.O., Inui Y. and Itioka T. 2009. Anti-herbivore effects of an ant species, Crematogaster difformis, inhabiting myrmecophytic epiphytes in the canopy of a tropical lowland rainforest in Borneo. Ecol. Res. 24: 1393-1397
Tayasu I. 1998. Use of carbon and nitrogen isotope ratios in termite research. Ecol. Res. 13: 377-387
Tayasu I., Abe T., Eggleton P. and 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. Ecol. Entomol. 22: 343-351
Tayasu I., Hyodo F., Takematsu Y., Sugimoto A., Inoue T., Kirtibutr N. and Abe T. 2000. Stable isotope ratios and uric acid preservation in termites belonging to three feeding habits in Thailand. Isotopes Environ. Health Stud. 36: 259-272
Tillberg C.V. and Breed M.D. 2004. Placing an omnivore in a complex food web: Dietary contributions to adult biomass of an ant. Biotropica 36: 266-272
Tillberg C.V., McCarthy D.P., Dolezal A.G. and Suarez A.V. 2006. Measuring the trophic ecology of ants using stable isotopes. Insect. Soc. 53: 65-69
Tilman D. 1982. Resource Competition and Community Structure. Princeton University Press, Princeton, N.J. 296 pp
Van Mele P. and Cuc N.T.T. 2000. Evolution and status of Oecophylla smaragdina (Fabricius) as a pest control agent in citrus in the Mekong Delta, Vietnam. Int. J. Pest Manage. 46: 295-301
Vanderklift M.A. and Ponsard S. 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136: 169-182
Wäckers F.L. 2004. Assessing the suitability of flowering herbs as parasitoid food sources: flower attractiveness and nectar accessibility. Biol. Cont. 29: 307-314
Watanabe H. and Tokuda G. 2010. Cellulolytic systems in insects. Annu. Rev. Entomol. 55: 609-632
Wilson E.O. 1958. The beginnings of nomadic and group-predatory behavior in the Ponerine ants. Evolution 12: 24-31
Yumoto T. and Nakashizuka T. 2005. The canopy biology program in Sarawak: Scope, methods, and merit. In: Pollination Ecology and the Rain Forest (Roubik D.W., Sakai S. and Hamid A.A., Eds). Springer, New York. pp 13-21
Acknowledgments
We thank Josef Kendawang (Forest Department, Sarawak) and Lucy Chong (Sarawak Forestry Corporation) for permission for research in Sarawak. We also thank Tohru Nakashizuka (Tohoku University) and Het Kaliang (Sarawak Forestry Corporation) for kind arrangement to conduct the field sampling, Seiki Yamane (Kagoshima University) for identification of ants and sphecid wasps and helpful discussion, Shuichi Ikudome (Kagoshima Women’s Junior College) for identification of bees and two anonymous reviewers and the Associate Editor for constructive comments on an earlier draft of this manuscript. This study was supported by Research Institute for Humanity and Nature, Japan (P3-1 and P3-5), by Grant-in-Aids (no. 17405006 to T.I., and no. 16405009 to Y.T.) and partly by Special Coordination funds for Promoting Sciences and Technology from the Japanese Ministry of Education, Science, and Culture. F.H. and T.M. were supported by the Research Fellowships of the Japan Society for the Promotion of Science (JSPS) for Young Scientists.
Author information
Authors and Affiliations
Corresponding author
Appendix
Appendix
δ15N and δ13C values of Hymenoptera and Isoptera examined in this study.
No. | Taxa | n | δ15N (‰) | δ13C (‰) | ||||||
---|---|---|---|---|---|---|---|---|---|---|
Mean (SE) | Range (min–max) | Mean (SE) | Range (min–max) | |||||||
Hymenoptera | ||||||||||
Ants | ||||||||||
Formicidae | ||||||||||
1 | Crematogaster borneensis | 5 | −1.2 (0.6) | D | hi | −2.3 to 0.8 | −33.9 (0.7) | C | g | −35.7 to −31.7 |
2 | Crematogaster difformis | 5 | 2.6 (0.5) | B | de | 1.0 to 3.7 | −26.4 (0.2) | A | ab | −27.0 to −25.9 |
3 | Camponotus gigas | 9 | 1.8 (0.4) | B | def | 0.5 to 4.3 | −26.9 (0.2) | A | ab | −27.7 to −26.2 |
4 | Leptogenys diminuta | 3 | 6.3 (0.6) | A | ab | 5.0 to 7.0 | −26.6 (0.2) | A | abc | −26.9 to −26.3 |
5 | Tetraponera attenuata | 16 | 0.3 (0.1) | C | gh | −1.1 to 1.3 | −28.4 (0.2) | B | cdef | −29.8 to −26.3 |
6 | Oecophylla smaragdina | 4 | 3.1 (0.2) | B | d | 2.6 to 3.5 | −26.5 (0.2) | A | ab | −27.1 to −26.0 |
Bees | ||||||||||
Apidae | ||||||||||
7 | Apis spp. | 3 | −2.0 (0.1) | B | ij | −2.2 to −1.7 | −25.4 (0.3) | A | a | −25.8 to −24.7 |
8 | Trigona spp. | 10 | −0.6 (0.1) | A | ghi | −1.5 to 0.0 | −27.2 (0.3) | B | abcd | −28.2 to −25.8 |
Anthophoridae | ||||||||||
9 | Amegilla sp. | 1 | −0.7 | −28.9 | ||||||
Halictidae | ||||||||||
10 | Nomia sp. | 1 | 1.0 | −31.0 | ||||||
11 | Megachilidae sp. | 1 | 1.8 | −23.2 | ||||||
Wasps | ||||||||||
12 | Braconidae sp. | 2 | −0.1 | −0.9 to 0.7 | −26.2 | −26.8 to −25.5 | ||||
13 | Ichneumonidae sp. | 4 | 5.9 (0.9) | AB | bc | 4.0 to 8.0 | −26.9 (0.7) | A | abcd | −28.6 to −24.9 |
Nyssonidae | ||||||||||
14 | Bembix sp. | 3 | 8.3 (0.9) | A | a | 6.7 to 9.9 | −25.4 (0.0) | A | a | −25.5 to −25.3 |
15 | Bembecinus sp. | 3 | 3.6 (0.7) | BC | cd | 2.2 to 4.6 | −26.5 (0.0) | A | ab | −26.6 to −26.5 |
16 | Pompilidae sp. | 2 | 7.4 | 5.4 to 9.4 | −25.3 | −26.1 to −24.5 | ||||
17 | Scoliidae sp. | 1 | 2.8 | −27.3 | ||||||
Sphecidae | ||||||||||
18 | Chalybion bengalense | 1 | 8.3 | −28.4 | ||||||
Vespidae | ||||||||||
19 | Polybioides pescas | 2 | 2.0 | 1.8 to 2.2 | −26.2 | −26.4 to −26.0 | ||||
20 | Provespa anomala | 6 | 2.3 (0.3) | C | def | 1.3 to 3.3 | −26.8 (0.1) | A | ab | −27.3 to −26.0 |
21 | Ropalidia spp. | 3 | 1.1 (0.3) | C | defg | 0.5 to 1.5 | −27.3 (0.4) | A | abcdef | −28.0 to −26.7 |
22 | Vespa affinis | 2 | 6.1 | 5.5 to 6.7 | −26.5 | −26.9 to −26.2 | ||||
Termites | ||||||||||
Isoptera | ||||||||||
Termitidae | ||||||||||
23 | Hospitalitermes hospitalis | 4 | −3.4 (0.3) | E | j | −4.0 to −2.6 | −28.9 (0.4) | B | def | −29.7 to −27.9 |
24 | Macrotermes malaccensis | 5 | −1.6 (0.2) | D | ij | −2.2 to −1.1 | −27.0 (0.4) | A | abcd | −28.4 to −26.1 |
25 | Odontotermes sarawakensis | 1 | 0.3 | −25.4 | ||||||
26 | Odontotermes denticulatus | 1 | 2.1 | −25.9 | ||||||
27 | Microcerotermes sabahensis | 4 | −0.4 (0.3) | CD | ghi | −0.9 to 0.6 | −29.2 (0.3) | B | e | −30.0 to −28.2 |
28 | Longipeditermes longipes | 3 | 0.5 (0.2) | BC | efghi | 0.1 to 0.9 | −29.3 (0.2) | B | ef | −29.6 to −29.0 |
29 | Homallotermes foraminifer | 9 | 0.7 (0.4) | B | fg | −1.0 to 2.6 | −27.6 (0.4) | A | bcdef | −29.6 to -25.9 |
30 | Prohamitermes mirabilis | 9 | 5.9 (0.2) | A | b | 5.1 to 6.6 | −27.5 (0.2) | A | bcdf | −28.1 to −26.7 |
31 | Termes rostratus | 2 | 5.6 | 4.9 to 6.4 | −25.3 | −25.4 to −25.2 | ||||
32 | Dicuspiditermes nemorosus | 4 | 6.7 (0.2) | A | ab | 6.3 to 7.2 | −26.7 (0.2) | A | ab | −27.1 to −26.2 |
Rights and permissions
About this article
Cite this article
Hyodo, F., Takematsu, Y., Matsumoto, T. et al. Feeding habits of Hymenoptera and Isoptera in a tropical rain forest as revealed by nitrogen and carbon isotope ratios. Insect. Soc. 58, 417–426 (2011). https://doi.org/10.1007/s00040-011-0159-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00040-011-0159-9