Termites and ants contribute more to animal biomass in tropical rain forests than any other single group and perform vital ecosystem functions. Although ants prey on termites, at the community level the linkage between these groups is poorly understood. Thus, assessing the distribution and specificity of ant termitophagy is of considerable interest. We describe an approach for quantifying ant-termite food webs by sequencing termite DNA (cytochrome c oxidase subunit II, COII) from ant guts and apply this to a soil-dwelling ant community from tropical rain forest in Gabon. We extracted DNA from 215 ants from 15 species. Of these, 17.2 % of individuals had termite DNA in their guts, with BLAST analysis confirming the identity of 34.1 % of these termites to family level or better. Although ant species varied in detection of termite DNA, ranging from 63 % (5/7; Camponotus sp. 1) to 0 % (0/7; Ponera sp. 1), there was no evidence (with small sample sizes) for heterogeneity in termite consumption across ant taxa, and no evidence for species-specific ant-termite predation. In all three ant species with identifiable termite DNA in multiple individuals, multiple termite species were represented. Furthermore, the two termite species that were detected on multiple occasions in ant guts were in both cases found in multiple ant species, suggesting that ant-termite food webs are not strongly compartmentalised. However, two ant species were found to consume only Anoplotermes-group termites, indicating possible predatory specialisation at a higher taxonomic level. Using a laboratory feeding test, we were able to detect termite COII sequences in ant guts up to 2 h after feeding, indicating that our method only detects recent feeding events. Our data provide tentative support for the hypothesis that unspecialised termite predation by ants is widespread and highlight the use of molecular approaches for future studies of ant-termite food webs.

Global Conservation Program Wildlife Conservation Society Bronx New York 10460 United States of America

Institute of Entomology Biology Centre of Czech Academy of Sciences and Faculty of Science University of South Bohemia Branišovská 31 370 05 České Budějovice Czech Republic

Institute of Entomology Biology Centre of Czech Academy of Sciences and Faculty of Science University of South Bohemia Branišovská 31 370 05 České Budějovice Czech Republic; Forest Ecology and Conservation Group Imperial College London Silwood Park Campus Buckhurst Road Ascot Berkshire SL5 7PY United Kingdom; Institute for Tropical Biology and Conservation Universiti Malaysia Sabah 88400 Kota Kinabalu Sabah Malaysia

Life Sciences Department Natural History Museum Cromwell Road London SW6 5BD United Kingdom

School of Biological Sciences University of Essex Wivenhoe Park Colchester CO4 3SQ United Kingdom

Science Facilities Department Natural History Museum Cromwell Road London SW6 5BD United Kingdom

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Hölldobler B, Wilson EO. The Ants: Cambridge: Belknap Press; 732 p.; 1990.

Fittkau EJ, Klinge H. On biomass and trophic structure of the central Amazonian rain forest ecosystem. Biotropica. 1973;5:2–14.

Eggleton P, Bignell DE, Sands WA, Mawdsley NA, Lawton JH, Wood TG, et al. The diversity, abundance and biomass of termites under differing levels of disturbance in the Mbalmayo Forest Reserve, southern Cameroon. Philosophical Transactions: Biological Sciences. 1996;351:51–68.

Folgarait PJ. Ant biodiversity and its relationship to ecosystem functioning: a review. Biodiversity and Conservation. 1998;7:1221–1244.

Donovan SE, Eggleton P, Bignell DE. Gut content analysis and a new feeding group classification of termites. Ecological Entomology. 2001;26:356–366.

Lawton JH, Bignell DE, Bloemers GF, Eggleton P, Hodda ME. Carbon flux and diversity of nematodes and termites in Cameroon forest soils. Biodiversity and Conservation. 1996;5:261–273.

Crist TO. Biodiversity, species interactions, and functional roles of ants (Hymenoptera: Formicidae) in fragmented landscapes: a review. Myrmecological News. 2009;12:3–13.

Cerdá X, Dejean A. Predation by ants on arthropods and other animals In: Polidori C, editor. Predation in the hymenoptera: an evolutionary perspective: Kerala: Transworld Research Network; 2011. pp. 39–78.

Prestwich GD. Defense mechanisms of termites. Annual Review of Entomology. 1984;29:201–232.

Scholtz OI, Macleod N, Eggleton P. Termite soldier defence strategies: a reassessment of Prestwich's classification and an examination of the evolution of defence morphology using extended eigenshape analyses of head morphology. Zoological Journal of the Linnean Society. 2008;153:631–650.

Dejean A, Fénéron R. Polymorphism and oligogyny in the ponerine ant Centromyrmex bequaerti (Formicidae: Ponerinae). Insectes Sociaux. 1996;43:87–99.

Dejean A, Schatz B, Orivel J, Beugnon G, Lachaud JP, Corbara B. Feeding preferences in African ponerine ants: A cafeteria experiment (Hymenoptera: Formicidae). Sociobiology. 1999;34:555–568.

Bolton B, Fisher BL. Afrotropical ants of the ponerine genera Centromyrmex Mayr, Promyopias Santschi gen. rev. and Feroponera gen. n., with a revised key to genera of African Ponerinae (Hymenoptera: Formicidae). Zootaxa. 2008;1929:1–37.

Longhurst C, Johnson RA, Wood TG. Predation by Megaponera foetens (Fabr.) (Hymenoptera: Formicidae) on termites in the Nigerian southern Guinea savanna. Oecologia. 1978;32:101–107. PubMed

Longhurst C, Baker R, Howse PE. Termite predation by Megaponera foetens (Fab.) (Hymenoptera: Formicidae)—Coordination of raids by glandular secretions. Journal of Chemical Ecology. 1979;5:703–719.

Longhurst C, Howse PE. The use of kairomones by Megaponera foetens (Fab.) (Hymenoptera: Formicidae) in the detection of its termite prey. Animal Behaviour. 1978;26:1213–1218.

Schatz B, Orivel J, Lachaud JP, Beugnon G, Dejean A. Sitemate recognition: the case of Anochetus traegordhi (Hymenoptera; Formicidae) preying on Nasutitermes (Isoptera: Termitidae). Sociobiology. 1999;34:569–580.

Longhurst C, Johnson RA, Wood TG. Foraging, recruitment and predation by Decamorium uelense (Sanstchi) (Formicidae: Myrmicinae) on termites in southern Guinea savanna, Nigeria. Oecologia. 1979;38:83–91. PubMed

Dejean A, Lachaud JP, Beugnon G. Efficiency in the exploitation of patchy environments by the ponerine ant Paltothyreus tarsatus: an ecological consequence of the flexibility of prey capture behavior. Journal of Ethology. 1993;11:43–53.

Schöning C, Moffett MW. Driver ants invading a termite nest: why do the most catholic predators of all seldom take this abundant prey? Biotropica. 2007;39:663–667.

Leponce M, Roisin Y, Pasteels JM. Community interactions between ants and arboreal-nesting termites in New Guinea coconut plantations. Insectes Sociaux. 1999;46:126–130.

Dejean A, Kenne M, Moreau CS. Predatory abilities favour the success of the invasive ant Pheidole megacephala in an introduced area. Journal of Applied Entomology. 2007;131:625–629.

Pequeno PACL Pantoja PO. Negative effects of Azteca ants on the distribution of the termite Neocapritermes braziliensis in central Amazonia. Sociobiology. 2012;59:893–902.

Ellwood MDF, Jones DT, Foster WA. Canopy ferns in lowland dipterocarp forest support a prolific abundance of ants, termites and other invertebrates. Biotropica. 2002;34:575–583. PubMed

DeSouza O, Araújo APA, Reis-Jr R. Trophic controls delaying foraging by termites: reasons for the ground being brown? Bulletin of Entomological Research. 2009;99:603–609. 10.1017/S000748530900666X PubMed DOI

Morris RJ, Lewis OT, Godfray HCJ. Experimental evidence for apparent competition in a tropical forest food web. Nature. 2004;428:310–313. PubMed

Buczkowski G, Bennett G. Behavioral interactions between Aphaenogaster rudis (Hymenoptera: Formicidae) and Reticulitermes flavipes (Isoptera: Rhinotermitidae): the importance of physical barriers. Journal of Insect Behavior. 2008;21:296–305.

Quinet Y, Tekule N, de Biseau JC. Behavioural interactions between Crematogaster brevispinosa rochai Forel (Hymenoptera: Formicidae) and two Nasutitermes species (Isoptera: Termitidae). Journal of Insect Behavior. 2005;18:1–17.

Traniello JFA. Enemy deterrence in the recruitment strategy of a termite: Soldier-organized foraging in Nasutitermes costalis . Proceedings of the National Academy of Sciences USA. 1981;78:1976–1979. PubMed PMC

Buczkowski G, Bennett G. Protein marking reveals predation on termites by the woodland ant, Aphaenogaster rudis . Insectes Sociaux. 2007;54:219–224.

Hrcek J, Miller SE, Quicke DLJ, Smith MA. Molecular detection of trophic links in a complex insect host-parasitoid food web. Molecular Ecology Resources. 2011;11:786–794. 10.1111/j.1755-0998.2011.03016.x PubMed DOI

Rougerie R, Smith MA, Fernandez-Triana J, Lopez-Vaamonde C, Ratnasingham S, Hebert PDN. Molecular analysis of parasitoid linkages (MAPL): gut contents of adult parasitoid wasps reveal larval host. Molecular Ecology. 2011;20:179–186. 10.1111/j.1365-294X.2010.04918.x PubMed DOI

Jurado-Rivera JA, Vogler AP, Reid CAM, Petitpierre E, Gomez-Zurita J. DNA barcoding insect-host plant associations. Proceedings of the Royal Society B-Biological Sciences. 2009;276:639–648. 10.1098/rspb.2008.1264 PubMed DOI PMC

Pompanon F, Deagle BE, Symondson WOC, Brown DS, Jarman SN, Taberlet P. Who is eating what: diet assessment using next generation sequencing. Molecular Ecology. 2012;21:1931–1950. 10.1111/j.1365-294X.2011.05403.x PubMed DOI

Went FW, Wheeler J, Wheeler GC. Feeding and digestion in some ants (Veromessor and Manica). BioScience. 1972;22:82–88.

Scholtz O. Inter-continental patterns in the fine-scale spatial ecology of rain forest termites: University of Plymouth, PhD thesis. 2010

Inward DJG, Vogler AP, Eggleton P. A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Molecular Phylogenetics and Evolution. 2007;44:953–967. PubMed

Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology. 1994;3:294–299. PubMed

Okonechnikov K, Golosova O, Fursov M. Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics. 2012;28:1166–1167. 10.1093/bioinformatics/bts091 PubMed DOI

Jones M, Ghoorah A, Blaxter M. jMOTU and Taxonerator: turning DNA barcode sequences into annotated operational taxonomic units. PLoS ONE. 2011;6:e19259 10.1371/journal.pone.0019259 PubMed DOI PMC

Barrett RDH, Hebert PDN. Identifying spiders through DNA barcodes. Canadian Journal of Zoology-Revue Canadienne De Zoologie. 2005;83:481–491.

Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947–2948. PubMed

Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology. 2008;57:758–771. 10.1080/10635150802429642 PubMed DOI

LaPolla JS, Brady SG, Shattuck SO. Phylogeny and taxonomy of the Prenolepis genus-group of ants (Hymenoptera: Formicidae). Systematic Entomology. 2010;35:118–131.

Smith MA, Fisher BL, Hebert PDN. DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: the ants of Madagascar. Philosophical Transactions of the Royal Society B: Biological Sciences. 2005;360:1825–1834. PubMed PMC

Moreau CS, Bell CD, Vila R, Archibald SB, Pierce NE. Phylogeny of the ants: diversification in the age of angiosperms. Science. 2006;312:101–104. PubMed

Cameron SL, Whiting MF. Mitochondrial genomic comparisons of the subterranean termites from the Genus Reticulitermes (Insecta: Isoptera: Rhinotermitidae). Genome. 2007;50:188–202. PubMed

Dormann CF, Gruber B, Fründ J. Introducing the bipartite package: analysing ecological networks. Rnews. 2008;8:8–11.

Ledoux A. Recherches préliminaires sur quelques points de la biologie d’Odontomachus assiniensis Latr. (Hym. Form., Poneridae). Annales des Sciences Naturelles (Zoologie et Biologie Animale) 1952;14:231–248.

Dejean A, Bashingwa EP. La prédation chez Odontomachus troglodytes Santschi (Formicidae-Ponerinae). Insectes Sociaux. 1985;32:23–42.

Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL. GenBank. Nucleic Acids Research. 2005;33:D34–D38. PubMed PMC

Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: a better web interface. Nucleic Acids Research. 2008;36:W5–W9. 10.1093/nar/gkn201 PubMed DOI PMC

Eggleton P, Bignell DE, Hauser S, Dibog L, Norgrove L, Madong B. Termite diversity across an anthropogenic disturbance gradient in the humid forest zone of West Africa. Agriculture Ecosystems & Environment. 2002;90:189–202.