Nest composition, stable isotope ratios and microbiota unravel the feeding behaviour of an inquiline termite
Termites are eusocial insects having evolved several feeding, nesting and reproductive strategies. Among them, inquiline termites live in a nest built by other termite species: some of them do not forage outside the nest, but feed on food stored by the host or on the nest material itself. In this study, we characterized some dimensions of the ecological niche of Cavitermes tuberosus (Termitidae: Termitinae), a broad-spectrum inquiline termite with a large neotropical distribution, to explain its ecological success. We used an integrative framework combining ecological measures (physico-chemical parameters, stable isotopic ratios of N and C) and Illumina MiSeq sequencing of 16S rRNA gene to identify bacterial communities and to analyse termites as well as the material from nests constructed by different termite hosts (the builders). Our results show that (1) nests inhabited by C. tuberosus display a different physico-chemical composition when compared to nests inhabited by its builder alone; (2) stable isotopic ratios suggest that C. tuberosus feeds on already processed, more humified, nest organic matter; and (3) the gut microbiomes cluster by termite species, with the one of C. tuberosus being much more diverse and highly similar to the one of its main host, Labiotermes labralis. These results support the hypothesis that C. tuberosus is a generalist nest feeder adapted to colonize nests built by various builders, and explain its ecological success.
KeywordsIsoptera Termitidae Cavitermes tuberosus Humivorous Neotropical Nitrogen Nest
We are grateful to the late Philippe Cerdan, to Régis Vigouroux and the staff of the Laboratoire Environnement HYDRECO of Petit Saut (EDF-CNEH) for logistic support during field work. We thank Xavier Goux and Nicolas Kaczmarek for their help in the field, and Alexandre Van Baekel for assistance during ICP-OES measurements.
Author contribution statement
SH and YR designed the study. SH, MM, DF, and YR collected the material. SH and TD performed soil analyses; SH and GL performed isotopic analyses; and MM and MC performed Illumina sequencing and subsequent analyses. All authors contributed significantly to the manuscript and approved the final version.
This work was supported by the Belgian National Fund for Scientific Research F.R.S.-FNRS (PhD fellowship to SH and Grant PDR T.0065.15 to YR) and by the Luxembourg National Research Fund through an FNR 2014 CORE project (OPTILYS; Exploring the higher termite lignocellulolytic system to optimize the conversion of biomass into energy and useful platform molecules/C14/SR/8286517). GL and DF are appointed as Research Associates for the F.R.S.-FNRS.
Compliance with ethical standards
Conflict of interest
We declare we have no competing interests.
Sequences produced for this study have been deposited in GenBank repository under Project accession KBWO01000000 (see details in Supplementary Table S2).
- Abe T (1987) Evolution of life types in termites. In: Kawano S, Connell JH, Hidaka T (eds) Evolution and coadaptation in biotic communities. Univeristy of Tokyo Press, Tokyo, pp 125–148Google Scholar
- Araujo RL (1977) Further notes in the bionomics of Serritermes (Isoptera). Rev Bras Entomol 21:31–32Google Scholar
- Beck MW (2017) ggord: ordination plots with ggplot 2. R package version 1.0.0. https://zenodo.org/badge/latestdoi/35334615
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300Google Scholar
- Brune A, Dietrich C (2015) The gut microbiota of termites: digesting the diversity in the light of ecology and evolution. Annu Rev Microbiol 69:145–166. https://doi.org/10.1146/annurev-micro-092412-155715 CrossRefPubMedGoogle Scholar
- Brune A, Ohkuma M (2011) Role of the termite gut microbiota in symbiotic digestion. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 439–475Google Scholar
- Constantino R (1991) Termites (Isoptera) from the lower Japurá river, Amazonas state, Brazil. Bol Mus Para Emílio Goeldi, séries Zool 7:189–224Google Scholar
- Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34. https://doi.org/10.1146/annurev-ento-010814-020822 CrossRefPubMedGoogle Scholar
- Emerson AE (1925) The termites of Kartabo, Bartica District, British Guiana. Zoologica 6:291–459Google Scholar
- Garnier-Sillam E, Villemin G, Toutain F, Renoux J (1985) Formation of organo-mineral micro-aggregates in termites faeces. C r séances Acad sci Sér 3 Sci vie 301:213–218Google Scholar
- Mathews AGA (1977) Studies on termites from the Mato Grosso state, Brazil. Academia Brasileira de Ciências, Rio de JaneiroGoogle Scholar
- Myles TG (1999) Review of secondary reproduction in termites (Insecta: Isoptera) with comments on its role in termite ecology and social evolution. Sociobiology 33:1–91Google Scholar
- Nadelhoffer KJ, Fry B (1994) Nitrogen isotope studies in terrestrial ecosystems. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology and environmental science. Blackwell Science Ltd, Oxford, pp 22–44Google Scholar
- Noirot C (1970) The nest of termites. In: Krishna K, Weesner FM (eds) Biology of termites, vol 2. Academic Press, New York, pp 73–125Google Scholar
- Ohkuma M, Brune A (2011) Diversity, structure, and evolution of the termite gut microbial community. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 413–438Google Scholar
- R Development Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Schnitzer M (1971) Characterization of humic constituents by spectroscopy. In: McLaren AD, Skujins J (eds) Soil biochemistry, vol 2. Marcel Dekker, New York, pp 60–95Google Scholar
- Thorne BL, Haverty MI (1991) A review of intracolony, intraspecific, and interspecific agonism in termites. Sociobiology 19:115–145Google Scholar
- Waller DA, La Fage JP (1987) Nutritional ecology of termites. In: Slansky F, Rodriguez J (eds) Nutritional ecology of insects, mites, and spiders. Wiley, New York, pp 487–532Google Scholar