Skip to main content
SpringerLink
Log in

Crop-gizzard content and volume variations among afrotropical Apicotermitinae (Blattodea, Termitidae)

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

Termites are dominant organisms of tropical ecosystems. Their success is partly due to the diversity of their feeding substrates, from dead plant tissues to mineralised soils. The Apicotermitinae is one of the richest subfamilies of soil-feeding termites, which are traditionally classified in feeding groups according to anatomical criteria, deemed to the reveal whether species feed on organic-rich layers (group III) or on mineralised soil (group IV). Previous studies based on δ15N isotopic values showed that this subfamily's niche covers a broad range along the gradient of humification. We hypothesised that this broad feeding range could be reflected in the crop-gizzard (Cr-Gi) content and volume. We investigated 17 African species distributed between the two feeding groups. Our results showed a variation of Cr-Gi volume and a consistent composition of content among Apicotermitinae species. Some small-bodied species had a very large Cr-Gi volume relative to their size, indicating a difference in foraging behaviour. These species might use this enhanced storage capacity to forage for longer periods of time. Cr-Gi content was dominated by clay (kaolinite) suggesting that a dietary specialisation could be based on the quality of organic compounds from organo-mineral aggregates. Variations in crystalline solids (quartz) between species indicate either differences in the abundance of mineral grains between feeding patches or active discrimination among particles by foragers. The similar composition of Cr-Gi contents in afrotropical Apicotermitinae suggests that the anatomical criteria used to assign species to feeding groups III or IV are not appropriate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data accessibility

Measurements for crop-gizzard volume and content are available in Online Resource 3.

References

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. JR Stat Soc B 57:289–300

    Google Scholar 

  • Bignell DE (1977) Some observations on the distribution of gut flora in the american cockroach, Periplaneta americana. J Invertebr Pathol 29:338–343

    Article  Google Scholar 

  • Bignell DE (2011) Morphology, physiology, biochemistry and functional design of the termite gut: an evolutionary wonderland. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer SBM, Dordrecht, pp 375–412

    Chapter  Google Scholar 

  • Bignell DE, Eggleton P (1995) On the elevated instestinal pH of higher termites (Isoptera, Termitidae). Insect Soc 42:57–69

    Article  Google Scholar 

  • Boeckx P, Steppe K, Verbeeck H, Beeckman H, Bogaert J, Defourny P, Dessein S, Verheyen E, Leirs H (2017) Congo basin integrated monitoring for forest carbon mitigation and biodiversity (COBIMFO)—Final Report. Belgian Science Policy, Brussels, p 93

  • Bottinelli N, Jouquet P, Capowiez Y, Podwojewski P, Grimaldi M, Peng X (2015) Why is the influence of soil macrofauna on soil structure only considered by soil ecologists? Soil Till Res 146:118–124

    Article  Google Scholar 

  • Bourguignon T, Šobotník J, Lepoint G, Martin JM, Roisin Y (2009) Niche differentiation among neotropical soldierless soil-feeding termites revealed by stable isotope ratios. Soil Biol Biochem 41:2038–2043

    Article  CAS  Google Scholar 

  • Bourguignon T, Šobotník J, Lepoint G, Martin JM, Hardy O, Dejean A, Roisin Y (2011) Feeding ecology and phylogenetic structure of a complex neotropical termite assemblage, revealed by nitrogen stable isotope ratios. Ecol Entomol 36:261–269

    Article  Google Scholar 

  • Bourguignon T, Drouet T, Šobotník J, Hanus R, Roisin Y (2015a) Influence of soil properties on soldierless termite distribution. PLoS ONE 10(8):e0135341

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bourguignon T, Lo N, Cameron S, Šobotník J, Hayashi Y, Shigenobu S, Watanabe D, Roisin Y, Miura T, Evans TA (2015b) The evolutionary history of termites as inferred from 66 mitochondrial genomes. Mol Biol Evol 32:406–421

    Article  PubMed  CAS  Google Scholar 

  • Bourguignon T, Šobotník J, Dahlsjö C, Roisin Y (2016) The soldierless Apicotermitinae: insights into a poorly known and ecologically dominant tropical taxon. Insect Soc 63:39–50

    Article  Google Scholar 

  • Bourguignon T, Lo N, Šobotník J, Ho S, Iqbal N, Coissac É, Lee M, Jendryka M, Sillam-Dussès D, Křížková B, Roisin Y, Evans T (2017) Mitochondrial phylogenomics resolves the global spread of higher termites, ecosystem engineers of the tropics. Mol Biol Evol 34:589–597

    PubMed  CAS  Google Scholar 

  • Bretz F, Hothorn T, Westfall P (2011) Multiple comparisons using R. Chapman & Hall/ CRC Press, Boca Raton

    Google Scholar 

  • Brune A, Kühl M (1996) pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J Insect Physiol 42:1121–1127

    Article  CAS  Google 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 SBM, Dordrecht, pp 413–475

    Google Scholar 

  • Dahlsjö C, Parr C, Malhi Y, Rahman H, Meir P, Jones DT, Eggleton P (2014) First comparison of quantitative estimates of termite biomass and abundance reveals strong intercontinental differences. J Trop Ecol 30:143–152

    Article  Google Scholar 

  • Donovan SE, Eggleton P, Bignell DE (2001a) Gut content analysis and a new feeding group classification of termites. Ecol Entomol 26:356–366

    Article  Google Scholar 

  • Donovan SE, Eggleton P, Dubbin WE, Batchelder M, Dibog L (2001b) The effect of a soil-feeding termite, Cubitermes fungifaber (Isoptera: Termitidae) on soil properties: termites may be an important source of soil microhabitat heterogeneity in tropical forests. Pedobiologia 45:1–11

    Article  Google Scholar 

  • Dosso K, Konaté S, Aidara D, Linsenmair KE (2010) Termite diversity and abundance across fire-induced habitat variability in a tropical moist savanna (Lamto, central Côte d’Ivoire). J Trop Ecol 26:323–334

    Article  Google Scholar 

  • Eggleton P (2011) An introduction to termites: biology, taxonomy and functional morphology. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer SBM, Dordrecht, pp 1–26

    Google Scholar 

  • Eggleton P, Tayasu I (2001) Feeding groups, lifetypes and the global ecology of termites. Ecol Res 16:941–960

    Article  Google Scholar 

  • Eggleton P, Bignell DE, Sands WA, Waite B, Wood TG, Lawton JH (1995) The species richness of termites (Isoptera) under differing levels of forest disturbance in the Mbalmayo forest reserve, southern Cameroon. J Trop Ecol 11:85–98

    Article  Google Scholar 

  • Eggleton P, Bignell DE, Sands WA, Mawdsley NA, Lawton JH, Wood TG, Bignell NC (1996) The diversity, abundance and biomass of termites under differing levels of disturbance in Mbalmayo forest reserve, Southern Cameroon. Phil Trans R Soc Lond B 351:51–68

    Article  Google Scholar 

  • Eggleton P, Davies RG, Bignell DE (1998) Body size and energy use in termites (Isoptera): the responses of soil feeders and wood feeders differ in a tropical forest assemblage. Oikos 81:525–530

    Article  Google Scholar 

  • Garnier-Sillam E, Harry M (1995) Distribution of humic compounds in mounds of some soil-feeding termite species of tropical rainforests: its influence on soil structure stability. Insect Soc 42:167–185

    Article  Google Scholar 

  • Grassé PP (1982) Termitologia. Volume I. Masson, Paris, p 676

    Google Scholar 

  • Grassé PP, Noirot C (1954) Apicotermes arquieri (Isoptère): ses constructions, sa biologie. Considérations générales sur la sous-famille des Apicotermitinae nov. Ann Sci Nat Zool Biol Anim 16:345–388

    Google Scholar 

  • Ji R, Brune A (2005) Digestion of peptidic residues in humic substances by an alkali-stable and humic-acid-tolerant proteolytic activity in the gut of soil-feeding termites. Soil Biol Biochem 37:1648–1655

    Article  CAS  Google Scholar 

  • Johnson RA (1979) Configuration of the digestive tube as an aid to identification of worker Termitidae (Isoptera). Syst Entomol 4:31–38

    Article  Google Scholar 

  • Jouquet P, Bottinelli N, Lata JC, Mora P, Caquineau S (2007) Role of the fungus-growing termite Pseudacanthotermes spiniger (Isoptera, Macrotermitinae) in the dynamic of clay and soil organic matter content. An experimental analysis. Geoderma 139:127–133

    Article  CAS  Google Scholar 

  • Jouquet P, Bottinelli N, Shanbhag R, Bourguignon T, Traoré S, Abbasi SA (2016) Termites: the neglected soil engineers of tropical soils. Soil Sci 181:157–165

    Article  CAS  Google Scholar 

  • Kappler A, Brune A (1999) Influence of gut alkalinity and oxygen status on mobilization and size-class distribution of humic acids in the hindgut of soil-feeding termites. Appl Soil Ecol 13:219–229

    Article  Google Scholar 

  • Klowden MJ (2013) Physiological systems in insects, 3rd edn. Academic Press, London, p 682

    Google Scholar 

  • Krishna K, Grimaldi D, Krishna V, Engel M (2013) Treatise on the isoptera of the world. Bull Am Mus Nat Hist 377:1–2704

    Article  Google Scholar 

  • Madejová J (2003) FTIR techniques in clay mineral studies. Vib Spectrosc 31:1–10

    Article  Google Scholar 

  • Martin SJ, Funch RR, Hanson PR, Yoo E-H (2018) A vast 4,000-year-old spatial pattern of termite mounds. Curr Biol 28:R1292–R1293

    Article  PubMed  CAS  Google Scholar 

  • Michels J, Büntzow M (2010) Assessment of Congo red as a fluorescence marker for the exoskeleton of small crustaceans and the cuticle of polychaetes. J Microsc 238:95–101

    Article  PubMed  CAS  Google Scholar 

  • Misture ST, Snyder RL (2001) X-ray diffraction. In: Buschow KHJ, Cahn RW, Flemings MC, Ilschner B, Kramer EJ, Mahajan S, Veyssière P (eds) Encyclopedia of materials: science and technology. Elsevier, Oxford, pp 9799–9808

    Chapter  Google Scholar 

  • Mujinya BB, Mees F, Erens H, Dumon M, Baert G, Boeckx P, Ngongo M, Van Ranst E (2013) Clay composition and properties in termite mounds of the Lubumbashi area, D.R. Congo. Geoderma 192:304–315

    Article  CAS  Google Scholar 

  • Nduwarugira D, Mpawenayo B, Roisin Y (2017) The role of high termitaria in the composition and structure of the termite assemblage in Miombo woodlands of southern Burundi. Insect Conserv Divers 10:120–128

    Article  Google Scholar 

  • Noirot C (1969) Formation of castes in higher termites. In: Krishna K, Weesner FM (eds) Biology of termites. Academic Press, New York, pp 311–350

    Chapter  Google Scholar 

  • Noirot C (1982) La caste des ouvriers, élément majeur du succès évolutif des termites. Riv Biol 75:157–195

    Google Scholar 

  • Noirot C (2001) The gut of termites (Isoptera): comparative anatomy, systematics, phylogeny. II. Higher termites (Termitidae). Ann Soc Entomol Fr (NS) 37:431–471

    Google Scholar 

  • Noirot C, Noirot-Timothée C (1969) The digestive system. In: Krishna K, Weesner FM (eds) Biology of termites. Academic Press, New York, pp 49–88

    Chapter  Google 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 SBM, Dordrecht, pp 413–438

    Google Scholar 

  • Poorter L, Jans L, Bongers F, Vanrompaey RSAR (1994) Spatial distribution of gaps along three catenas in the moist forest of Taï National Park, Ivory Coast. J Trop Ecol 10:385–398

    Article  Google Scholar 

  • R Development Core Team (2019) R: a language and environment for statistical computing [Internet]. Viena: R Foundation for Statistical Computing. https://www.r-project.org/. Accessed 13 Mar 2019

  • Roisin Y, Pasteels JM (1996) The nasute termites (Isoptera, Nasutitermitinae) of Papua New Guinea. Invertebr Taxon 10:507–616

    Article  Google Scholar 

  • Sands WA (1972) The soldierless termites of Africa (Isoptera: Termitidae). Bull Br Mus Nat Hist (Entomol) 18:1–244

    Google Scholar 

  • Sands WA (1998) The identification of worker castes of termite genera from soils of Africa and the middle east. CAB International, Cambridge, p 500

    Google Scholar 

  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682

    Article  PubMed  CAS  Google Scholar 

  • Semhi K, Chaudhuri S, Clauer N, Boeglin JL (2008) Impact of termite activity on soil environment: a perspective from their soluble chemical components. Int J Environ Sci Technol 5:431–444

    Article  CAS  Google Scholar 

  • Sleaford F, Bignell DE, Eggleton P (1996) A pilot analysis of gut contents in termites from the Mbalmayo forest reserve, Cameroon. Ecol Entomol 21:279–288

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Warton DI, Duursma RA, Falster DS, Taskinen S (2012) smatr 3—an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Belgian National Fund for Scientific Research F.R.S.-FNRS, PDR T.0065.15 to YR. We thank Pierre Devaif for his help with lighting techniques in microscopy, and Guy Josens for facilitating access to stereomicroscope. We acknowledge the Department 4MAT, Materials Engineering, Characterization, Processing and Recycling at the Université Libre de Bruxelles for their help for XRD and µFTIR measurements. We thank Hugo Darras for his critical input to the manuscript.

Author information

Authors and Affiliations

  1. Unit of Evolutionary Biology and Ecology, Université Libre de Bruxelles, Brussels, Belgium

    J. Romero Arias & Y. Roisin

  2. Biogeochemistry and Earth System Modelling, Department of Geosciences, Environment and Society, Université Libre de Bruxelles, Brussels, Belgium

    S. Bonneville

Authors
  1. J. Romero Arias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Bonneville
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Roisin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Romero Arias.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Romero Arias, J., Bonneville, S. & Roisin, Y. Crop-gizzard content and volume variations among afrotropical Apicotermitinae (Blattodea, Termitidae). Insect. Soc. 67, 261–271 (2020). https://doi.org/10.1007/s00040-020-00760-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-020-00760-x

Keywords

Search

Navigation