Journal of Insect Conservation

, Volume 22, Issue 2, pp 197–208 | Cite as

Intermediate disturbance promotes termite functional diversity in intensively managed Vietnamese coffee agroecosystems

  • Kok-Boon Neoh
  • My Thi Nguyen
  • Vuong Tan Nguyen
  • Masayuki Itoh
  • Osamu Kozan
  • Tsuyoshi Yoshimura


The intensive agricultural practices used in coffee plantations have profound impacts on invertebrate biodiversity. We surveyed termite diversity in the central highlands of Vietnam and evaluated it relative to the in situ ecological conditions of the coffee farms. Two survey sites were established at farms that were in place for 1 month and 1, 3, 5, and 25 years at the time of sampling. In addition, two models were tested: the diversity–resource relationship and the diversity–disturbance relationship. Our results demonstrated that the loss of termite diversity due to land perturbation in newly cultivated coffee farms may be as high as 86% compared with the nearest forested site. Only two feeding groups of termite (Group II and Group III) were present in the study sites. Termite composition of young and old farms was similar, but they only shared 48% similarity and differed significantly from the composition of the 1, 3, and 5 year old coffee farms. Understory vegetation cover and moisture content were positively associated with the occurrence of Group II and III termites but negatively associated with soil bulk density. Termite species richness did not increase linearly with the increased biomass production (plant litter) that is characteristic of old coffee farms. In contrast, termite species richness and occurrence were related to the intensity of farm management. Farms subjected to an intermediate level of management intensity due to annual crop cultivation recorded the highest diversity. Our study highlights the importance of annual crop cultivation to enhance termite diversity.


Feeding group Biodiversity loss Species richness Coffee monoculture Soil-dwelling insects 



We would like to thank Yoko Takematsu (Yamaguchi University) for assistance in identifying termite specimens and anonymous reviewers whose comments greatly improved the manuscript.


This study was supported by the Large-Scale Research Program ‘Promoting the Study of Sustainable Humanosphere in Southeast Asia’ funded by the Japanese Ministry of Education, Culture, Sports, Science, and Technology, 2011–2016 and the project (No. 14200117), Research Institute for Humanity and Nature (RIHN). K.-B.N. was an international research fellow at the Japan Society for the Promotion of Science.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10841_2018_53_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 19 KB)


  1. Ahmad M (1965) Termites (Isoptera) of Thailand. Bull Am Mus Nat Hist 131:1–114Google Scholar
  2. Armbrecht I, Rivera L, Perfecto I (2005) Reduced diversity and complexity in the leaf-litter ant assemblage of Colombian coffee plantations. Conserv Biol 19:897–907CrossRefGoogle Scholar
  3. Armbrecht I, Perfecto I, Silverman E (2006) Limitation of nesting resources for ants in Colombian forests and coffee plantations. Ecol Entomol 31:403–410CrossRefGoogle Scholar
  4. Beaudrot L, Du Y, Kassim AR, Rejmánek M, Harrison RD (2011) Do epigeal termite mounds increase the diversity of plant habitats in a tropical rain forest in Peninsular Malaysia? PLoS ONE 6(5):e19777. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bignell DE, Eggleton P (2000) Termites in ecosystems. In: Abe T, Bignell DE, Higashi M (eds) Termite: evolution, sociality, symbioses, ecology. Kluwer Academic, Dordrecht, pp 363–388CrossRefGoogle Scholar
  6. Bourguignon T, Dahlsjö CAL, Jacquemin J, Gang L, Wijedasa LS, Evans TA (2017) Ant and termite communities in isolated and continuous forest fragments in Singapore. Insect Soc 64:505–514CrossRefGoogle Scholar
  7. Briggs HM, Perfecto I, Brosi BJ (2013) The role of the agricultural matrix: coffee management and euglossine bee (Hymenoptera: Apidae: Euglossini) communities in Southern Mexico. Environ Entomol 42:1210–1217CrossRefPubMedGoogle Scholar
  8. Colwell RK 2013. EstimateS: statistical estimation of species richness and shared species from samples. Version 9. User’s Guide and application published at:
  9. Coulibaly T, Akpesse AAM, Boga J-P, Yapi A, Kouassi KP, Roisin Y (2016) Change in termite communities along a chronosequence of mango tree orchards in the north of Côte d’Ivoire. J Insect Conserv 20:1011–1019CrossRefGoogle Scholar
  10. D’haeze D, Deckers J, Raes D, Phong TA, Chanh NDM (2003) Over-irrigation of coffea canephora in the Central Highlands of Vietnam revisited: simulation of soil moisture dynamics in Rhodic Ferralsols. Agric Water Manag 63:185–202CrossRefGoogle Scholar
  11. D’haeze D, Deckers J, Raes D, Phong TA, Loi HV (2005) Environmental and socio-economic impacts of institutional reforms on the agricultural sector of Vietnam: land suitability assessment for Robusta coffee in the Dak Gan region. Agric Ecosyst Environ 105:59–76CrossRefGoogle Scholar
  12. Davies RG, Eggleton P, Dibog L, Lawton JH, Bignell DE, Brauman A, Hartmann C, Nunes L, Holt J, Rouland C (1999) Successional response of a tropical forest termite assemblage to experimental habitat perturbation. J Appl Ecol 36:946–962CrossRefGoogle Scholar
  13. Donovan SE, Eggleton P, Bignell DE (2001a) Gut content analysis and a new feeding group classification of termites. Ecol Entomol 26:356–366CrossRefGoogle Scholar
  14. 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 45:1–11CrossRefGoogle Scholar
  15. Eggleton P, Bignell D, Sands W, Waite B, Wood T, Lawton J (1995) The species richness of termites (Isoptera) under differing levels of forest disturbance in the Mbalmayo Forest Reserve, Southern Cameroon. J Trop Ecol 11:85–98CrossRefGoogle Scholar
  16. 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 81:525–530CrossRefGoogle Scholar
  17. Eggleton P, Homathevi R, Jones DT, MacDonald JA, Jeeva D, Bignell DE, Davies RG, Maryati M (1999) Termite assemblages, forest disturbance and greenhouse gas fluxes in Sabah, East Malaysia. Philos Trans R Soc Lond B 354:1791–1802CrossRefGoogle Scholar
  18. Eggleton P, Bignell DE, Hauser S, Dibog L, Norgrove L, Madong B (2002) Termite diversity across an anthropogenic disturbance gradient in the humid forest zone of West Africa. Agric Ecosyst Environ 90:189–202CrossRefGoogle Scholar
  19. Evans TA, Dawes TZ, Ward PR, Lo N (2011) Ants and termites increase crop yield in a dry climate. Nat Commun 2:262. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gordon CE, McGill B, Ibarra-Núñez G, Greenberg R, Perfecto I (2009) Simplification of a coffee foliage-dwelling beetle community under low-shade management. Basic Appl Ecol 10:246–254CrossRefGoogle Scholar
  21. Guimaraes GP, Mendona ED, Passos RR, Andrade FV (2014) Soil aggregation and organic carbon of oxisols under coffee in agroforestry systems. Rev Bras Cienc Solo 38:278–287CrossRefGoogle Scholar
  22. Hajian-Forooshani Z, Gonthier DJ, Marin L, Iverson AL, Perfecto I (2014) Changes in species diversity of arboreal spiders in Mexican coffee agroecosystems: untangling the web of local and landscape influences driving diversity. Peer J 2:e623. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Holt JA, Lepage M (2000) Termites and soil properties. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic, Dordrecht, pp 389–407CrossRefGoogle Scholar
  24. Hu J, Neoh K-B, Appel AG, Lee C-Y (2012) Subterranean termite open-air foraging and tolerance to desiccation: comparative water relation of two sympatric Macrotermes spp. (Blattodea: Termitidae). Comp Biochem Physiol A Mol Integr Physiol 161:201–207CrossRefPubMedGoogle Scholar
  25. Jones DT, Eggleton P (2000) Sampling termite assemblages in tropical forests: testing a rapid biodiversity assessment protocol. J Appl Ecol 37:191–203CrossRefGoogle Scholar
  26. Jones DT, Susilo FX, Bignell DE, Hardiwinoto S, Gillison AN, Eggleton P (2003) Termite assemblage collapse along a land-use intensification gradient in lowland central Sumatra, Indonesia. J Appl Ecol 40:380–391CrossRefGoogle Scholar
  27. Lazaro A, Tscheulin T, Devalez J, Nakas G, Petanidou T (2016) Effects of grazing intensity on pollinator abundance and diversity, and on pollination services. Ecol Entomol 41:400–412CrossRefGoogle Scholar
  28. Lepage M, Abbadie L, Mariotti A (1993) Food habits of sympatric termite species (Isoptera, Macrotermitinae) as determined by stable carbon isotope analysis in a Guinean savanna (Lamto, Cote d’Ivoire). J Trop Ecol 9:303–311CrossRefGoogle Scholar
  29. Lindell C, Smith M (2003) Nesting bird species in sun coffee, pasture, and understory forest in southern Costa Rica. Biodivers Conserv 12:423–440CrossRefGoogle Scholar
  30. Lopez-Rodriguez G, Sotomayor-Ramirez D, Amador JA, Schroder EC (2015) Contribution of nitrogen from litter and soil mineralization to shade and sun coffee (Coffea arabica L.) agroecosystems. Trop Ecol 56:155–167Google Scholar
  31. Luke SH, Fayle TM, Eggleton P, Turner EC, Davies RG (2014) Functional structure of ant and termite assemblages in old growth forest, logged forest and oil palm plantation in Malaysian Borneo. Biodivers Conserv 23:2817–2832CrossRefGoogle Scholar
  32. Mas AH, Dietsch TV (2003) An index of management intensity for coffee agroecosystems to evaluate butterfly species richness. Ecol Appl 13:1491–1501CrossRefGoogle Scholar
  33. McGlynn TP, Weiser MD, Dunn RR (2010) More individuals but fewer species: testing the ‘more individuals hypothesis’ in a diverse tropical fauna. Biol Lett 6:490–493CrossRefPubMedPubMedCentralGoogle Scholar
  34. Neoh K-B, Bong L-J, My NT, Vuong NT, Quoc HN, Itoh M, Kozan O, Yoshimura T (2015) Termite diversity and complexity in Vietnamese agroecosystems along a gradient of increasing disturbance. J Insect Conserv 19:1129–1139CrossRefGoogle Scholar
  35. Neoh K-B, Bong L-J, Muhammad A, Itoh M, Kozan O, Takematsu Y et al. (2017) The effect of remnant forest on insect successional response in tropical fire-impacted peatland: a bi-taxa comparison. PLoS ONE 12(3): e0174388. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Nguyen D, Nguyen T, Trinh V, Nguyen V, Le V, Nguyen T, Vu V, Ngo T, Vo T (2007) Fauna of Vietnam, vol 15. isoptera—termites (in Vietnamese). Science and Technology, HanoiGoogle Scholar
  37. Okwakol MJN (2000) Changes in termite (Isoptera) communities due to the clearance and cultivation of tropical forest in Uganda. Afr J Ecol 38:1–7CrossRefGoogle Scholar
  38. Perfecto I, Mas A, Dietsch T, Vandermeer J (2003) Conservation of biodiversity in coffee agroecosystems: a tri-taxa comparison in southern Mexico. Biodivers Conserv 12:1239–1252CrossRefGoogle Scholar
  39. Philpott SM, Armbrecht I (2006) Biodiversity in tropical agroforests and the ecological role of ants and ant diversity in predatory function. Ecol Entomol 31:369–377CrossRefGoogle Scholar
  40. Philpott SM, Perfecto I, Vandermeer J (2006) Effects of management intensity and season on arboreal ant diversity and abundance in coffee agroecosystems. Biodivers Conserv 15:139–155CrossRefGoogle Scholar
  41. Philpott SM, Arendt WJ, Armbrecht I, Bichier P, Diestch TV, Gordon C, Greenberg R, Perfecto I, Reynoso-Santos R, Soto-Pinto L, Tejeda-Cruz C, Williams-Linera G, Valenzuela J, Zolotoff JM (2008) Biodiversity loss in Latin American coffee landscapes: review of the evidence on ants, birds, and trees. Conserv Biol 22:1093–1105CrossRefPubMedGoogle Scholar
  42. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2017) nlme: linear and nonlinear mixed effects models. R package version 3.1-131,
  43. R Core Team (2017) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna
  44. Takematsu Y, Vongkaluang C (2012) A taxonomic review of the Rhinotermitidae (Isoptera) of Thailand. J Nat Hist 46:1079–1109CrossRefGoogle Scholar
  45. ter Braak C, Smilauer P (2012) Canoco reference manual and user’s guide: software for ordination (version 5.0). Microcomputer Power, Ithaca, NYGoogle Scholar
  46. Uchida K, Ushimaru A (2014) Biodiversity declines due to abandonment and intensification of agricultural lands: patterns and mechanisms. Ecol Monogr 84:637–658CrossRefGoogle Scholar
  47. Urrutia-Escobar M, Armbrecht I (2013) Effect of two agroecological management strategies on ant (Hymenoptera: Formicidae) diversity on coffee plantations in southwestern Colombia. Environ Entomol 42:194–203CrossRefPubMedGoogle Scholar
  48. Veddeler D, Schulze CH, Steffan-Dewenter I, Buchori D, Tscharntke T (2005) The contribution of tropical secondary forest fragments to the conservation of fruit-feeding butterflies: effects of isolation and age. Biodivers Conserv 14:3577–3592CrossRefGoogle Scholar
  49. Whiles MR, Goldowitz BS (2001) Hydrologic influences on insect emergence production from central Platte River wetlands. Ecol Appl 11:1829–1842CrossRefGoogle Scholar
  50. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New YorkCrossRefGoogle Scholar
  51. Williams-Guillen K, Perfecto I (2010) Effects of agricultural intensification on the assemblage of leaf-nosed bats (Phyllostomidae) in a coffee landscape in Chiapas, Mexico. Biotropica 42:605–613CrossRefGoogle Scholar
  52. Yee DA, Juliano SA (2007) Abundance matters: a field experiment testing the more individuals hypothesis for richness-productivity relationships. Oecologia 153:153–162CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of EntomologyNational Chung Hsing UniversityTaichungTaiwan
  2. 2.Institute of Ecology and Works ProtectionHanoiVietnam
  3. 3.Center for Southeast Asian StudiesKyoto UniversityKyotoJapan
  4. 4.Laboratory of Innovative Humano-habitability, Research Institute for Sustainable HumanosphereKyoto UniversityUjiJapan

Personalised recommendations