Evidence from Mid-Infrared Spectroscopy (MIRS) that the biochemical fingerprints of Odontotermes obesus colonies change according to their geographical location and age

  • P. Jouquet
  • A. Pando
  • H. Aroui
  • A. Harit
  • Y. Capowiez
  • N. Bottinelli
Research Article
  • 37 Downloads

Abstract

In this study, we used Mid-Infrared Spectroscopy (MIRS) to analyze the biochemical fingerprints of nine termite colonies (soldiers, minor and major workers). We then examined whether these spectra could be used to differentiate termite colonies and if their differences could be explained by the geographical distances between colonies and/or their ages. We demonstrated that when only data from the heads of minor workers were considered, the specific fingerprint of each colony appeared to reflect its coordinate position in the study site. However, termite mound height, a proxy for colony age, was the main factor governing these signatures when data from the abdomen of major workers were used. Thus, this study shows the potential of MIRS for differentiating termite colonies in the field. It also highlights the close relationship between the physiological states of termite colonies and their environment.

Keywords

Termite Mounds Niche construction Extended phenotype India 

References

  1. Ajayi O (2012) Biochemical analyses and nutritional content of four castes of subterranean termites, Macrotermes subhyalinus (Rambur) (Isoptera: Termitidae): differences in digestibility and anti-nutrient contents among castes. Int J Biol 4:54CrossRefGoogle Scholar
  2. Attignon SE, Lachat T, Sinsin B, Nagel P, Peveling R (2005) Termite assemblages in a West-African semi-deciduous forest and teak plantations. Agric Ecosyst Environ 110:318–326CrossRefGoogle Scholar
  3. Badertscher S, Gerber C, Leuthold RH (1983) Polyethism in food-supply and processing in termite colonies of Macrotermes subhyalinus (Isoptera). Behav Ecol Sociobiol 12:115–119CrossRefGoogle Scholar
  4. Barbiero L, Parate HR, Descloitres M, Bost A, Furian S, Kumar MSM, Kumar C, Braun JJ (2007) Using a structural approach to identify relationships between soil and erosion in a semi-humid forested area, South India. Catena 70:313–329CrossRefGoogle Scholar
  5. Barthes BG, Brunet D, Rabary B, Ba O, Villenave C (2011) Near infrared reflectance spectroscopy (NIRS) could be used for characterization of soil nematode community. Soil Biol Biochem 43:1649–1659CrossRefGoogle Scholar
  6. Black HIJ, Okwakol MJN (1997) Agricultural intensification, soil biodiversity and agroecosystem function in the tropics: the role of termites. Appl Soil Ecol 6:37–53CrossRefGoogle Scholar
  7. Bottinelli N, Capowiez Y, Hallaire V, Jouquet P (2013) An inability of Near Infrared Reflectance Spsctroscopy (NIRS) to identify belowground earthworm casts in no-tillage soil. Appl Soil Ecol 70:57–61CrossRefGoogle Scholar
  8. Braun JJ, Descloitres M, Riotte J, Deschamps P, Violette A, Marechal JC, Sekhar M, Kumar MSM, Subramanian S (2009) Contemporary versus long-term weathering rates in Tropics: Mule Hole, South India. Geochim Cosmochim Acta 73:157–157CrossRefGoogle Scholar
  9. Bulmer MS, Adams ES, Traniello JFA (2001) Variation in colony structure in the subterranean termite Reticulitermes flavipes. Behav Ecol Sociobiol 49:236–243CrossRefGoogle Scholar
  10. Cabrera BJ, Rust MK (1999) Caste differences in feeding and trophallaxis in the western drywood termite, Incisitermes minor (Hagen) (Isoptera, Kalotermitidae). Insect Soc 46:244–249CrossRefGoogle Scholar
  11. Cécillon L, Cassagne N, Czarnes S, Gros R, Brun JJ (2008) Variable selection in near infrared spectra for the biological characterization of soil and earthworm casts. Soil Biol Biochem 40:1975–1979CrossRefGoogle Scholar
  12. Chouvenc T, Su NY (2014) Colony age-dependent pathway in caste development of Coptotermes formosanus Shiraki. Insect Soc 61:171–182CrossRefGoogle Scholar
  13. Chouvenc T, Su NY (2017) Testing the role of cuticular hydrocarbons on intercolonial agonism in two subterranean termite species (Coptotermes) and their hybrids. Insect Soc 64:347–355CrossRefGoogle Scholar
  14. Chouvenc T, Basille M, Su NY (2015) The production of soldiers and the maintenance of caste proportions delay the growth of termite incipient colonies. Insect Soc 62:23–29CrossRefGoogle Scholar
  15. Clairotte M, Grinand C, Kouakoua E, Thébault A, Saby NPA, Bernoux M, Barthès BG (2016) National calibration of soil organic carbon concentration using diffuse infrared reflectance spectroscopy. Geoderma 276:41–52CrossRefGoogle Scholar
  16. Conforti M, Castrignanò A, Robustelli G, Scarciglia F, Stelluti M, Buttafuoco G (2015) Laboratory-based Vis–NIR spectroscopy and partial least square regression with spatially correlated errors for predicting spatial variation of soil organic matter content. Catena 124:60–67CrossRefGoogle Scholar
  17. Darlington JPEC, Dransfield RD (1987) Size relationships in nest populations and mound parameters in the termite Macrotermes michaelseni in Kenya. Insect Soc 34:165–180CrossRefGoogle Scholar
  18. Davies RG, Hernandez LM, Eggleton P, Didham RK, Fagan LL, Winchester NN (2003) Environmental and spatial influences upon species composition of a termite assemblage across Neotropical forest islands. J Trop Ecol 19:509–524CrossRefGoogle Scholar
  19. Gobrecht A, Roger JM, Bellon-Maurel V (2014) Major issues of diffuse reflectance NIR spectroscopy in the specific context of soil carbon content estimation: a review. Adv Agron 123:145–175CrossRefGoogle Scholar
  20. Grassé PP, Noirot C (1947) Le polymorphisme social du termite à cou jaune (Calotermes flavicollis F.). Les faux-ouvriers ou pseudergates et les mues régressives. C R Acad Sci 224:219–221Google Scholar
  21. Haverty MI (1977) The proportion of soldiers in termite colonies: a list and a bibliography. Sociobiology 2:199–216Google Scholar
  22. Haverty MI, Howard RW (1981) Production of soldiers and maintenance of soldier proportions by laboratory experimental groups of Reticulitermes flavipes (Kollar) and Reticulitermes virginicus (Banks) (Isoptera: Rhinotermitidae). Insect Soc 28:32–39CrossRefGoogle Scholar
  23. Haverty MI, Copren KA, Getty GM, Lewis VR (1999) Agonistic behavior and cuticular hydrocarbon phenotypes of colonies of Reticulitermes (Isoptera: Rhinotermitidae) from northern California. Ann Entomol Soc Am 92:269–277CrossRefGoogle Scholar
  24. Hedde M, Lavelle P, Joffre R, Jimenez JJ, Decäens T (2005) Specific functional signature in soil macro-invertebrate biostructures. Funct Ecol 19:785–793CrossRefGoogle Scholar
  25. Hinze B, Leuthold RH (1999) Age related polyethism and activity rhythms in the nest of the termite Macrotermes bellicosus (Isoptera, Termitidae). Insect Soc 46:392–397CrossRefGoogle Scholar
  26. Hinze B, Crailsheim K, Leuthold RH (2002) Polyethism in food processing and social organisation in the nest of Macrotermes bellicosus (Isoptera, Termitidae). Insect Soc 49:31–37CrossRefGoogle Scholar
  27. Holt AJ, Lepage M (2000) Termites and soil properties. In: Abe T, Bignell DE, Higashi M (eds) Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer Academic Publishers, Dordrecht, pp 389–407CrossRefGoogle Scholar
  28. Josens G, Soki K (2010) Relation between termite numbers and the size of their mounds. Insect Soc 57:303–316CrossRefGoogle Scholar
  29. Jouquet P, Zangerlé A, Rumpel C, Brunet D, Bottinelli N, Tran Duc T (2009) Relevance of the biogenic and physicogenic classification. A comparison of approaches to discriminate the origin of soil aggregates. Eur J Soil Sci 60:1117–1125CrossRefGoogle Scholar
  30. Jouquet P, Henry-des-Tureaux T, Doan Thu T, Tran Duc T, Orange D (2010) Utilization of near infrared reflectance spectroscopy (NIRS) to quantify the impact of earthworms on soil and carbon erosion in steep slope ecosystem. A study case in Northern Vietnam. Catena 81:113–116CrossRefGoogle Scholar
  31. Jouquet P, Capowiez Y, Bottinelli N, Traoré S (2014) Potential of Near Infrared Reflectance Spectroscopy for identifying termite species. Eur J Soil Biol 60:49–52CrossRefGoogle Scholar
  32. Jouquet P, Guilleux N, Shanbhag RR, Subramanian S (2015) Influence of soil type on the properties of termite mound nests in Southern India. Appl Soil Ecol 96:282–287CrossRefGoogle Scholar
  33. Jouquet P, Guilleux N, Caner L, Chintakunta S, Ameline M, Shanbhag R (2016) Influence of soil pedological properties on termite mound stability. Geoderma 262:45–51CrossRefGoogle Scholar
  34. Korb J, Linsenmair KE (2001) Resource availability and distribution patterns, indicators of competition between Macrotermes bellicosus and other macro-detritivores in the Comoé National Park, Côte d’Ivoire. Afr J Ecol 39:257–265CrossRefGoogle Scholar
  35. Li GH, Lei CL, Wang ZH, Huang QY (2015) Dynamics of sex ratio, fresh weight and nutrient contents at five developmental stages of alates in the subterranean termite Reticulitermes chinensis. Insect Soc 62:51–57CrossRefGoogle Scholar
  36. Liu Y, Henderson G, Mao L, Laine RA (2005a) Effects of temperature and nutrition on juvenile hormone titers of Coptotermes formosanus (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 98:732–737CrossRefGoogle Scholar
  37. Liu Y, Henderson G, Mao L, Laine RA (2005b) Seasonal variation of juvenile hormone titers of the Formosan subterranean termite, Coptotermes formosanus (Rhinotermitidae). Environ Entomol 34:557–562CrossRefGoogle Scholar
  38. Luykx P (1986) Termite colony dynamics as revealed by the sex- and caste-ratios of whole colonies of Incisitermes schwarzi Banks (Isoptera: Kalotermitidae). Insect Soc 33:221–248CrossRefGoogle Scholar
  39. Machida M, Kitade O, Miura T, Matsumoto T (2001) Nitrogen recycling through proctodeal trophallaxis in the Japanese damp-wood termite Hodotermopsis japonica (Isoptera, Termopsidae). Insect Soc 48:52–56CrossRefGoogle Scholar
  40. Madari BE, Reeves IJB, Machado PLOA, Guimarães CM, Torres E, McCarty GW (2006) Mid- and near-infrared spectroscopic assessment of soil compositional parameters and structural indices in two Ferralsols. Geoderma 136:245–259CrossRefGoogle Scholar
  41. Madhavan DB, Kitching M, Mendham DS, Weston CJ, Baker TG (2016) Mid-infrared spectroscopy for rapid assessment of soil properties after land use change from pastures to Eucalyptus globulus plantations. J Environ Manage 175:67–75CrossRefPubMedGoogle Scholar
  42. Mevik BH, Wehrens R (2007) The pls package: principal component and partial least squares regression in R. J Stat Soft 18:1–24CrossRefGoogle Scholar
  43. Nalepa CA (2015) Origin of termite eusociality: trophallaxis integrates the social, nutritional, and microbial environments. Ecol Entomol 40:323–335CrossRefGoogle Scholar
  44. Nutting WL (1969) Flight and colony foundation. In: Krishna K, Weesner F (eds) Biology of Termites. Academic Press, New York, pp 233–282CrossRefGoogle Scholar
  45. Pequeno L, Franklin E, Venticinque EM, Serrao AAN (2013) The scaling of colony size with nest volume in termites: a role in population dynamics? Ecol Entomol 38:515–521CrossRefGoogle Scholar
  46. R Development Core Team (2012) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna http://www.R-project.org/)
  47. Reeves I, McCarty GW, Mimmo T (2002) The potential of diffuse reflectance spectroscopy for the determination of carbon inventories in soils. Environ Pollut 116:277–284CrossRefGoogle Scholar
  48. Reeves I, James B (2010) Near- versus mid-infrared diffuse reflectance spectroscopy for soil analysis emphasizing carbon and laboratory versus on-site analysis: Where are we and what needs to be done? Geoderma 158:3–14CrossRefGoogle Scholar
  49. Roisin Y (2000) Diversity and evolution of caste patterns. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Springer, Dordrecht, pp 95–119CrossRefGoogle Scholar
  50. Roonwal ML (1970) Measurements of termites (Isoptera) for taxonomic purposes. J Zool Soc India 21:9–66Google Scholar
  51. Roonwal ML (1978) Bioecological and economical observations on termites of Peninsular India. Z Angew Entomol 85:15–30CrossRefGoogle Scholar
  52. Rossel VRA, Walvoort DJJ, McBratney AB, Janik LJ, Skjemstad JO (2006) Visible, near infrared, mid infrared or combined diffuse reflectance spectroscopy for simultaneous assessment of various soil properties. Geoderma 131:59–75CrossRefGoogle Scholar
  53. Spragg WT, Paton R (1980) Tracing, trophallaxis and population measurement of colonies of subterranean termites (Isoptera) using a radioactive tracer. Ann Entomol Soc Am 73:708–714CrossRefGoogle Scholar
  54. Stuart BH (2004) Organic molecules. In: Infrared spectroscopy: fundamentals and applications. Wiley, Chichester, pp 71–93CrossRefGoogle Scholar
  55. Suárez ME, Thorne BL (2000) Rate, amount, and distribution pattern of alimentary fluid transfer via trophallaxis in three species of termites (Isoptera: Rhinotermitidae, Termopsidae). Ann Entomol Soc Am 93:145–155CrossRefGoogle Scholar
  56. Tenenhaus M (1998) La régression PLS: théorie et pratique. Editions Technip, ParisGoogle Scholar
  57. Thorne BL, Haverty MI (1991) A review of intracolony, intraspecific, and interspecific agonism in termites. Sociobiology 19:115–145Google Scholar
  58. Thorne BL (1997) Evolution of eusociality in termites. Annu Rev Ecol Syst 28:27–54CrossRefGoogle Scholar
  59. Turner JS (2004) Extended phenotypes and extended organisms. Biol Philos 19:327–352CrossRefGoogle Scholar
  60. Velasquez E, Pelosi C, Brunet D, Grimaldi M, Martins M, Rendeiro AC, Barrios E, Lavelle P (2007) This ped is my ped: visual separation and near infrared spectra allow determination of the origins of soil macroaggregates. Pedobiologia 51:75–87CrossRefGoogle Scholar
  61. Waller D, La Fage J (1988) Environmental influence on soldier differentiation in Coptotermes formosanus Shiraki (Rhinotermitidae). Insect Soc 35:144–152CrossRefGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2017

Authors and Affiliations

  • P. Jouquet
    • 1
    • 2
  • A. Pando
    • 1
  • H. Aroui
    • 1
  • A. Harit
    • 2
  • Y. Capowiez
    • 3
  • N. Bottinelli
    • 1
    • 4
  1. 1.Institute of Ecology and Environmental Sciences (UMR 242 iEES Paris), Institute of Research for Development (IRD)BondyFrance
  2. 2.Indo-French Cell for Water Science (IFCWS), Indian Institute of ScienceBangaloreIndia
  3. 3.INRA, UR1115 ‘Plantes et Systèmes de culture Horticoles’Avignon cedex 09France
  4. 4.Soils and Fertilizers Research Institute (SFRI)HanoiVietnam

Personalised recommendations