Abstract
Stingless bees are important pollinators of plants, and also producers of honey. Species within the African stingless bee genus Hypotrigona are difficult to differentiate due to morphological similarities. Chemical profiles of whole head extracts from workers of three Hypotrigona species: H. gribodoi, H. araujoi and H. ruspolii were studied by gas chromatography–mass spectrometry. A total of 50 components belonging to six chemical classes: hydrocarbons, aldehydes, alcohols, terpenoids, steroids and fatty acids were identified. Twenty-nine compounds were found in H. araujoi, 26 in H. gribodoi and 33 in H. ruspolii head extracts. Hydrocarbons, alcohols and fatty acids were the major classes, whilst steroids and terpenoids were minor. Aldehydes were found only in H. ruspolii while terpenoids were only present in extracts of H. gribodoi and H. araujoi. Eight chemical compounds were specific to H. araujoi, six to H. gribodoi and nine to H. ruspolii, showing both qualitative and quantitative differences. Workers were successfully grouped into their respective species using their chemical profiles. This study shows that head extracts can be used as a reliable taxonomic tool for identifying and differentiating Hypotrigona species.
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References
Blum M, Brand J (1972) Social insect pheromones: their chemistry and function. Am Zool 12:553–576
Carlson DA, Roan CS, Yost RA et al (1989) Dimethyl disulphide derivatives of long-chain alkenes, alkadienes, and alkatrienes for gas chromatography/mass spectrometry. Anal Chem 61:1564–1571
Cruz-López L, Patricio E, Morgan E (2001) Secretions of stingless bees: the Dufour gland of Nannotrigona testaceicornis. J Chem Ecol 27:69–80
Cruz-López L, Malo EAE, Morgan ED et al (2005) Mandibular gland secretion of Melipona beecheii: chemistry and behavior. J Chem Ecol 31:1621–1632. https://doi.org/10.1007/s10886-005-5802-3
Dani FR, Jones GR, Corsi S et al (2005) Nest mate recognition cues in the honey Bee: differential importance of cuticular alkanes and alkenes. Chem Sens 30:477–489. https://doi.org/10.1093/chemse/bji040
De Meulemeester T, Gerbaux P, Boulvin M (2011) A simplified protocol for bumble bee species identification by cephalic secretion analysis. Insectes Soc 58:227–236. https://doi.org/10.1007/s00040-011-0146-1 doi
Eardley CD (2004) Taxonomic revision of the African stingless bees (Apoidea: Apidae: Apinae: Meliponini). Afri Plant Prot 10:63–96
Engels W, Engels E, Lübke G (1990) Volatile cephalic secretions of drones, queens and workers in relation to reproduction in the stingless bee, Scaptotrigona postica (Hymenoptera: Apidae: Trigonini). Entomol Gen 15:91–101
Engels E, Engels W, Lubke G et al (1993) Age-related patterns of volatile cephalic constituents in queens of the neotropical stingless bee Scaptotrigona-postica Latr (Hymenoptera, Apidae). Apidologie 24:539–548. https://doi.org/10.1051/apido:19930601
Engels W, Engels E, Francke W (1997) Ontogeny of cephalic volatile patterns in queens and mating biology of the neotropical stingless bee, Scaptotrigona postica. Invertebr Reprod Dev 31:251–256. https://doi.org/10.1080/07924259.1997.9672583
Fombong AT, Teal PE, Arbogast RT et al (2012) Chemical communication in the honey bee scarab pest Oplostomus haroldi: role of (Z)-9-pentacosene. J Chem Ecol 38:1463–1473
Francke W, Lübke G, Schröder W et al (2000) Identification of oxygen containing volatiles in cephalic secretions of workers of Brazilian stingless bees. J Braz Chem Soc 11:562–571
Free JBJ (1987) Pheromones of social bees. Chapman and Hall, London, p 154
Gracioli-Vitti LF, Cruz-landim C, Abdalla F (2012) Volatile substances of mandibular gland secretion of a stingless bee: Scaptotrigona postica Latreille. Anim Biol 3:78–88
Heard TAT (1999) The role of stingless bees in crop pollination. Annu Rev Entomol 44:183–206. https://doi.org/10.1146/annurev.ento.44.1.183
Jarau S, Schulz CM, Hrncir M, Francke W, Zucchi R, Barth FG, Ayasse M (2006) Hexyl Decanoate, the first trail pheromone compound identified in a stingless bee, Trigona recursa. J Chem Ecol 32:1555–1564
Kakutani T, Inoue T, Tezuka T, Maeta Y (1993) Pollination of strawberry by the stingless bee, Trigona minangkabau and the honey bee, Apis mellifera: an experimental study of fertilization efficiency. Res Popul Ecol 35:95–111
Kather MR, Drijfhout FP, Martin JS (2011) Task group differences in cuticular lipids in the honey bee Apis mellifera ricarda. J Chem Ecol 37:205–212. https://doi.org/10.1007/s10886-014-0423-3
Kiatoko N, Kumar RS, Langevelde F (2016) A vertical compartmented hive design for reducing post-harvest colony losses in three afrotropical stingless bee species (APIDAE: MELIPONINAE). IJDR 6:9026–9034
Le Conte Y, Hefetz A (2008) Primer pheromones in social hymenoptera. Annu Rev Entomol 53:523–542. https://doi.org/10.1146/annurev.ento.52.110405.091434
Leonhardt S (2017) Chemical ecology of stingless bees. J Chem Ecol 43:385–402. https://doi.org/10.1007/s10886-017-0837-9
Leonhardt SD, Blüthgen N, Schmitt T (2009) Smelling like resin: terpenoids account for species-specific cuticular profiles in South East-Asian stingless bees. Insectes Soc 56:157–170. https://doi.org/10.1007/s00040-009-0007-3
López LC, Patricio E, Maile R, Morgan E (2002) Secretions of stingless bees: cephalic secretions of two Frieseomelitta species. J Insect Physiol 48:453–458
Martin SJ, Shemilt SC, Cândida B et al (2017) Are isomeric alkenes used in species recognition among neo-tropical stingless bees (Melipona spp.). J Chem Ecol 43:1066–1072. https://doi.org/10.1007/s10886-017-0901-5
Michener CD (1959) Sibling species of Trigona from Angola (Hymenoptera, Apinae). Am Mus Novit 1956:1–5
Michener C (2007) The bees of the world, 2nd edn. The Johns Hopkins University Press, Baltimore, p 803
Moure JS (1961) A preliminary supra-specific classification of the old world meliponine bees (Hymenoptera, Apoidea). Studia Ent 4:181–242
Ndungu NN, Nkoba K, Sole CL et al (2018) Resolving taxonomic ambiguity and cryptic speciation of Hypotrigona species through morphometrics and DNA barcoding. J Api Res 8839:1–10. https://doi.org/10.1080/00218839.2018.1426348
Nkoba K, Raina SK, Muli E et al (2012) Species richness and nest dispersion of some tropical meliponine bees (Apidae: Meliponinae) in six habitat types in the Kakamega forest, western Kenya. Int J Trop Insect Sci 32:194–202. https://doi.org/10.1017/S1742758412000355
Patricio E, López L, Maile R, Morgan E (2003) Secretions of stingless bees: the Dufour glands of some Frieseomelitta species (Apidae, Meliponinae). Apidologie 34:359–365. https://doi.org/10.1051/apido:2003027
Poiani SB, Morgan ED, Drijfhout FP, da Cruz-Landim C (2014) Separation of Scaptotrigona postica workers into defined task groups by the chemical profile on their epicuticle wax layer. J Chem Ecol 40:331–340. https://doi.org/10.1007/s10886-014-0423-3
Rasmussen C, Cameron S (2010) Global stingless bee phylogeny supports ancient divergence, variance, and long distance dispersal. Biol J Linn Soc 99:206–232
Schorkopf D, Jarau S, Francke W et al (2007) Spitting out information: Trigona bees deposit saliva to signal resource locations. P R Soc B 274:895–898
Schorkopf D, Hrncir M, Mateus S et al (2009) Mandibular gland secretions of meliponine worker bees: further evidence for their role in interspecific and intraspecific defence and aggression and against their role in food source signalling. J Exp Biol 212:1153–1162. https://doi.org/10.1242/jeb.021113
Yusuf AA, Pirk CWW, Crewe RM et al (2010) Nestmate recognition and the role of cuticular hydrocarbons in the African termite raiding ant Pachycondyla analis. J Chem Ecol 36:441–448. https://doi.org/10.1007/s10886-010-9774-6
Yusuf AA, Pirk CWW, Crewe RM (2015) Mandibular gland pheromone contents in workers and queens of Apis mellifera adansonii. Apidologie 46:559–572. https://doi.org/10.1007/s13592-014-0346-6
Acknowledgements
The authors would like to thank members of Bee Health and Molecular Biology and Bioinformatics (MBBU) teams at ICIPE for their technical support. We acknowledge the financial support for this research by the following organizations and agencies: the European Union (EU) (Grant Contract No. DCI-FOOD/2013/313-659: African Reference Laboratory (with satellite stations) for the Management of Pollination Bee Diseases and Pests for Food Security); the South African National Research Foundation (NRF) Research Career Advancement Fellowship (Grant no: 91419) to AAY; NRF Incentive Funding for Rated Researchers to CWWP and AAY; UK Aid from the UK Government; Swedish International Development Cooperation Agency (Sida); the Swiss Agency for Development and Cooperation (SDC) and the Kenyan Government. The first author was supported by a German Academic Exchange Service (DAAD) In-Region Postgraduate Scholarship.
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Communicated by Günther Raspotnig.
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Ndungu, N.N., Kiatoko, N., Masiga, D.K. et al. Compounds extracted from heads of African stingless bees (Hypotrigona species) as a prospective taxonomic tool. Chemoecology 28, 51–60 (2018). https://doi.org/10.1007/s00049-018-0256-6
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DOI: https://doi.org/10.1007/s00049-018-0256-6





