Skip to main content
SpringerLink
Log in

The role of wax and resin in the nestmate recognition system of a stingless bee, Tetragonisca angustula

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Recent research has shown that entrance guards of the stingless bee Tetragonisca angustula make less errors in distinguishing nestmates from non-nestmates than all other bee species studied to date, but how they achieve this is unknown. We performed four experiments to investigate nestmate recognition by entrance guards in T. angustula. We first investigated the effect of colony odours on acceptance. Nestmates that acquired odour from non-nestmate workers were 63% more likely to be rejected while the acceptance rate of non-nestmates treated with nestmate odour increased by only 7%. We further hypothesised that guards standing on the wax entrance tube might use the tube as an odour referent. However, our findings showed that there was no difference in the acceptance of non-nestmates by guards standing on their own colony’s entrance tube versus the non-nestmate’s entrance tube. Moreover, treatment of bees with nestmate and non-nestmate resin or wax had a negative effect on acceptance rates of up to 65%, regardless of the origin of the wax or resin. The role of resin as a source of recognition cues was further investigated by unidirectionally transferring resin stores between colonies. Acceptance rates of nestmates declined by 37% for hives that donated resin, contrasting with resin donor hives where acceptance of non-nestmates increased by 21%. Overall, our results confirm the accuracy of nestmate recognition in T. angustula and reject the hypothesis that this high level of accuracy is due to the use of the wax entrance tubes as a referent for colony odour. Our findings also suggest that odours directly acquired from resin serve no primary function as nestmate recognition cues. The lack of consistency among colonies plus the complex results of the third and fourth experiments highlight the need for further research on the role of nest materials and cuticular profiles in understanding nestmate recognition in T. angustula.

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

References

  • Abdalla FC, Jones GR, Morgan ED, da Cruz-Landim C (2003) Comparative study of the cuticular hydrocarbon composition of Melipona bicolor Lepeletier, 1836 (Hymenoptera, Meliponini) workers and queens. Genet Mol Res 2:191–199

    PubMed  CAS  Google Scholar 

  • Bates D (2007) lme4: Linear mixed-effects models using S4 classes. R package version 0.99875-7

  • Beale G (1990) Self and nonself recognition in the ciliate protozoan Euplotes. Trends Genet 6:137–139

    Article  PubMed  CAS  Google Scholar 

  • Bell WJ, Breed MD, Richards KW, Michener CD (1974) Social, stimulatory and motivational factors involved in intraspecific nest defense of a primitively eusocial halictine bee. J Comp Physiol 93:173–181

    Article  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Breed MD (1983) Nestmate recognition in honey bees. Anim Behav 31:86–91

    Article  Google Scholar 

  • Breed MD, Page RE (1991) Intra- and interspecific nestmate recognition in Melipona workers (Hymenoptera: Apidae). J Insect Behav 4:463–469

    Article  Google Scholar 

  • Breed MD, Garry MF, Pearce AN, Hibbard BE, Bjostad LB, Page J (1995) The role of wax comb in honey bee nestmate recognition. Anim Behav 50:489–496

    Article  Google Scholar 

  • Breed MD, Diaz PH, Lucero KD (2004) Olfactory information processing in honeybee, Apis mellifera, nestmate recognition. Anim Behav 68:921–928

    Article  Google Scholar 

  • Buchwald R, Breed MD (2005) Nestmate recognition cues in a stingless bee, Trigona fulviventris. Anim Behav 70:1331–1337

    Article  Google Scholar 

  • Butler CG, Free JB (1952) The behaviour of worker honey bees at the hive entrance. Behaviour 4:262–292

    Article  Google Scholar 

  • Couvillon MJ, Ratnieks FLW (2008) Odour transfer in stingless bee marmelada (Frieseomelitta varia) demonstrates that entrance guards use an “undesirable–absent” recognition system. Behav Ecol Sociobiol 62:1099–1105

    Article  Google Scholar 

  • Couvillon MJ, Caple JP, Endsor SL, Kärcher MH, Russell TF, Storey DE, Ratnieks FLW (2007a) Nest-mate recognition template of guard honeybees (Apis mellifera) is modified by wax comb transfer. Biol Lett 3:228–230

    Article  PubMed  Google Scholar 

  • Couvillon MJ, Wenseleers T, Imperatriz-Fonseca VL, Nogueira-Neto P, Ratnieks FLW (2007b) Comparative study in stingless bees (Meliponini) demonstrates that nest entrance size predicts traffic and defensivity. J Evol Biol 21:194–201

    PubMed  Google Scholar 

  • Couvillon MJ, Robinson EJH, Atkinson B, Child L, Dent KR, Ratnieks FLW (2008) En garde: rapid shifts in honeybee, Apis mellifera, guarding behaviour are triggered by onslaught of conspecific intruders. Anim Behav 76:1653–1658

    Article  Google Scholar 

  • Couvillon MJ, Roy GGF, Ratnieks FLW (2009) Recognition errors by honey bee (Apis mellifera) guards demonstrate overlapping cues in conspecific recognition. J Apicult Res 48:225–232

    Article  Google Scholar 

  • Couvillon MJ, Barton SN, Cohen JA, Fabricius OK, Kärcher MH, Cooper LS, Silk MJ, Helanterä H, Ratnieks FLW (2010) Alarm pheromones do not mediate rapid shifts in honey bee guard acceptance threshold. J Chem Ecol 36:1306–1308

    Article  PubMed  CAS  Google Scholar 

  • d’Ettorre P, Heinze J (2005) Individual recognition in ant queens. Curr Biol 15:2170–2174

    Article  PubMed  Google Scholar 

  • d’Ettorre P, Wenseleers T, Dawson J, Hutchinson S, Boswell T, Ratnieks FLW (2006) Wax combs mediate nestmate recognition by guard honeybees. Anim Behav 71:773–779

    Article  Google Scholar 

  • Downs SG, Ratnieks FLW (1999) Recognition of conspecifics by honeybee guards uses nonheritable cues acquired in the adult stage. Anim Behav 58:643–648

    Article  PubMed  Google Scholar 

  • Downs SG, Ratnieks FLW (2000) Adaptive shifts in honey bee (Apis mellifera L.) guarding behavior support predictions of the acceptance threshold model. Behav Ecol 11:326–333

    Article  Google Scholar 

  • Downs SG, Ratnieks FLW, Jeffries SL, Rigby HE (2000) The role of floral oils in the nestmate recognition system of honey bees (Apis mellifera L.). Apidologie 31:357–365

    Article  Google Scholar 

  • Downs SG, Ratnieks FLW, Badcock NS, Mynott A (2001) Honeybee guards do not use food-derived odours to recognize non-nest mates: a test of the odour convergence hypothesis. Behav Ecol 12:47–50

    Google Scholar 

  • Espelie KE, Wenzel JW, Chang G (1990) Surface lipids of social wasp Polistes melricus say and its nest and nest pedicel and their relation to nestmate recognition. J Chem Ecol 16:2229–2241

    Article  CAS  Google Scholar 

  • Gastauer M, Campos LAO, Wittmann D (2011) Handling sticky resin by stingless bees (Hymenoptera, Apidae). Rev Bras Entomol 55:234–240

    Article  Google Scholar 

  • Glass NL, Kaneko I (2003) Fatal attraction: non-self recognition and heterokaryon incompatibility in filamentous fungi. Eukaryot Cell 2:1–8

    Article  PubMed  CAS  Google Scholar 

  • Grüter C, Kärcher MH, Ratnieks FLW (2011) The natural history of nest defence in a stingless bee, Tetragonisca angustula (Latreille) (Hymenoptera: Apidae), with two distinct types of entrance guards. Neotrop Entomol 40:55–61

    Article  PubMed  Google Scholar 

  • Guerrieri FJ, Nehring V, Jørgensen CG, Nielsen J, Galizia CG, d’Ettorre P (2009) Ants recognize foes and not friends. P R Soc B 276:2461–2468

    Article  CAS  Google Scholar 

  • Janeway CA, Medzhitov R (2002) Innate immune recognition. Ann Rev Immunol 20:197–216

    Article  CAS  Google Scholar 

  • Jungnickel H, da Costa AJS, Tentschert J, Patricio EFLRA, Imperatriz-Fonseca VL, Drijfhout F, Morgan ED (2004) Chemical basis for inter-colonial aggression in the stingless bee Scaptotrigona bipunctata (Hymenoptera: Apidae). J Insect Physiol 50:761–766

    Article  PubMed  CAS  Google Scholar 

  • Kärcher MH, Ratnieks FLW (2009) Standing and hovering guards of the stingless bee Tetragonisca angustula complement each other in entrance guarding and intruder recognition. J Apicult Res 48:209–214

    Article  Google Scholar 

  • Kerr WE, Jungnickel H, Morgan ED (2004) Workers of the stingless bee Melipona scutellaris are more similar to males than to queens in their cuticular compounds. Apidologie 35:611–618

    Article  Google Scholar 

  • Lacy RC, Sherman PW (1983) Kin recognition by phenotype matching. Am Nat 121:489–512

    Article  Google Scholar 

  • Leonhardt SD, Blüthgen N, Schmitt T (2009) Smelling like resin: terpenoids account for species-specific cuticular profiles in Southeast-Asian stingless bees. Insectes Soc 56:157–170

    Article  Google Scholar 

  • Leonhardt SD, Schmitt T, Blüthgen N (2011) Tree Resin Composition, Collection Behavior and Selective Filters Shape Chemical Profiles of Tropical Bees (Apidae: Meliponini). PLoS ONE 6:e23445

  • Leonhardt SD, Blüthgen N, Schmitt T (2011) Chemical profiles of body surfaces and nests from six Bornean stingless bee species. J Chem Ecol 37:98–104

    Article  PubMed  CAS  Google Scholar 

  • Martin SJ, Helanterä H, Drijfhout FP (2008) Colony-specific hydrocarbons identify nest mates in two species of Formica ant. J Chem Ecol 34:1072–1080

    Article  PubMed  CAS  Google Scholar 

  • Michener CD (1974) The social behaviour of the bees. Harvard University Press, Cambridge

    Google Scholar 

  • Nasrallah JB (2002) Recognition and rejection of self in plant reproduction. Science 296:305–308

    Article  PubMed  CAS  Google Scholar 

  • Nogueira-Neto P (1997) Vida e criação de abelhas indigenas sem ferrão. Editora Nogueirapis, São Paulo

  • Nunes TM, Nascimento FS, Turatti IC, Lopes NP, Zucchi R (2008) Nestmate recognition in a stingless bee: does the similarity of chemical cues determine guard acceptance? Anim Behav 75:1165–1171

    Article  Google Scholar 

  • Nunes TM, Mateus S, Turatti IC, Morgan ED, Zucchi R (2011) Nestmate recognition in the stingless bee Frieseomelitta varia (Hymenoptera, Apidae, Meliponini): sources of chemical signals. Anim Behav 81:463–467

    Article  Google Scholar 

  • Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Y, Nisimura T, Yamaoka R (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309:311–314

    Article  PubMed  CAS  Google Scholar 

  • Ratnieks FLW (1991) Facultative sex allocation biasing by workers in social Hymenoptera. Evolution 45:281–292

    Article  Google Scholar 

  • Ratnieks FLW, Kärcher MH, Firth V, Parks D, Richards A, Richards P, Helanterä H (2011) Acceptance by honey bee guards of non–nestmates is not increased by treatment with nestmate odours. Ethology 117:655–663

    Article  Google Scholar 

  • R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat 133:407–435

    Article  Google Scholar 

  • Roubik DW (2006) Stingless bee nesting biology. Apidologie 37:124–143

    Article  Google Scholar 

  • Sawaya ACHF, Cunha IBS, Marcucci MC, Rodrigues RFD, Eberlin MN (2006) Brazilian propolis of Tetragonisca angustula and Apis mellifera. Apidologie 37:398–407

    Article  CAS  Google Scholar 

  • Sherman PW, Reeve HK, Pfennig DW (1997) Recognition systems: behavioural ecology: an evolutionary approach, 4th edn. Wiley-Blackwell, Cambridge, pp 69–96

    Google Scholar 

  • Tibbetts EA (2002) Visual signals of individual identity in the wasp Polistes fuscatus. P Roy Soc Lond B Bio 269:1423–1428

    Article  Google Scholar 

  • van Veen JW, Sommeijer MJ (2000) Observations on gynes and drones around nuptial flights in the stingless bees Tetragonisca angustula and Melipona beecheii (Hymenoptera, Apidae, Meliponinae). Apidologie 31:47–54

    Article  Google Scholar 

  • van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons: insect hydrocarbons. Cambridge University Press, Cambridge, pp 222–243

    Google Scholar 

  • van Zweden JS, Grüter C, Jones SM, Ratnieks FLW (2011) Hovering guards of the stingless bee Tetragonisca angustula increase colony defensive perimeter as shown by intra- and inter-specific comparisons. Behav Ecol Sociobiol 65:1277–1282

    Article  Google Scholar 

  • Vander Meer RK, Saliwanchik D, Lavine B (1989) Temporal changes in colony cuticular hydrocarbon patterns of Solenopsis invicta—implications for nestmate recognition. J Chem Ecol 15:2115–2125

    Article  CAS  Google Scholar 

  • Vander Meer RK, Breed MD, Espelie KE, Winston M (1998) Nestmate recognition in ants. In: Vander Meer RK (ed) Pheromone communication in social insects: ants, wasps, bees and termites. Westview, Oxford

    Google Scholar 

  • Velikova M, Bankova V, Marcucci MC, Tsvetkova I, Kujumgiev A (2000) Chemical composition and biological activity of propolis from Brazilian Meliponinae. Z Naturforsch C 55:785–789

    PubMed  CAS  Google Scholar 

  • Wille A (1983) Biology of the stingless bees. Ann Rev Entomol 28:41–64

    Article  Google Scholar 

  • Wittmann D (1985) Aerial defense of the nest by workers of the stingless bee Trigona (Tetragonisca) angustula (Latreille) (Hymenoptera: Apidae). Behav Ecol Sociobiol 16:111–114

    Article  Google Scholar 

  • Wittmann D, Radtke R, Zeil J, Lübke G, Francke W (1990) Robber bees (Lestrimelitta limao) and their host chemical and visual cues in nest defense by Trigona (Tetragonisca) angustula (Apidae: Meliponinae). J Chem Ecol 16:631–641

    Article  CAS  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, p 574

    Book  Google Scholar 

Download references

Acknowledgements

We thank Dr. Paulo Noguiera-Neto for his hospitality at Fazenda Aretuzina and giving us permission to manipulate and study his bee colonies. We also thank Dr. Margaret Couvillon, Associate Editor, Dr William Hughes and anonymous referees for their comments and criticisms. S.M.J. was funded by a GTA grant from the University of Sussex. J.S.v.Z. was supported by a postdoctoral fellowship from the Danish Council for Independent Research (09066595) and C.G. by a postdoctoral fellowship from the Swiss National Science Foundation (SNSF grant PBBEP3-123648). T.C. was supported by a Ph.D. studentship from BBSRC. FAPESP provided funding for C.M. (07/50218-1), D.A.A. (05/58093-8; 10/19717-4), P.N.S (07/03864-5), V.L.I.F. (04/15801-0) and F.L.W.R (08/57782-2).

Author information

Author notes

  1. Jelle S. van Zweden

    Present address: Centre for Social Evolution, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark

  2. Cristiano Menezes

    Present address: Embrapa Amazônia Oriental, Trav. Dr. Enéas Pinheiro s/ nr., Belém, Para, Brazil

  3. Vera L. Imperatriz-Fonseca

    Present address: Universidade Federal Rural do Semiárido, Mossoró, Rio Grande do Norte, Brazil

Authors and Affiliations

  1. Laboratory of Apiculture and Social Insects, School of Life Sciences, University of Sussex, Falmer, Brighton, BN1 9QG, UK

    Sam M. Jones, Jelle S. van Zweden, Christoph Grüter, Tomer Czaczkes & Francis L. W. Ratnieks

  2. Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, USP, Avenida Bandeirantes nr, 3900, Monte Alegre, Ribeirão Preto, SP, Brazil

    Cristiano Menezes, Denise A. Alves, Patrícia Nunes-Silva & Vera L. Imperatriz-Fonseca

  3. Departamento de Ecologia, Instituto de Biociências, USP, Rua do Matão, trav. 14 nr. 321, Cidade Universitária, São Paulo, Brazil

    Denise A. Alves

Authors
  1. Sam M. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jelle S. van Zweden
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christoph Grüter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cristiano Menezes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Denise A. Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Patrícia Nunes-Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tomer Czaczkes
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Vera L. Imperatriz-Fonseca
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Francis L. W. Ratnieks
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sam M. Jones.

Additional information

Communicated by W. Hughes

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 660 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jones, S.M., van Zweden, J.S., Grüter, C. et al. The role of wax and resin in the nestmate recognition system of a stingless bee, Tetragonisca angustula . Behav Ecol Sociobiol 66, 1–12 (2012). https://doi.org/10.1007/s00265-011-1246-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-011-1246-7

Keywords

Search

Navigation