Skip to main content

Two aggressive neighbours living peacefully: the nesting association between a stingless bee and the bullet ant

Insectes Sociaux volume 67, pages 103–112 (2020)Cite this article

Abstract

Stingless bees often associate with termites, while association with ants is uncommon due to the high costs related to the aggressiveness of ants. Few combative genera of stingless bees can associate with a larger number of hosts, including ants. Here, we describe for the first time the association between a stingless bee (Partamona testacea) and the aggressive predator bullet ant (Paraponera clavata). In the study area, the colonies of P. testacea we spotted were all associated with P. clavata or Atta sp. ants. COI mitochondrial gene sequences of bees associated with bullet ants and leafcutter ants did not show any divergence, thus revealing no evidence that the two nesting strategies represent a case of cryptic speciation and specialisation on specific hosts. Bees are not unarmed respect to the bullet ants; when ants attempted to penetrate in the colony entrance, they were dragged inside the nest and covered by a resin-like substance. Behavioural experiments focused on ants in arenas and focused on bees at their nest entrance proved that the ants are significantly less aggressive toward associated bees and that guard bees are less alarmed when associated ants are presented. We verified by Gas Chromatography and Mass Spectrometry that P. testacea maintains its species-specific cuticular signature in the association with different ant species and that ants and bees possess typical colony signatures. The differential behavioural responses expressed toward associated colony members by both species are likely based on learning these heterospecific cuticular signatures as it occurs in ant parabiotic associations.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Aitchison J (1982) The statistical analysis of compositional data. J R Stat Soc Ser B Stat Methodol 44(2):139–177

    Google Scholar 

  • Breed MD, Butler L, Stiller TM (1985) Kin discrimination by worker honey bees in genetically mixed groups. Proc Natl Acad Sci USA 82:3058–3061

    CAS  Article  Google Scholar 

  • Camargo JM, Pedro SR (2003) Meliponini neotropicais: o gênero Partamona Schwarz, 1939 (Hymenoptera, Apidae, Apinae)-bionomia e biogeografia. Rev Bras Entomol 47:311–372

    Article  Google Scholar 

  • Carrijo TF, Gonçalves RB, Santos RG (2012) Review of bees as guests in termite nests, with a new record of the communal bee, Gaesochira obscura (Smith, 1879) (Hymenoptera, Apidae), in nests of Anoplotermes banksi Emerson, 1925 (Isoptera, Termitidae, Apicotermitinae). Insect Soc 59:141–149. https://doi.org/10.1007/s00040-012-0218-x

    Article  Google Scholar 

  • Dani FR, Jones GR, Corsi S, Beard R, Pradella D, Turillazzi S (2005) Nestmate recognition cues in the honey bee: differential importance of cuticular alkanes and alkenes. Chem Senses 30:477–489

    CAS  Article  Google Scholar 

  • de Camargo JMF (1980) O grupo Partamona (Partamona) testacea (Klug): suas espécies, distribuição e diferenciação geográfica (Meliponinae, Apidae, Hymenoptera). Acta Amazon 10:5–175

    Article  Google Scholar 

  • Dejean A (2011) Prey capture behavior in an arboreal African ponerine ant. PLoS One 6(5):e19837

    CAS  Article  Google Scholar 

  • Dincă V, Montagud S, Talavera G et al (2015) DNA barcode reference library for Iberian butterflies enables a continental-scale preview of potential cryptic diversity. Sci Rep. https://doi.org/10.1038/srep12395

    Article  PubMed  PubMed Central  Google Scholar 

  • Emery VJ, Tsutsui ND (2013) Recognition in a social symbiosis: chemical phenotypes and nestmate recognition behaviors of neotropical parabiotic ants. PLoS One 8(2):e56492

    CAS  Article  Google Scholar 

  • Errard C, Regla JI, Hefetz A (2003) Interspecific recognition in Chilean parabiotic ant species. Insect Soc 50:268–273

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Guerrieri FJ, d’Ettorre P (2008) The mandible opening response: quantifying aggression elicited by chemical cues in ants. J Exp Biol 211:1109–1113

    CAS  Article  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc B 270:313–321. https://doi.org/10.1098/rspb.2002.2218

    CAS  Article  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    CAS  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 

  • Lenoir A, d’Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599

    CAS  Article  Google Scholar 

  • Leonhardt SD, Wallace HM, Schmitt T (2011) The cuticular profiles of Australian stingless bees are shaped by resin of the eucalypt tree Corymbia torelliana. Austral Ecol 36:537–543

    Article  Google Scholar 

  • Menzel F, Schmitt T (2012) Tolerance requires the right smell: first evidence for interspecific selection on chemical recognition cues. Evolution 66:896–904

    Article  Google Scholar 

  • Menzel F, Blüthgen N, Schmitt T (2008) Tropical parabiotic ants: highly unusual cuticular substances and low interspecific discrimination. Front Zool 5:16

    Article  Google Scholar 

  • Michener CD (2000) The bees of the world, vol 1. JHU Press, Baltimore

    Google Scholar 

  • Nunes TM, Turatti IC, Lopes NP, Zucchi R (2009) Chemical signals in the stingless bee, Frieseomelitta varia, indicate caste, gender, age, and reproductive status. J Chem Ecol 35:1172

    CAS  Article  Google Scholar 

  • Orivel J, Errard C, Dejean A (1997) Ant gardens: interspecific recognition in parabiotic ant species. Behav Ecol Sociobiol 40:87–93

    Article  Google Scholar 

  • Ratnasingham S, Hebert PD (2013) A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE 8(7):e66213

    CAS  Article  Google Scholar 

  • Roubik DW (1983) Nest and colony characteristics of stingless bees from Panama (Hymenoptera: Apidae). J Kans Entomol Soc 56:327–355

    Google Scholar 

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

    Article  Google Scholar 

  • Sakagami SF, Inoue T, Yamane S, Salmah S (1989) Nests of the myrmecophilous stingless bee, Trigona moorei: how do bees initiate their nest within an arboreal ant nest? Biotropica 21:265–274

    Article  Google Scholar 

  • Schwarz HF (1948) Stingless bees (Meliponinae) of the western hemisphere. Bull Am Mus Nat Hist 90:1–546

    Google Scholar 

  • Siqueira ENL, Bartelli BF, Nascimento ART, Nogueira-Ferreira FH (2012) Diversity and nesting substrates of stingless bees (Hymenoptera, Meliponina) in a forest remnant. Psyche 2012:1–9

    Article  Google Scholar 

  • Stucky BJ (2012) SeqTrace: a graphical tool for rapidly processing DNA sequencing chromatograms. J Biomolec Tech JBT 23:90

    Article  Google Scholar 

  • van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. Insect Hydrocarb Biol Biochem Chem Ecol 11:222–243

    Article  Google Scholar 

  • Wille A, Michener CD (1973) The nest architecture of stingless bees with special reference to those of Costa Rica (Hymenoptera, Apidae). Rev Biol Trop 21:1–278

    Google Scholar 

  • Wilson EO (1971) The insect societies. Harvard University Press, Cambridge Mass

    Google Scholar 

  • Young AM, Hermann HR (1980) Notes on foraging of the giant tropical ant Paraponera clavata (Hymenoptera: Formicidae: Ponerinae). J Kans Entomol Soc 53:35–55

    Google Scholar 

Download references

Acknowledgements

This work was supported by funds from Florence University and from Urku estudios Amazonicos, by Canziani funding to AL (University of Bologna) and by an International Mobility fund granted to AB by the University of Ferrara. Permits for collecting and exporting specimens were obtained by Peruvian ministry (RESOLUCIÓN DIRECTORAL EJECUTIVA N. 265-2017/GRSM/ARA/DEACRN). We thank two anonymous referees for critically reading the manuscript and suggesting substantial improvements.

Author information

Author notes

  1. Leonardo Dapporto and Marilena Marconi co-supervised the study.

Authors and Affiliations

  1. Dipartimento di Biologia dell’Università degli studi di Firenze, Sesto Fiorentino, Firenze, Italy

    A. Bordoni, G. Mocilnik, M. Bercigli, S. Turillazzi & L. Dapporto

  2. Dipartimento di Scienze Biologiche Geologiche e Ambientali, Università di Bologna, Bologna, Italy

    G. Forni & A. Luchetti

  3. Urku Estudios Amazónicos, Tarapoto, Peru

    C. D. V. Giove & M. Marconi

  4. Centro Interdipartimentale di Spettrometrie di Massa, Università degli studi di Firenze, Firenze, Italy

    S. Turillazzi

Authors
  1. A. Bordoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Mocilnik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. Forni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Bercigli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. D. V. Giove
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. Luchetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. S. Turillazzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. L. Dapporto
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. M. Marconi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Bordoni.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 9 (M4 V 3448 kb)

Supplementary material 10 (M4 V 1553 kb)

Supplementary material 11 (M4 V 4745 kb)

Supplementary material 12 (M4 V 1089 kb)

Supplementary material 13 (M4 V 2849 kb)

Supplementary material 14 (M4 V 2229 kb)

Supplementary material 1 (TXT 28 kb)

Supplementary material 2 (TXT 1 kb)

Supplementary material 3 (TXT 1 kb)

Supplementary material 4 (R 6 kb)

Supplementary material 5 (TXT 92 kb)

Supplementary material 6 (TXT 32 kb)

Supplementary material 7 (TXT 20 kb)

Supplementary material 8 (DOCX 650 kb)

Supplementary material 15 (JPEG 4726 kb)

Supplementary material 16 (JPEG 7171 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bordoni, A., Mocilnik, G., Forni, G. et al. Two aggressive neighbours living peacefully: the nesting association between a stingless bee and the bullet ant. Insect. Soc. 67, 103–112 (2020). https://doi.org/10.1007/s00040-019-00733-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-019-00733-9

Keywords

  • Paraponera clavata
  • Partamona testacea
  • COI
  • GC/MS
  • Recognition
  • Nesting association