Skip to main content
Log in

Looking beyond the flowers: associations of stingless bees with sap-sucking insects

  • Original Paper
  • Published:
The Science of Nature Aims and scope Submit manuscript

Abstract

The main sources of food for stingless bees are the nectar and pollen harvested from flowers, whereas one important kind of nesting material (i.e. wax) is produced by their own abdominal glands. Stingless bees can, nonetheless, obtain alternative resources of food and wax from exudates released by sap-sucking insects as honeydew and waxy cover, respectively. To date, there are no comprehensive studies investigating how diversified and structured the network interactions between stingless bees and sap-sucking insects are. Here, we conducted a survey of the data on relationship between stingless bees and sap-sucking insects to evaluate: (1) which resources are collected by which stingless bee species; (2) how diverse the interaction network is, using species degree and specialisation index as a proxy; and if (3) there would be any phylogenetic signal in the species degree and specialisation indices. Our findings demonstrate that approximately 21 stingless bee species like Trigona spp. and Oxytrigona spp. have been observed interacting with 11 sap-sucking species, among which Aethalion reticulatum is the main partner. From ca. 50 records, Brazil is the country with most observations (n = 38) of this type of ecological interaction. We found also that stingless bees harvest fivefold more honeydew than waxy covers on sap-sucking insects. However, we did not find any phylogenetic signal for the occurrence of this interaction, considering species degree and specialisation indices, suggesting that both traits apparently evolved independently among stingless bee species. We suggest that specific ecological demands may drive this opportunistic behaviour exhibited by stingless bees, because major sources of food are obtained from flowers and these bees produce their own wax.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abouheif E (1999) A method for testing the assumption of phylogenetic independence in comparative data. Evol Ecol Res 1:895–909

    Google Scholar 

  • Adams DC, Collyer ML (2018) Multivariate phylogenetic comparative methods: evaluations, comparisons, and recommendations. Syst Biol 67:14–31. https://doi.org/10.1093/sysbio/syx055

    Article  PubMed  Google Scholar 

  • Aidar IF, Bartelli BF, Nogueira-Ferreira FH (2015) Network of bee-plant interactions and recognition of key species in semideciduous forest. Sociobiology 62:583–592. https://doi.org/10.13102/sociobiology.v62i4.610

    Article  Google Scholar 

  • Almeida-Neto M, Izzo TJ, Raimundo RLG, Rossa-Feres DC (2003) Reciprocal interference between ants and stingless bees attending the honeydew-producing homopteran Aetalion reticulatum (Homoptera: Aetalionidae). Sociobiology 42:369–380

    Google Scholar 

  • Auclair JL (1963) Aphid feeding and nutrition. Annu Rev Entomol 8:439–490. https://doi.org/10.1146/annurev.en.08.010163.002255

    Article  Google Scholar 

  • Azevedo RL, Carvalho CAL, Marques OM (2008) Insetos associados à cultura do feijão Guandu na região do recôncavo da Bahia, Brasil. Caatinga 21:83–88

    Google Scholar 

  • Barônio GJ, Pires ACV, Aoki C (2012) Trigona branneri (Hymenoptera: Apidae) as a collector of honeydew from Aethalion reticulatum (Hemiptera: Aethalionidae) on Bauhinia forficata (Fabaceae: Caesalpinoideae) in a Brazilian savanna. Sociobiology 59:407–414

    Article  Google Scholar 

  • Barrows EM (1979) Polistes wasps (Hymenoptera, Vespidae) show interference competition with other insects for Kermes scale insect (Homoptera, Kermesidae) secretions. Proc Entomol Soc Washingt 81:570–575

  • Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312(80):431–434

    Article  CAS  PubMed  Google Scholar 

  • Batra SWT (1993) Opportunistic bumble bees congregate to feed at rare, distant alpine honeydew bonanzas. J Kansas Entomol Soc 66:125–127

    Google Scholar 

  • Bian Z, Fales HM, Blum MS, Jones TH, Rinderer TE, Howard DF (1984) Chemistry of cephalic secretion of fire bee Trigona (Oxytrigona) tataira. J Chem Ecol 10:451–461. https://doi.org/10.1007/BF00988091

    Article  CAS  PubMed  Google Scholar 

  • Bishop JA (1994) Bumble bees (Bombus hypnorum) collect aphid honeydew on stone pine (Pinus pumila) in the Russian Far East. J Kansas Entomol Soc 67:220–222

    Google Scholar 

  • Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9. https://doi.org/10.1186/1472-6785-6-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Bourgoin T, Campbell BC (2002) Inferring a phylogeny for Hemiptera: falling into the ‘autapomorphic trap’. Denisia 4:67–82

    Google Scholar 

  • Brown RL (1976) Behavioral observations on Aethalion reticulatum (Hem. Aethalionidae) and associated ants. Insect Soc 23:99–108

    Article  Google Scholar 

  • Buckley R, Gullan PJ (1991) More aggressive ant species (Hymenoptera: Formicidae) provide better protection for soft scales and mealybugs (Homoptera: Coccidae, Pseudococcidae). Biotropica 23:282–286. https://doi.org/10.2307/2388205

    Article  Google Scholar 

  • Camargo JMF, Pedro SRM (2002) Mutualistic association between a tiny Amazonian stingless bee and a wax-producing scale insect. Biotropica 34:446–451. https://doi.org/10.1111/j.1744-7429.2002.tb00559.x

    Article  Google Scholar 

  • Camargo JMF, Pedro SRM (2013) Meliponini Lepeletier, 1836. In: Moure JS, Urban D, Melo, GAR (eds) Catalogue of bees (Hymenoptera, Apoidea) in the neotropical region—online version

  • Cardinal S, Danforth B (2013) Bees diversified in the age of eudicots. Proc R Soc B biol Sci 280:20122686. https://doi.org/10.1098/rspb.2012.2686

    Article  Google Scholar 

  • Chamorro FJ, Nates-Parra G, Kondo T (2013) Mielato de Stigmacoccus asper (Hemiptera: Stigmacoccidae): recurso melifero de bosques de roble en Colombia. Rev Colomb Entomol 39:61–70

    Google Scholar 

  • Corke D (1999) Are honeydew/sap-feeding butterflies (Lepidoptera: Rhopalocera) affected by particulate air-pollution? J Insect Conserv 3:5–14. https://doi.org/10.1023/a:1009670404398

    Article  Google Scholar 

  • Cortopassi-Laurino M (1977) Notas sobre associações de Trigona (Oxytrigona) tataira (Apidae, Meliponinae). Bol Zool da Univ São Paulo 2:183–187

    Google Scholar 

  • Cruz-Landim C (1967) Estudo comparativo de algumas glândulas das abelhas (Hymenoptera, Apoidea) e respectivas implicações evolutivas. Arq Zool 15:177–290

    Article  Google Scholar 

  • Delabie JHC (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotrop Entomol 30:501–516. https://doi.org/10.1590/S1519-566X2001000400001

    Article  Google Scholar 

  • Dimou M, Thrasyvoulou A (2007) Collection of wax scale (Ceroplastes sp.) by the honey bee Apis mellifera. J Apic Res 46:129. https://doi.org/10.1080/00218839.2007.11101381

    Article  Google Scholar 

  • Dormann CF, Fruend J, Bluethgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24

    Article  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Figueiredo RA (1996) Interactions between stingless meliponine bees, honeydew-producing homopterans, ants and figs in a cerrado area. Naturalia 21:159–164

    Google Scholar 

  • Giannini TC, Garibaldi LA, Acosta AL, Silva JS, Maia KP, Saraiva AM, Guimarães PR, Kleinert AMP (2015) Native and non-native supergeneralist bee species have different effects on plant-bee networks. PLoS One 10:e0137198. https://doi.org/10.1371/journal.pone.0137198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • González AMM, Dalsgaard B, Olesen JM (2010) Centrality measures and the importance of generalist species in pollination networks. Ecol Complex 7:36–43. https://doi.org/10.1016/j.ecocom.2009.03.008

    Article  Google Scholar 

  • Hamity MGA, Román LEN, Zamar MI (2003) Aspectos bioecológicos de Aethalion reticulatum Linnaeus, 1767 (Hemiptera: Aethalionidae) especie perjudicial en árboles y arbustos de la Prepuna jujeña. Jujuy-Argentina IDESIA 21:31–39

    Google Scholar 

  • Herrmann M, Burger F, Muller A, Tischendorf S (2003) Distribution, habitat, and biology of the sweat bee Lasioglossum pallens (Brullé 1832) and its cuckoo bee Sphecodes majalis Pérez 1903 in Germany (Hymenoptera, Apidae, Halictinae). Carolinae 61:133–144

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314

    Google Scholar 

  • Inkscape (2017) Inkscape. version 0.92. Available at http://www.inkscape.org/. Accessed 23 April 2018

  • Jordano P, Bascompte J, Olesen JM (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecol Lett 6:69–81. https://doi.org/10.1046/j.1461-0248.2003.00403.x

    Article  Google Scholar 

  • Koch H, Corcoran C, Jonker M (2011) Honeydew collecting in Malagasy stingless bees (Hymenoptera: Apidae: Meliponini) and observations on competition with invasive ants. African Entomol 19:36–41. https://doi.org/10.4001/003.019.0111

    Article  Google Scholar 

  • Kondo T (2010) Taxonomic revision of the myrmecophilous, meliponiphilous and rhizophilous soft scale genus Cryptostigma Ferris (Hemiptera: Coccoidea: Coccidae)

  • Konrad R, Wackers FL, Babendreier D (2009) Honeydew feeding in the solitary bee Osmia bicornis as affected by aphid species and nectar availability. J Insect Physiol 55:1158–1166. https://doi.org/10.1016/j.jinsphys.2009.08.012

    Article  CAS  PubMed  Google Scholar 

  • Letouneau DK, Choe JC (1987) Homopteran attendance by wasps and ants: the stochastic nature of interactions. Psyche (Stuttg) 94:81–92

    Article  Google Scholar 

  • Lunau K (2004) Adaptive radiation and coevolution—pollination biology case studies. Org Divers Evol 4:207–224. https://doi.org/10.1016/j.ode.2004.02.002

    Article  Google Scholar 

  • Maschwitz U, Hanel H (1985) The migrating herdsman Dolichoderus (Diabolus) cuspidatus: an ant with a novel mode of life. Behav Ecol Sociobiol 17:171–184

    Google Scholar 

  • Mitchell RJ, Irwin RE, Flanagan RJ, Karron JD (2009) Ecology and evolution of plant-pollinator interactions. Ann Bot 103:1355–1363. https://doi.org/10.1093/aob/mcp122

    Article  PubMed  PubMed Central  Google Scholar 

  • Naskrecki P, Nishida K (2007) Novel trophobiotic interactions in lantern bugs (Insecta: Auchenorrhyncha: Fulgoridae). J Nat Hist 41:2397–2402. https://doi.org/10.1080/00222930701633570

    Article  Google Scholar 

  • Novgorodova TA (2015) Organization of honeydew collection by foragers of different species of ants (Hymenoptera: Formicidae): effect of colony size and species specificity. Eur J Entomol 112:688–697. https://doi.org/10.14411/eje.2015.077

    Article  Google Scholar 

  • Oda FH, Aoki C, Oda TM, da Silva RA, Felismino MF (2009) Interação entre abelha Trigona hyalinata (Lepeletier, 1836) (Hymenoptera: Apidae) e Aethalion reticulatum Linnaeus, 1767 (Hemiptera: Aethalionidae) em Clitoria fairchildiana Howard (Papilionoideae). EntomoBrasilis 2:58–60

    Article  Google Scholar 

  • Oda FH, Oliveira AF, Aoki C (2014) Oxytrigona tataira (Smith) (Hymenoptera: Apidae: Meliponini) as a collector of honeydew from Erechtia carinata (Funkhouser) (Hemiptera: Membracidae) on Caryocar brasiliense Cambessèdes (Malpighiales: Caryocaraceae) in the Brazilian Savanna. Sociobiology 61:566–569. https://doi.org/10.13102/sociobiology.v61i4.566-569

    Article  Google Scholar 

  • Olesen JM, Jordano P (2002) Geographic patterns in plant—pollinator mutualistic networks. Ecology 83:2416–2424

    Google Scholar 

  • Pagel M (1994) Detecting correlated evolution on phylogenies: a general method for the com parative analysis of discrete characters. Proc R Soc B Biol Sci 255:37–45

    Article  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Peronti ALBG, Fernandes LBR, Fernandes MA (2013) A facultative association between Plebeia droryana (Friese, 1900) (Hymenoptera: Apidae: Meliponini) and a wax scale insect, Ceroplastes janeirensis (Hemiptera: Coccoidea: Coccidae). Brazilian J Biol 73:453–454

    Article  CAS  Google Scholar 

  • Poinar GO, Danforth BN (2006) A fossil bee from Early Cretaceous Burmese amber. Science 314:2006. https://doi.org/10.1126/science.1134103

    Article  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. The R foundation for statistical computing, Vienna, Austria. Available at https://cran.r-project.org/

  • Rasmussen C, Cameron SA (2010) Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biol J Linn Soc 99:206–232. https://doi.org/10.1111/j.1095-8312.2009.01341.x

    Article  Google Scholar 

  • Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x

    Article  Google Scholar 

  • Rezende EL, Jordano P, Bascompte J (2007) Effects of phenotypic complementarity and phylogeny on the nested structure of mutualistic networks. Oikos 116:1919–1929

    Article  Google Scholar 

  • Rohlfs R, Nielsen R (2015) Phylogenetic ANOVA: the expression variance and evolution model for quantitative trait evolution. Syst Biol 64:695–708. https://doi.org/10.1093/sysbio/syv042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roubik DW (2006) Stingless bee nesting biology. Apidologie 37:124–143. https://doi.org/10.1051/apido

    Article  Google Scholar 

  • Roubik DW, Smith BH, Carlson RG (1987) Formic acid in caustic cephalic secretions of stingless bee, Oxytrigona (Hymenoptera: Apidae). J Chem Ecol 13:1079–1085. https://doi.org/10.1007/BF01020539

    Article  CAS  PubMed  Google Scholar 

  • Sansum P (2013) Honeydew feeding in adult Noctuidae and Erebidae—some observations and a note on differing modes of access. J Res Lepid 46:75–80

    Google Scholar 

  • Santas LA (1983) Insects producing honeydew exploited by bees in Greece. Apidologie 14:93–103. https://doi.org/10.1051/apido:19830204

    Article  Google Scholar 

  • Schorkopf DLP, Hrncir M, Mateus S, Zucchi R, Schmidt VM, Barth FG (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

    Article  CAS  PubMed  Google Scholar 

  • Schuster JC (1981) Stingless bees attending honeydew-producing treehoppers in Guatemala. Florida Entomol 64:192

    Article  Google Scholar 

  • Schwarz HF (1948) Stingless bees (Meliponidae) of the Western Hemisphere: Lestrimelitta and the following subgenera of Trigona: Trigona, Paratrigona, Schwarziana, Parapartamona, Cephalotrigona, Oxytrigona, Scaura, and Mourella. Bull Am Museum Nat Hist 90:1–546

    Google Scholar 

  • Shackleton K, Al Toufailia H, Balfour NJ et al (2015) Appetite for self-destruction: suicidal biting as a nest defense strategy in Trigona stingless bees. Behav Ecol Sociobiol 69:273–281. https://doi.org/10.1007/s00265-014-1840-6

    Article  PubMed  Google Scholar 

  • Simova S, Atanassov A, Shishiniova M, Bankova V (2012) A rapid differentiation between oak honeydew honey and nectar and other honeydew honeys by NMR spectroscopy. Food Chem 134:1706–1710. https://doi.org/10.1016/j.foodchem.2012.03.071

    Article  CAS  PubMed  Google Scholar 

  • Slaa EJ, Wassenberg J, Biesmeijer JC (2003) The use of field-based social information in eusocial foragers: local enhancement among nestmates and heterospecifics in stingless bees. Ecol Entomol 28:369–379. https://doi.org/10.1046/j.1365-2311.2003.00512.x

    Article  Google Scholar 

  • Stang M, Klinkhamer PGL, Waser NM, Stang I, van der Meijden E (2009) Size-specific interaction patterns and size matching in a plant-pollinator interaction web. Ann Bot 103:1459–1469. https://doi.org/10.1093/aob/mcp027

    Article  PubMed  PubMed Central  Google Scholar 

  • Vieira CU, Rodovalho CM, Almeida LO et al (2007) Interação entre Trigona spinipes Fabricius, 1793 (Hymenoptera: Apidae) e Aethalion reticulatum Linnaeus, 1767 (Hemiptera: Aethalionidae) em Mangifera indica (Anacardiaceae). Biosci J 23:10–13

    Google Scholar 

  • Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344

    Article  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York

    Book  Google Scholar 

  • Wolff VRS, Witter S, Lisboa BB (2015) Reporte de Stigmacoccus paranaensis Foldi (Hemiptera, Stigmacoccidae), insecto escama asociado con la producción de miel de mielato en Rio Grande do Sul, Brasil. Insecta mundi 434:1–7

    Google Scholar 

Download references

Acknowledgements

The authors are grateful to Gervásio Silva Carvalho and Kedar Devkota for critically reading and providing comments on the manuscript. We would also like to thank Camila Aoki for providing us picture of hemipteran with stingless bee. CFS would like to thank the National Postdoctoral Program (PNPD) of the Coordination for the Improvement of Higher Education Personnel (CAPES). P.D.S.S is grateful to CNPq for the provision of scholarships. R.H. is thankful to CAPES [13190066-4] for awarding scholarships.

Funding

BB is supported by the National Council for Scientific and Technological Development (CNPq) for the research grant. E.A.B.A. is grateful to the São Paulo Research Foundation—FAPESP (2011/09477-9) and to CNPq (459826/2014-0, 304735/2016-7).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charles Fernando dos Santos.

Additional information

Communicated by: Rumyana Jeleva

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(XLS 43 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

dos Santos, C.F., Halinski, R., de Souza dos Santos, P.D. et al. Looking beyond the flowers: associations of stingless bees with sap-sucking insects. Sci Nat 106, 12 (2019). https://doi.org/10.1007/s00114-019-1608-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00114-019-1608-y

Keywords

Navigation