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Interactions between two species of recently-sympatric invasive honeybees: Apis cerana induces aggression in Apis mellifera during foraging

Abstract

Honeybees Apis mellifera (European honeybee) and Apis cerana (Asian honeybee) are cosmopolitan, having colonized continents beyond their natural ranges. In tropical Australia, these alien species have recently become sympatric. The environmental and economic impacts of these species when in sympatry remain to be seen; however, any interspecific competition may be of significance. We examined conspecific and heterospecific interactions between honeybees foraging at the nectar- and pollen-providing flowers of Antipogon leptopus (Polygonaceae). We cross-classified 554 encounters by three variables; incoming bee species, resident bee species, and one of four potential responses: (1) incoming defers to resident; (2) incoming procures the flower from resident; (3) incoming and resident share the flower; or (4) both incoming and resident abandon the flower. We also measured aggression and foraging rates of workers at flowers. Both species visited similar numbers of flowers in a foraging bout and spent similar foraging times on individual flowers. Incoming A. mellifera were more likely to procure flowers from resident A. cerana, and incoming A. cerana were more likely to defer to resident A. mellifera. A. mellifera were more aggressive toward heterospecifics than conspecifics, with heterospecifics 4.5 times more likely to provoke an aggressive response. However, no significant difference between conspecific and heterospecific aggression was observed for incoming A. cerana. A. mellifera were less abundant, yet overall more likely to acquire flowers and use aggression to do so. Costs of aggression may help explain the population-scale dominance of A. cerana over A. mellifera in this study.

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Data availability

The data that support the findings of this study are stored by and available from the University of New England and provided as open access, under a CC-BY 4.0 license. Data can be accessed from TBA (https://hdl.handle.net/1959.11/27494).

References

  1. Abrol D (2003) Antigonon leptopus. Bee World 84:86–87

    Article  Google Scholar 

  2. Amarasekare P (2002) Interference competition and species coexistence. Proc R Soc Lond B Biol Sci 269(1509):2541–2550

    Article  Google Scholar 

  3. Anderson D, Annand N (2012) Control of Asian honey bees in Solomon Islands. ACIAR, Canberra

    Google Scholar 

  4. Anderson D, Annand N, Lacey M, Ete S (2012) Control of Asian honeybees in the Solomon Islands—final report. Australian Government, Australian Centre for International Agricultural Research, Canberra

    Google Scholar 

  5. Bailey F (1982) Beekeeping in Australia: for pleasure and profit. William Heinemann, Richmond

    Google Scholar 

  6. Barry S, Cook D, Duthie R, Clifford D, Anderson D (2010) Future surveillance needs for honeybee biosecurity. Rural Industries Research and Development Corporation 10:107, Barton

    Google Scholar 

  7. Beismeijer JC, Richter JA, Smeets MAJP, Sommeijer MJ (1999) Niche differentiation in nectar-collecting stingless bees: the influence of morphology, floral choice and interference competition. Ecol Entomol 24:380–388

    Article  Google Scholar 

  8. Briffa M, Sneddon LU (2007) Physiological constraints on contest behaviour. Funct Ecol 21:627–637

    Article  Google Scholar 

  9. Cairns CE, Villanueva-Gutiérrez R, Koptur S, Bray DB (2005) Bee populations, forest disturbance, and africanization in Mexico. Biotropica 37:686–692

    Article  Google Scholar 

  10. Carr A (2011) Asian honeybee: possible environmental impacts. Report for the Department of Sustainability, Environment, Water, Population and Communities. Sustineo Pty Ltd., Canberra

  11. Chifamba PC, Mauru T (2017) Comparative aggression and dominance of Oreochromis niloticus (Linnaeus, 1758) and Oreochromis mortimeri (Trewavas, 1966) from paired contest in aquaria. Hydrobiologia 788:193–203

    Article  CAS  Google Scholar 

  12. Crane EE (2013) The world history of beekeeping and honey hunting. Routledge, New York

    Book  Google Scholar 

  13. Crowl TA, Crist TO, Parmenter RR et al (2008) The spread of invasive species and infectious disease as drivers of ecosystem change. Front Ecol Environ 6:238–246

    Article  Google Scholar 

  14. Dworschak K, Bluethgen N (2010) Networks and dominance hierarchies: does interspecific aggression explain flower partitioning among stingless bees? Ecol Entomol 35:216–225

    Article  Google Scholar 

  15. Gordon J, Davis L (2003) Valuing honeybee pollination. The Centre for International Economics. Report prepared for Rural Industries Research and Development Corporation, Project No. CIE-15A, Publication No. 03/077

  16. Gross C (1996) Is resource overlap disadvantageous to three sympatric legumes? Aust J Ecol 21:133–143

    Article  Google Scholar 

  17. Gross CL (2015) The buzz about Asian honey bees. Wildl Aust 52:42–44

    Google Scholar 

  18. Gross CL, Mackay D (1998) Honeybees reduce fitness in the pioneer shrub Melastoma affine (Melastomataceae). Biol Conserv 86:169–178

    Article  Google Scholar 

  19. Gross CL, Gorrell L, Macdonald MJ, Fatemi M (2010) Honeybees facilitate the invasion of Phyla canescens (Verbenaceae) in Australia—no bees, no seed! Weed Res 50:364–372

    Google Scholar 

  20. Grumbine RE (1994) What is ecosystem management? Conserv Biol 8:27–38

    Article  Google Scholar 

  21. Hingston AB, McQuillan PB (1999) Displacement of Tasmanian native megachilid bees by the recently introduced bumblebee Bombus terrestris (Linnaeus, 1758) (Hymenoptera: Apidae). Aust J Zool 47:59–65

    Article  Google Scholar 

  22. Houston AI, McNamara JM (1988) Fighting for food: a dynamic version of the Hawk–Dove game. Evol Ecol 2:51–64

    Article  Google Scholar 

  23. Hu L, Wu X (2019) The difference in pollen harvest between Apis mellifera and Apis cerana in a Tibetan alpine meadow. J Mt Sci 16:1598–1605

    Article  Google Scholar 

  24. Hubbell SP, Johnson LK (1978) Comparative foraging behavior of six stingless bee species exploiting a standardized resource. Ecology 59:1123–1136

    Article  Google Scholar 

  25. Jean RP (2005) Quantifying a rare event: pollen theft by honey bees from bumble bees and other bees (Apoidea: Apidae, Megachilidae) foraging at flowers. J Kansas Entomol Soc 78:172–175

    Article  Google Scholar 

  26. Johnson LK, Hubbell SP (1975) Contrasting foraging strategies and coexistence of two bee species on a single resource. Ecology 56:1398–1406

    Article  Google Scholar 

  27. Koetz AH (2013) Ecology, behaviour and control of Apis cerana with a focus on relevance to the Australian incursion. Insects 4:558–592

    Article  PubMed  PubMed Central  Google Scholar 

  28. Lichtenberg E, Imperatriz-Fonseca V, Nieh J (2010) Behavioral suites mediate group-level foraging dynamics in communities of tropical stingless bees. Insectes Soc 57:105–113

    Article  CAS  Google Scholar 

  29. Manila-Fajardo A, Cervancia C (2003) Performance of honey bees (Apis mellifera L.) in three ecosystems in Laguna, Philippines. Philipp Agric Sci 86:146–157

    Google Scholar 

  30. McCormick MI, Weaver CJ (2012) It pays to be pushy: intracohort interference competition between two reef fishes. PLoS ONE 7:e42590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Nagamitsu T, Inoue T (1997) Aggressive foraging of social bees as a mechanism of floral resource partitioning in an Asian tropical rainforest. Oecologia 110:432–439

    Article  Google Scholar 

  32. Oldroyd BP, Wongsiri S (2009) Asian honey bees: biology, conservation, and human interactions. Harvard University Press, Cambridge

    Google Scholar 

  33. Oldroyd B, Rinderer T, Wongsiri S (1992) Pollen resource partitioning by Apis dorsata, A. cerana, A. andreniformis and A. florea in Thailand. J Apic Res 31:3–7

    Article  Google Scholar 

  34. Oliveira DJ, de Carvalho CAL, Sodré GS, Paixão JF, Alves RM (2017) Partitioning of pollen resources by two stingless bee species in the north Bahia, Brazil. Grana 56:285–293

    Article  Google Scholar 

  35. Padil (2019). http://www.padil.gov.au/pests-and-diseases/search?queryText1=Apis+cerana&queryType1=all. Accessed 29 May 2019

  36. Paini DR, Roberts JD (2005) Commercial honey bees (Apis mellifera) reduce the fecundity of an Australian native bee (Hylaeus alcyoneus). Biol Conserv 123:103–112

    Article  Google Scholar 

  37. Paton DC (1993) Honeybees in the Australian environment. Bioscience 43:95–103

    Article  Google Scholar 

  38. Persson L (1985) Asymmetrical competition: are larger animals competitively superior? Am Nat 126:261–266

    Article  Google Scholar 

  39. Pintar MR, Bohenek JR, Eveland LL, Resetarits WJ (2018) Colonization across gradients of risk and reward: nutrients and predators generate species-specific responses among aquatic insects. Funct Ecol 32:1589–1598

    Article  Google Scholar 

  40. QldGov (2017) Asian honey bee. https://www.business.qld.gov.au/industries/farms-fishing-forestry/agriculture/land-management/health-pests-weeds-diseases/pests/invasive-animals/restricted/asian-honey-bees. Accessed 16 Feb 2017

  41. Raju AJS, Raju VK, Victor P, Naidu SA (2001) Floral ecology, breeding system and pollination in Antigonon leptopus L. (Polygonaceae). Plant Species Biol 16:159–164

    Article  Google Scholar 

  42. RCoreTeam (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org. Accessed 25 June 2015

  43. Roubik DW (1978) Competitive interactions between neotropical pollinators and Africanized honey bees. Science 201:1030–1032

    Article  CAS  Google Scholar 

  44. Sakagami SF (1959) Some interspecific relations between Japanese and European honeybees. J Anim Ecol 28:51–68

    Article  Google Scholar 

  45. Santos CFd, Absy ML (2012) Interactions between carpenter bees and orchid bees (Hymenoptera: Apidae) in flowers of Bertholletia excelsa Bonpl. (Lecythidaceae). Acta Amazonica 42:89–94

    Article  Google Scholar 

  46. Smith JM, Parker GA (1976) The logic of asymmetric contests. Anim Behav 24:159–175

    Article  Google Scholar 

  47. Sneddon LU, Taylor AC, Huntingford FA (1999) Metabolic consequences of agonistic behaviour: crab fights in declining oxygen tensions. Anim Behav 57:353–363

    Article  CAS  Google Scholar 

  48. Suryanarayana MC, Mohana Rao G, Singh TSMS (1992) Studies on pollen sources for Apis cerana Fabr and Apis mellifera L. bees at Muzaffarpur, Bihar, India. Apidologie 23:33–46

    Article  Google Scholar 

  49. Tan K, Yang S, Wang Z-W, Radloff SE, Oldroyd BP (2012) Differences in foraging and broodnest temperature in the honey bees Apis cerana and A. mellifera. Apidologie 43:618–623

    Article  Google Scholar 

  50. Thomson D (2004) Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85:458–470

    Article  Google Scholar 

  51. Thorp RW, Briggs DL (1980) Bees collecting pollen from other bees (Hymenoptera: Apoidea). J Kansas Entomol Soc 53:166–170

    Google Scholar 

  52. Wittig RM, Crockford C, Weltring A, Deschner T, Zuberbühler K (2015) Single aggressive interactions increase urinary glucocorticoid levels in wild male chimpanzees. PLoS ONE 10:e0118695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Wolf LL (1978) Aggressive social organization in nectarivorous birds. Am Zool 18:765–778

    Article  Google Scholar 

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Acknowledgements

This work was funded by a Price Bequest grant to CG, NRA and DP. We thank G. Trembath of Gordonvale for access to her garden.

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Correspondence to C. L. Gross.

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Gross, C.L., Whitehead, J.D., Mackay, E.S.G. et al. Interactions between two species of recently-sympatric invasive honeybees: Apis cerana induces aggression in Apis mellifera during foraging. Biol Invasions 21, 3697–3706 (2019). https://doi.org/10.1007/s10530-019-02081-y

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Keywords

  • Aggression
  • Competition
  • Honeybee
  • Invasive species
  • Resource use