, Volume 183, Issue 4, pp 1111–1120 | Cite as

Asymmetric competition for nectar between a large nectar thief and a small pollinator: an energetic point of view

  • Eliška PadyšákováEmail author
  • Jan Okrouhlík
  • Mark Brown
  • Michael Bartoš
  • Štěpán Janeček
Plant-microbe-animal interactions - original research


There are two alternative hypotheses related to body size and competition for restricted food sources. The first one supposes that larger animals are superior competitors because of their increased feeding abilities, whereas the second one assumes superiority of smaller animals because of their lower food requirements. We examined the relationship between two unrelated species of different size, drinking technique, energy requirements and roles in plant pollination system, to reveal the features of their competitive interaction and mechanisms enabling their co-existence while utilising the same nectar source. We observed diurnal feeding behaviour of the main pollinator, the carpenter bee Xylocopa caffra and a nectar thief, the northern double-collared sunbird Cinnyris reichenowi on 19 clumps of Hypoestes aristata (Acanthaceae) in Bamenda Highlands, Cameroon. For comparative purpose, we established a simplistic model of daily energy expenditure and daily energy intake by both visitor species assuming that they spend all available daytime feeding on H. aristata. We revealed the energetic gain–expenditure balance of the studied visitor species in relation to diurnal changes in nectar quality and quantity. In general, smaller energy requirements and related ability to utilise smaller resources made the main pollinator X. caffra competitively superior to the larger nectar thief C. reichenowi. Nevertheless, sunbirds are endowed with several mechanisms to reduce asymmetry in exploitative competition, such as the use of nectar resources in times of the day when rivals are inactive, aggressive attacks on carpenter bees while defending the nectar plants, and higher speed of nectar consumption.


Africa Carpenter bee Cinnyris Hypoestes Sunbird Xylocopa 



We thank to Ernest Vunan Amohlon for his help and kind reception in Big Babanki village, and to Benjamin Vubangsi, the local chief of Kedjom-Keku community, for providing us the permission and access to study area. This work was supported by the projects of Czech Science Foundation 16-11164Y, Grant Agency of the University of South Bohemia 136/2010/P and 156/2013/P, institutional support RVO:60077344 and the long-term research development Project No. 67985939. EP acknowledges Fellowship Reg. No. L200961552 from the Programme of Support of Promising Human Resources, awarded by The Czech Academy of Sciences.

Author contribution statement

EP, ŠJ, MB conceived and designed the experiments, and conducted fieldworks. ŠJ performed statistical analysis. JO developed the mathematical models. MB collaborated in making models and analysis. EP, ŠJ, JO wrote the manuscript; other authors provided editorial advice.

Supplementary material

442_2017_3817_MOESM1_ESM.docx (542 kb)
Supplementary material 1 (DOCX 542 kb)


  1. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: Guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  2. Armstrong DP, Perrott JK (2000) An experiment testing whether condition and survival are limited by food supply in a reintroduced Hihi population. Conserv Biol 14(4):1171–1181CrossRefGoogle Scholar
  3. Baker HG (1975) Sugar concentrations in nectars from hummingbird flowers. Biotropica 74:37–41CrossRefGoogle Scholar
  4. Balkwill K, Norris FG (1985) Taxonomic studies in the Acanthaceae—the genus Hypoestes in southern Africa. S Afr J Bot 51:133–144CrossRefGoogle Scholar
  5. Ballance LT, Pitman RL, Reilly SB (1997) Seabird community structure along a productivity gradient: importance of competition and energetic constraint. Ecology 78:1502–1518. doi:10.1890/0012-9658(1997)078[1502:scsaap];2Google Scholar
  6. Barnes DKA (2003) Competition asymmetry with taxon divergence. Proc R Soc B Biol Sci 270:557–562. doi: 10.1098/rspb.2002.2274 CrossRefGoogle Scholar
  7. Barrows EM (1976) Nectar robbing and pollination of Lantana camara (Verbenaceae). Biotropica 8:132–135CrossRefGoogle Scholar
  8. Bartoš M et al (2012) Nectar properties of the sunbird-pollinated plant Impatiens sakeriana: a comparison with six other co-flowering species. S Afr J Bot 78:63–74CrossRefGoogle Scholar
  9. Bartoš M et al (2015) Specialization of pollination systems of two co-flowering phenotypically generalized Hypericum species (Hypericaceae) in Cameroon. Arthropod-Plant Interact 9:241–252CrossRefGoogle Scholar
  10. Bednekoff PA, Houston AI (1994) Avian daily foraging patterns: effects of digestive constraints and variability. Evol Ecol 8:36–52CrossRefGoogle Scholar
  11. Borrow N, Demey R (2001) Birds of western Africa. Christopher Helm Publishers, LondonGoogle Scholar
  12. Boyden TC (1978) Territorial defense against hummingbirds and insects by tropical hummingbirds. Condor 80:216–221CrossRefGoogle Scholar
  13. Brown JH, Kodric-Brown A, Whitman TG, Bond HW (1981) Competition between hummingbirds and insects for the nectar of two species of shrubs. Southwest Nat 26:133–145CrossRefGoogle Scholar
  14. Brown M, Downs CT, Johnson SD (2009) Pollination of the red hot poker Kniphofia caulescens by short-billed opportunistic avian nectarivores. S Afr J Bot 75:707–712. doi: 10.1016/j.sajb.2009.07.015 CrossRefGoogle Scholar
  15. Bystrom P, Garcia-Berthou E (1999) Density dependent growth and size specific competitive interactions in young fish. Oikos 86:217–232. doi: 10.2307/3546440 CrossRefGoogle Scholar
  16. Cheek M, Onana JM, Pollard JB (2000) The plants of Mount Oku and the Ijim Ridge, Cameroon. A conservation Checklist. Royal Botanic Gardens, KewGoogle Scholar
  17. Clutton-Brock TH, Albon SD, Gibson RM, Guiness FE (1979) The logical stag: aspects of fighting in red deer (Cervus elaphus L.). Anim Behav 27:211–275CrossRefGoogle Scholar
  18. Colwell RK (1973) Competition and coexistence in a simple tropical community. Am Nat 107:737–760CrossRefGoogle Scholar
  19. Eardley CD (1983) A taxonomic revision of the genus Xylocopa Latreille (Hymenoptera: Anthophoridae) in southern Africa. Entomology Entomology Memoir, Department of Agriculture of Republic of South Africa, PretoriaGoogle Scholar
  20. Ferriere R, Gauduchon M, Bronstein JL (2007) Evolution and persistence of obligate mutualists and exploiters: competition for partners and evolutionary immunization. Ecol Lett 10:115–126. doi: 10.1111/j.1461-0248.2006.01008.x CrossRefPubMedGoogle Scholar
  21. Ford HA (1979) Interspecific competition in Australian honeyeaters—depletion of common resources. Aust J Ecol 4:145–164CrossRefGoogle Scholar
  22. Ford HA (1981) Territorial behaviour in an Australian nectar-feeding bird. Aust J Ecol 6:131–134CrossRefGoogle Scholar
  23. Ford HA, Paton DC (1976) Resource partitioning and competition in honeyeaters of the genus Meliphaga. Aust J Ecol 1:281–287CrossRefGoogle Scholar
  24. Ford HA, Paton DC (1982) Partitioning of nectar sources in an Australian honeyeater community. Aust J Ecol 7:149–159CrossRefGoogle Scholar
  25. Galen C, Geib JC (2007) Density-dependent effects of ants on selection for bumble bee pollination in Polemonium viscosum. Ecology 88:1202–1209. doi: 10.1890/06-1455 CrossRefPubMedGoogle Scholar
  26. Galetto L, Bernardello G (2005) Nectar energetics. In: Dafni A, Kevan PG, Husband BC (eds) Practical pollination biology. Enviroquest Ltd, Cambridge, pp 312–313Google Scholar
  27. Garrison JSE, Gass CL (1999) Response of a traplining hummingbird to changes in nectar availability. Behav Ecol 10:714–725CrossRefGoogle Scholar
  28. Gill FB (1988) Trapline foraging by hermit hummingbirds—competition for an undefended, renewable resource. Ecology 69:1933–1942. doi: 10.2307/1941170 CrossRefGoogle Scholar
  29. Gill FB, Wolf LL (1975) Economics of feeding territoriality in the golden-winged sunbird. Ecology 56:333–345CrossRefGoogle Scholar
  30. Hambly C, Pinshow B, Wiersma P, Verhulst S, Piertney SB, Harper EJ, Speakman JR (2004) Comparison of the cost of short flights in a nectarivorous and a non-nectarivorous bird. J Exp Biol 207:3959–3968CrossRefPubMedGoogle Scholar
  31. Hamrin SF, Persson L (1986) Asymmetrical competition between age classes as a factor causing population oscillations in an obligate planktivorous fish species. Oikos 47:223–232CrossRefGoogle Scholar
  32. Heinrich B (1975) Energetics of pollination. Annu Rev Ecol Syst 6:139–170CrossRefGoogle Scholar
  33. Heinrich B, Raven PH (1972) Energetics and pollination ecology. Science 176:597–602CrossRefPubMedGoogle Scholar
  34. Hepper FN (1963) Flora of west tropical Africa, vol 2. Royal Botanic Gardens, KewGoogle Scholar
  35. Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251–1253. doi: 10.2307/1936841 CrossRefGoogle Scholar
  36. Irwin RE, Brody AK (1998) Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia 116:519–527. doi: 10.1007/s004420050617 CrossRefGoogle Scholar
  37. Irwin RE, Brody AK (1999) Nectar-robbing bumble bees reduce the fitness of Ipomopsis aggregata (Polemoniaceae). Ecology 80:1703–1712CrossRefGoogle Scholar
  38. Irwin RE, Brody AK (2000) Consequences of nectar robbing for realized male function in a hummingbird-pollinated plant. Ecology 81:2637–2643. doi:10.1890/0012-9658(2000)081[2637:conrfr];2Google Scholar
  39. Irwin RE, Galen C, Rabenold JJ, Kaczorowski R, McCutcheon ML (2008) Mechanisms of tolerance to floral larceny in two wildflower species. Ecology 89:3093–3104. doi: 10.1890/08-0081.1 CrossRefGoogle Scholar
  40. Jacobi CM, Antonini Y (2008) Pollinators and defence of Stachytarpheta glabra (Verbenaceae) nectar resources by the hummingbird Colibri serrirostris (Trochilidae) on ironstone outcrops in south-east Brazil. J Trop Ecol 24:301–308. doi: 10.1017/s0266467408005051 CrossRefGoogle Scholar
  41. Janeček Š et al (2007) Importance of big pollinators for the reproduction of two Hypericum species in Cameroon, West Africa. Afr J Ecol 45:607–613. doi: 10.1111/j.1365-2028.2007.00779.x CrossRefGoogle Scholar
  42. Janeček Š et al (2012) Food selection by avian floral visitors: an important aspect of plant-flower interactions in West Africa. Biol J Linn Soc 107:355–367CrossRefGoogle Scholar
  43. Johnson LK, Hubbell SP (1974) Aggression and competition among stingless bees: field studies. Ecology 55:120–127CrossRefGoogle Scholar
  44. Jones EI, Bronstein JL, Ferriere R (2012) The fundamental role of competition in the ecology and evolution of mutualisms. Year Evolut Biol 1256:66–88. doi: 10.1111/j.1749-6632.2011.06552.x Google Scholar
  45. Keasar T, Sadeh A, Shmida A (2008) Variability in nectar production and standing crop, and their relation to pollinator visits in a Mediterranean shrub. Arthropod-Plant Interact 2:117–123CrossRefGoogle Scholar
  46. King C, Ballantyne G, Willmer PG (2013) Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods Ecol Evol 4:811–818. doi: 10.1111/2041-210x.12074 CrossRefGoogle Scholar
  47. Kodric-Brown A, Brown JH (1978) Influence of economics, interspecific competition, and sexual dimorphism on territoriality of migrant Rufous hummingbirds. Ecology 59:285–296CrossRefGoogle Scholar
  48. Kodric-Brown A, Brown JH (1979) Competition between distantly related taxa in the coevolutioin of plants and pollinators. Am Zool 19:1115–1127CrossRefGoogle Scholar
  49. Koehler A, Leseigneur CDC, Verburgt L, Nicolson SW (2010) Dilute bird nectars: viscosity constrains food intake by licking in a sunbird. Am J Physiol Regul Integr Comp Physiol 299:R1068–R1074CrossRefGoogle Scholar
  50. Lyon DL, Chadek C (1971) Exploitation of nectar resources by hummingbirds, bees (Bombus), and Diglossa baritula and its role in the evolution of Penstemon kunthii. Condor 73:246–248CrossRefGoogle Scholar
  51. Maloof JE (2001) The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior. Am J Bot 88:1960–1965. doi: 10.2307/3558423 CrossRefPubMedGoogle Scholar
  52. Maloof JE, Inouye DW (2000) Are nectar robbers cheaters or mutualists? Ecology 81:2651–2661. doi:10.1890/0012-9658(2000)081[2651:anrcom];10.1890/0012-9658(2000)081[2651:anrcom];2Google Scholar
  53. Morris WF (1996) Mutualism denied? Nectar-robbing bumble bees do not reduce female or male success of bluebells. Ecology 77:1451–1462. doi: 10.2307/2265542 CrossRefGoogle Scholar
  54. Navarro L (2001) Reproductive biology and effect of nectar robbing on fruit production in Macleania bullata (Ericaceae). Plant Ecol 152:59–65. doi: 10.1023/a:1011463520398 CrossRefGoogle Scholar
  55. Nicolson SW, Nepi M, Pacini E (2007) Nectaries and nectar. Springer, BerlinCrossRefGoogle Scholar
  56. Niven JE, Scharlemann JPW (2005) Do insect metabolic rates at rest and during flight scale with body mass? Biol Lett 1:346–349CrossRefPubMedPubMedCentralGoogle Scholar
  57. Ollerton J, Nuttman C (2013) Aggresive displacement of carpenter bees Xylocopa nigrita from flowers of Lagenaria sphaerica (Cucurbitaceae) by territorial male eastern olive sunbirds (Cyanomitra olivacea) in Tanzania. J Pollinat Ecol 11:21–26Google Scholar
  58. Padyšáková E, Bartoš M, Tropek R, Janeček Š (2013) Generalization versus specialization in pollination systems: visitors, thieves, and pollinators of Hypoestes aristata (Acanthaceae). PLoS ONE. doi: 10.1371/journal.pone.0059299 PubMedPubMedCentralGoogle Scholar
  59. Palmer TM, Stanton ML, Young TP (2003) Competition and coexistence: exploring mechanisms that restrict and maintain diversity within mutualist guilds. Am Nat 162:S63–S79. doi: 10.1086/378682 CrossRefPubMedGoogle Scholar
  60. Paton DC (1980) The behaviour and feeding ecology of the New Holland Honeyeater Phylidonyris novaehollandiae in Victoria. Ph.D. thesis, Monash UniversityGoogle Scholar
  61. Paton DC (1993) Honeybees in the Australian environment. Bioscience 43(2):95–103CrossRefGoogle Scholar
  62. Paton DC (2000) Disruption of bird-plant pollination systems in southern Australia. Conserv Biol 14(5):1232–1234CrossRefGoogle Scholar
  63. Paton DC, Carpenter FL (1984) Peripheral foraging by territorial rufous hummingbirds: defense by exploitation. Ecology 65(6):1808–1819CrossRefGoogle Scholar
  64. Persson L (1985) Asymmetrical competition: are larger animals competitively superior? Am Nat 126:261–266CrossRefGoogle Scholar
  65. Pimm SL, Rosenzweig ML, Mitchell W (1985) Competition and food selection: field tests of a theory. Ecology 66:798–807CrossRefGoogle Scholar
  66. Primack RB, Howe HF (1975) Interference competition between a hummingbird (Amazilia tzatcal) and skipper butterflies (Hesperiidae). Biotropica 7:55–58CrossRefGoogle Scholar
  67. Prinzinger R, Lubben I, Schuchmann KL (1989) Energy-metabolism and body-temperature in 13 sunbird species (Nectariniidae). Comparat Biochem Physiol A Physiol 92:393–402. doi: 10.1016/0300-9629(89)90581-1 CrossRefGoogle Scholar
  68. Prochazka P, Reif J, Horak D, Klvana P, Lee RW, Yohannes E (2010) Using stable isotopes to trace resource acquisition and trophic position in four Afrotropical birds with different diets. Ostrich 81:273–275. doi: 10.2989/00306525.2010.519889 CrossRefGoogle Scholar
  69. Ramalho M, Guibu LS, Giannini TC, Kleinertgiovannini A, Imperatrizfonseca VL (1991) Characterization of some southern Brazilian honey and bee plants through pollen analysis. J Apic Res 30:81–86CrossRefGoogle Scholar
  70. Reif J et al (2006) Unusual abundance-range size relationship in an Afromontane bird community: the effect of geographical isolation? J Biogeogr 33:1959–1968. doi: 10.1111/j.1365-2699.2006.01547.x CrossRefGoogle Scholar
  71. Reif J et al (2007) Habitat preferences of birds in a montane forest mosaic in the Bamenda Highlands, Cameroon. Ostrich 78:31–36. doi: 10.2989/ostrich.2007. CrossRefGoogle Scholar
  72. Richardson SC (2004) Are nectar-robbers mutualists or antagonists? Oecologia 139:246–254. doi: 10.1007/s00442-004-1504-8 CrossRefPubMedGoogle Scholar
  73. Riegert J et al (2011) Food niche differentiation in two syntopic sunbird species: a case study from the Cameroon Mountains. J Ornithol 152:819–825. doi: 10.1007/s10336-011-0650-0 CrossRefGoogle Scholar
  74. Riegert J, Antczak M, Fainova D, Blazkova P (2014) Group display in the socially monogamous Northern Double-collared Sunbird (Cinnyris reichenowi). Behav Process 103:138–144. doi: 10.1016/j.beproc.2013.12.006 CrossRefGoogle Scholar
  75. Roubik DW, Holbrook NM, Parra GV (1985) Roles of nectar robbers in reproduction of the tropical treelet Quassia amara (Simaroubaceae). Oecologia 66:161–167CrossRefGoogle Scholar
  76. Schoener TW (1983) Field experiments on interspecific competition. Am Nat 122:240–285CrossRefGoogle Scholar
  77. StatSoft I (2013) Electronic statistics textbook. StatSoft, Tulsa, OKGoogle Scholar
  78. Stoaks RD (2000) Foraging interactions at a hummingbird feeder: conflicts of the Anna hummingbird (Aves: Trochilidae) and the prairie yellowjacket (Hymenoptera: Vespidae). Sociobiology 35:49–62Google Scholar
  79. Temeles EJ, Roberts WM (1993) Effect of sexual dimorphism in bill length on foraging behavior—an experimental analysis of hummingbirds. Oecologia 94:87–94. doi: 10.1007/bf00317307 CrossRefGoogle Scholar
  80. Tiebout HM (1993) Mechanisms of competition in tropical hummingbirds: metabolic costs for losers and winners. Ecology 74:405–418CrossRefGoogle Scholar
  81. Tiple AD, Khurad AM, Dennis RLH (2009) Adult butterfly feeding-nectar flower associations: constraints of taxonomic affiliation, butterfly, and nectar flower morphology. J Nat Hist 43:855–884. doi: 10.1080/00222930802610568 CrossRefGoogle Scholar
  82. Traveset A, Willson MF, Sabag C (1998) Effect of nectar-robbing birds on fruit set of Fuchsia magellanica in Tierra del Fuego: a disrupted mutualism. Funct Ecol 12:459–464. doi: 10.1046/j.1365-2435.1998.00212.x CrossRefGoogle Scholar
  83. Tropek R, Konvicka M (2010) Forest eternal? Endemic butterflies of the Bamenda highlands, Cameroon, avoid close-canopy forest. Afr J Ecol 48:428–437. doi: 10.1111/j.1365-2028.2009.01129.x CrossRefGoogle Scholar
  84. Tropek R, Bartoš M, Padyšáková E, Janeček Š (2013) Interference competition between sunbirds and carpenter bees for the nectar of Hypoestes aristata. Afr Zool 48:392–394CrossRefGoogle Scholar
  85. Werner EE (1994) Ontogenic scaling of competitive relations-size-dependent effects and responses in 2 anuran larvae. Ecology 75:197–213. doi: 10.2307/1939394 CrossRefGoogle Scholar
  86. Wolf LL, Hainsworth FR (1977) Temporal patterning of feeding by hummingbirds. Anim Behav 25:976–989CrossRefGoogle Scholar
  87. Wolf LL, Hainsworth FR, Gill FB (1975) Foraging efficiencies and time budgets in nectar-feeding birds. Ecology 56:117–128CrossRefGoogle Scholar
  88. Zimmerman M (1988) Nectar production, flowering phenology, and strategies for pollination. In: Lovett Doust L, Lovett Doust L (eds) Plant reproductive ecology: patterns and strategies. Oxford University Press, OxfordGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Biology Centre, Institute of EntomologyAcademy of Sciences of the Czech RepublicCeske BudejoviceCzech Republic
  2. 2.Department of Zoology, Faculty of ScienceUniversity of South BohemiaCeske BudejoviceCzech Republic
  3. 3.Department of Ecology, Faculty of ScienceCharles University in PraguePrague 2Czech Republic
  4. 4.School of Life SciencesUniversity of KwaZulu-NatalDurbanSouth Africa
  5. 5.Institute of BotanyAcademy of Sciences of the Czech RepublicTřeboňCzech Republic

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