Skip to main content
SpringerLink
Log in

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

  • Plant-microbe-animal interactions - original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: Guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • 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):1171–1181

    Article  Google Scholar 

  • Baker HG (1975) Sugar concentrations in nectars from hummingbird flowers. Biotropica 74:37–41

    Article  Google Scholar 

  • Balkwill K, Norris FG (1985) Taxonomic studies in the Acanthaceae—the genus Hypoestes in southern Africa. S Afr J Bot 51:133–144

    Article  Google Scholar 

  • 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]2.0.co;2

  • Barnes DKA (2003) Competition asymmetry with taxon divergence. Proc R Soc B Biol Sci 270:557–562. doi:10.1098/rspb.2002.2274

    Article  Google Scholar 

  • Barrows EM (1976) Nectar robbing and pollination of Lantana camara (Verbenaceae). Biotropica 8:132–135

    Article  Google Scholar 

  • 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 78:63–74

    Article  Google Scholar 

  • Bartoš M et al (2015) Specialization of pollination systems of two co-flowering phenotypically generalized Hypericum species (Hypericaceae) in Cameroon. Arthropod-Plant Interact 9:241–252

    Article  Google Scholar 

  • Bednekoff PA, Houston AI (1994) Avian daily foraging patterns: effects of digestive constraints and variability. Evol Ecol 8:36–52

    Article  Google Scholar 

  • Borrow N, Demey R (2001) Birds of western Africa. Christopher Helm Publishers, London

    Google Scholar 

  • Boyden TC (1978) Territorial defense against hummingbirds and insects by tropical hummingbirds. Condor 80:216–221

    Article  Google Scholar 

  • 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 26:133–145

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cheek M, Onana JM, Pollard JB (2000) The plants of Mount Oku and the Ijim Ridge, Cameroon. A conservation Checklist. Royal Botanic Gardens, Kew

    Google Scholar 

  • Clutton-Brock TH, Albon SD, Gibson RM, Guiness FE (1979) The logical stag: aspects of fighting in red deer (Cervus elaphus L.). Anim Behav 27:211–275

    Article  Google Scholar 

  • Colwell RK (1973) Competition and coexistence in a simple tropical community. Am Nat 107:737–760

    Article  Google Scholar 

  • 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, Pretoria

  • 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

    Article  PubMed  Google Scholar 

  • Ford HA (1979) Interspecific competition in Australian honeyeaters—depletion of common resources. Aust J Ecol 4:145–164

    Article  Google Scholar 

  • Ford HA (1981) Territorial behaviour in an Australian nectar-feeding bird. Aust J Ecol 6:131–134

    Article  Google Scholar 

  • Ford HA, Paton DC (1976) Resource partitioning and competition in honeyeaters of the genus Meliphaga. Aust J Ecol 1:281–287

    Article  Google Scholar 

  • Ford HA, Paton DC (1982) Partitioning of nectar sources in an Australian honeyeater community. Aust J Ecol 7:149–159

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Galetto L, Bernardello G (2005) Nectar energetics. In: Dafni A, Kevan PG, Husband BC (eds) Practical pollination biology. Enviroquest Ltd, Cambridge, pp 312–313

    Google Scholar 

  • Garrison JSE, Gass CL (1999) Response of a traplining hummingbird to changes in nectar availability. Behav Ecol 10:714–725

    Article  Google Scholar 

  • Gill FB (1988) Trapline foraging by hermit hummingbirds—competition for an undefended, renewable resource. Ecology 69:1933–1942. doi:10.2307/1941170

    Article  Google Scholar 

  • Gill FB, Wolf LL (1975) Economics of feeding territoriality in the golden-winged sunbird. Ecology 56:333–345

    Article  Google Scholar 

  • 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 207:3959–3968

    Article  CAS  PubMed  Google Scholar 

  • Hamrin SF, Persson L (1986) Asymmetrical competition between age classes as a factor causing population oscillations in an obligate planktivorous fish species. Oikos 47:223–232

    Article  Google Scholar 

  • Heinrich B (1975) Energetics of pollination. Annu Rev Ecol Syst 6:139–170

    Article  Google Scholar 

  • Heinrich B, Raven PH (1972) Energetics and pollination ecology. Science 176:597–602

    Article  CAS  PubMed  Google Scholar 

  • Hepper FN (1963) Flora of west tropical Africa, vol 2. Royal Botanic Gardens, Kew

    Google Scholar 

  • Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251–1253. doi:10.2307/1936841

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Irwin RE, Brody AK (1999) Nectar-robbing bumble bees reduce the fitness of Ipomopsis aggregata (Polemoniaceae). Ecology 80:1703–1712

    Article  Google Scholar 

  • 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]2.0.co;2

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 107:355–367

    Article  Google Scholar 

  • Johnson LK, Hubbell SP (1974) Aggression and competition among stingless bees: field studies. Ecology 55:120–127

    Article  Google Scholar 

  • 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 

  • 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 2:117–123

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kodric-Brown A, Brown JH (1978) Influence of economics, interspecific competition, and sexual dimorphism on territoriality of migrant Rufous hummingbirds. Ecology 59:285–296

    Article  Google Scholar 

  • Kodric-Brown A, Brown JH (1979) Competition between distantly related taxa in the coevolutioin of plants and pollinators. Am Zool 19:1115–1127

    Article  Google Scholar 

  • 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–R1074

    Article  Google Scholar 

  • 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 73:246–248

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Maloof JE, Inouye DW (2000) Are nectar robbers cheaters or mutualists? Ecology 81:2651–2661. doi:10.1890/0012-9658(2000)081[2651:anrcom]2.0.co;10.1890/0012-9658(2000)081[2651:anrcom]2.0.co;2

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Nicolson SW, Nepi M, Pacini E (2007) Nectaries and nectar. Springer, Berlin

    Book  Google Scholar 

  • Niven JE, Scharlemann JPW (2005) Do insect metabolic rates at rest and during flight scale with body mass? Biol Lett 1:346–349

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 11:21–26

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Paton DC (1980) The behaviour and feeding ecology of the New Holland Honeyeater Phylidonyris novaehollandiae in Victoria. Ph.D. thesis, Monash University

  • Paton DC (1993) Honeybees in the Australian environment. Bioscience 43(2):95–103

    Article  Google Scholar 

  • Paton DC (2000) Disruption of bird-plant pollination systems in southern Australia. Conserv Biol 14(5):1232–1234

    Article  Google Scholar 

  • Paton DC, Carpenter FL (1984) Peripheral foraging by territorial rufous hummingbirds: defense by exploitation. Ecology 65(6):1808–1819

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Pimm SL, Rosenzweig ML, Mitchell W (1985) Competition and food selection: field tests of a theory. Ecology 66:798–807

    Article  Google Scholar 

  • Primack RB, Howe HF (1975) Interference competition between a hummingbird (Amazilia tzatcal) and skipper butterflies (Hesperiidae). Biotropica 7:55–58

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 30:81–86

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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.2007.78.1.5.49

    Article  Google Scholar 

  • Richardson SC (2004) Are nectar-robbers mutualists or antagonists? Oecologia 139:246–254. doi:10.1007/s00442-004-1504-8

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Roubik DW, Holbrook NM, Parra GV (1985) Roles of nectar robbers in reproduction of the tropical treelet Quassia amara (Simaroubaceae). Oecologia 66:161–167

    Article  Google Scholar 

  • Schoener TW (1983) Field experiments on interspecific competition. Am Nat 122:240–285

    Article  Google Scholar 

  • StatSoft I (2013) Electronic statistics textbook. StatSoft, Tulsa, OK

  • Stoaks RD (2000) Foraging interactions at a hummingbird feeder: conflicts of the Anna hummingbird (Aves: Trochilidae) and the prairie yellowjacket (Hymenoptera: Vespidae). Sociobiology 35:49–62

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Tiebout HM (1993) Mechanisms of competition in tropical hummingbirds: metabolic costs for losers and winners. Ecology 74:405–418

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Tropek R, Bartoš M, Padyšáková E, Janeček Š (2013) Interference competition between sunbirds and carpenter bees for the nectar of Hypoestes aristata. Afr Zool 48:392–394

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wolf LL, Hainsworth FR (1977) Temporal patterning of feeding by hummingbirds. Anim Behav 25:976–989

    Article  Google Scholar 

  • Wolf LL, Hainsworth FR, Gill FB (1975) Foraging efficiencies and time budgets in nectar-feeding birds. Ecology 56:117–128

    Article  Google Scholar 

  • 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, Oxford

    Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Biology Centre, Institute of Entomology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05, Ceske Budejovice, Czech Republic

    Eliška Padyšáková

  2. Department of Zoology, Faculty of Science, University of South Bohemia, Branišovská 31, 370 05, Ceske Budejovice, Czech Republic

    Eliška Padyšáková & Jan Okrouhlík

  3. Department of Ecology, Faculty of Science, Charles University in Prague, Viničná 7, 128 44, Prague 2, Czech Republic

    Eliška Padyšáková, Michael Bartoš & Štěpán Janeček

  4. School of Life Sciences, University of KwaZulu-Natal, Durban, South Africa

    Mark Brown

  5. Institute of Botany, Academy of Sciences of the Czech Republic, Dukelská 135, 379 82, Třeboň, Czech Republic

    Michael Bartoš & Štěpán Janeček

Authors
  1. Eliška Padyšáková
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jan Okrouhlík
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael Bartoš
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Štěpán Janeček
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eliška Padyšáková.

Additional information

Communicated by Nina Farwig.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 542 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Padyšáková, E., Okrouhlík, J., Brown, M. et al. Asymmetric competition for nectar between a large nectar thief and a small pollinator: an energetic point of view. Oecologia 183, 1111–1120 (2017). https://doi.org/10.1007/s00442-017-3817-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-017-3817-4

Keywords

Search

Navigation