Potential pollinators and robbers: a study of the floral visitors of Heliconia angusta (Heliconiaceae) and their behaviour

Katharina Stein; Isabell Hensen

doi:10.26786/1920-7603(2011)7

Authors

Katharina Stein
Isabell Hensen

DOI:

https://doi.org/10.26786/1920-7603(2011)7

Keywords:

hummingbirds, stingless bees, <i>Trigona</i>, pollen robbers, nectar, inflorescence attractiveness

Abstract

Floral syndromes are traditionally thought to be associated with particular pollinator groups. Ornithophilous flowers tend to have traits that facilitate bird pollination such as having long, narrow, tubular corollas, often vivid coloration and diluted, sucrose-rich nectar. However, recent studies have shown that flowers attract a broader spectrum of visitors than might be expected. Furthermore, the classification of floral visitors as ‘robbers’ or ‘pollinators’ often is not as simple as it seems, as pollinators can at times act as robbers and vice versa. We studied the species composition, behaviour and ecology of floral visitors, including potential pollinators and robbers, of Heliconia angusta (Heliconiaceae), an endemic understory herb of the Atlantic Rainforest of Brazil. In addition, the impact of the plant inflorescence attractiveness and of weather and light conditions on visitor abundance and frequency was investigated.

Flower visitors were found to be scarce with a total of only 151 visits being observed during 120 h of field observations. A stingless bee species (Trigona sp.) appeared to be the most abundant visitor to the ornithophilous flowers of H. angusta, along with four different species of hummingbirds and two species of butterflies. We consider Trigona sp. rather as pollen robber, but which still has the potential to be a secondary pollinator, whereas the hummingbirds were the principle legitimate visitors. Most flower visitors were recorded between 9.00 am and 1.00 pm with a higher number visiting under semi-shaded conditions than in full shade. Hummingbird numbers increased with flower abundance while the other visitor group numbers were not affected.

References

Almeda F (1977) Systematics of the neotropical genus Centradenia (Melastomataceae). Journal of the Arnold Arboretum 58:73-108. DOI: https://doi.org/10.5962/bhl.part.29236

Arizmendi MC, Domínguez CA, Dirzo R (1996) The role of an avian nectar robber and of hummingbird pollinators in the reproduction of two plant species. Functional Ecology 10:119-127. DOI: https://doi.org/10.2307/2390270

Baker HG, Baker I, Hodges SA (1998) Sugar composition of nectar and fruits consumed by birds and bats in the tropics and subtropics. Biotropica 30:559-586. DOI: https://doi.org/10.1111/j.1744-7429.1998.tb00097.x

Baker HG, Baker I (1990) The predictive value of nectar chemistry to the recognition of pollinator types. Israel Journal of Botany 39:157-166..

Bawa KS (1990) Plant-pollinator interactions in tropical rain forests. Annual Review of Ecology, Evolution, and Systematics 21:399-422. DOI: https://doi.org/10.1146/annurev.ecolsys.21.1.399

Bawa KS, Perry DR, Bullock SH, Coville RE, Grayum MH (1985) Reproductive biology of tropical lowland rain forest trees. II. Pollination mechanisms. American Journal of Botany 72:346-356. DOI: https://doi.org/10.1002/j.1537-2197.1985.tb05358.x

Biesmeijer JC, Slaa EJ, Siqueira de Castro M, Viana BF, Kleinert A, Imperatriz-Fonseca VL (2005) Connectance of Brazilian social bee – food plant networks is influenced by habitat, but not by latitude, altitude or network size. Biota Neotropica 5:1-9. DOI: https://doi.org/10.1590/S1676-06032005000100010

Biesmeijer JC, Richter JAP, Smeets MAJP, Sommeijer MJ (1999a) Niche differentiation in nectar-collecting stingless bees: the influence of morphology, floral choice and interference competition. Ecological Entomology 24:380-388. DOI: https://doi.org/10.1046/j.1365-2311.1999.00220.x

Biesmeijer JC, Smeets MAJP, Richter JAP, , Sommeijer MJ (1999b) Nectar foraging by stingless bees in Costa Rica: botanical and climatological influences on sugar concentration of nectar collected by Melipona. Apidologie 30:43-55. DOI: https://doi.org/10.1051/apido:19990106

Bosch M, Waser NM (2001) Experimental manipulation of plant density and its effect on pollination and reproduction of two confamilial montane herbs. Oecologia 126:76-83. DOI: https://doi.org/10.1007/s004420000488

Botes C, Johnson SD, Cowling RM (2009) The birds and the bees: using selective exclusion to identify effective pollinators of African tree Aloes. International Journal of Plant Sciences 170: 151-156. DOI: https://doi.org/10.1086/595291

Brody AK, Mitchell RJ (1997) Effects of experimental manipulation of inflorescence size on pollination and pre-dispersal seed predation in the hummingbird-pollinated plant Ipomopsis aggregata. Oecologia 110:86-93. DOI: https://doi.org/10.1007/s004420050136

Bruna EM, Kress WJ, Marques F, da Silva OF (2004) Heliconia acuminata reproductive success is independent of local floral density. Acta Amazonica 34:467-471. DOI: https://doi.org/10.1590/S0044-59672004000300012

Campbell DR, Waser NM, Price MV (1996) Mechanisms of hummingbird-mediated selection for flower width in Ipomopsis aggregata. Ecology 77:1463-1472. DOI: https://doi.org/10.2307/2265543

Canela MBF, Sazima M (2005) The pollination of Bromelia antiacantha (Bromeliaceae) in southeastern Brazil: ornithophilous versus melittophilous features. Plant Biology 7:411-416. DOI: https://doi.org/10.1055/s-2005-865619

Dahlgren RMT, Clifford HT, Yeo PF (1985) The families of the monocotyledons. Springer-Verlag, Berlin. DOI: https://doi.org/10.1007/978-3-642-61663-1

De Castro CC, De Oliveira PE (2002) Pollination biology of distylous Rubiaceae in the Atlantic rain forest, SE Brazil. Plant Biology 4:640-646. DOI: https://doi.org/10.1055/s-2002-35433

De Castro CC, Araujo AC (2004) Distyly and sequential pollinators of Psychotria nuda (Rubiaceae) in the Atlantic rain forest, Brazil. Plant Systematics and Evolution 244:131-139. DOI: https://doi.org/10.1007/s00606-003-0036-8

Deyrup M, Menges E (1997) Pollination ecology of the rare scrub mint Dicerandra frutescens (Lamiaceae). Florida Scientist 60:143-157.

Dias da Cruz D, Mello MAR, Van Sluys M (2006) Phenology and floral visitors of two sympatric Heliconia species in the Brazilian Atlantic forest. Flora 201:519-527. DOI: https://doi.org/10.1016/j.flora.2005.12.001

Döll S, Hensen I, Schmidt-Lebuhn AN, Kessler M (2007) Pollination ecology of Justicia rusbyi (Acanthaceae), a common understory plant in a tropical mountain forest in eastern Bolivia. Plant Species Biology 22:211-216. DOI: https://doi.org/10.1111/j.1442-1984.2007.00195.x

Feinsinger P (1976) Organization of a tropical guild of nectarivorous birds. Ecological monographs 46:257-291. DOI: https://doi.org/10.2307/1942255

Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics 35:375-403. DOI: https://doi.org/10.1146/annurev.ecolsys.34.011802.132347

Fidalgo A, Kleinert A (2010) Floral preferences and climate influence in nectar and pollen foraging by Melipona rufiventris Lepeletier (Hymenoptera: Meliponini) in Ubatuba, Sao Paulo State, Brazil. Neotropical Entomology 39:879-884. DOI: https://doi.org/10.1590/S1519-566X2010000600005

Freitas BM, Paxton RJ (1998) A comparison of two pollinators: the introduced honey bee Apis mellifera and an indigenous bee Centris tarsata on cashew Anacardium occidentale in its native range of NE Brazil. Journal of Applied Ecology 35:109-121. DOI: https://doi.org/10.1046/j.1365-2664.1998.00278.x

Galetto L (1998) Estructura floral y composición química del néctar en tres especies de Rubiaceae. Kurtziana 26:83-98.

Gao JY, Zhang L, Deng XB, Ren PY, Kong JJ, Li QJ (2004) The floral biology of Curcumorpha longiflora (Zingiberaceae): a ginger with two day flowers. American Journal of Botany 91:289-293. DOI: https://doi.org/10.3732/ajb.91.2.289

Garrison JSE, Gass CL (1999) Response of a traplining hummingbird to changes in nectar availability. Behavioural Ecology 6:714-725. DOI: https://doi.org/10.1093/beheco/10.6.714

Gass CL, Garrison JSE (1999) Energy regulation by traplining hummingbirds. Functional Ecology 13:483-492. DOI: https://doi.org/10.1046/j.1365-2435.1999.00335.x

Gass CL, Montgomerie RD (1981) Hummingbird foraging behaviour: decision-making and energy regulation. In: Karnil AC, Sargent TD (eds.) Foraging behaviour: ecological, ethological, and psychological approaches. Garland STPM Press, New York, pp 157-194.

Gentry AH (1974a) Coevolutionary patterns in Central American Bignoniaceae. Annals of the Missouri Botanical Garden 61:728-759. DOI: https://doi.org/10.2307/2395026

Gentry AH (1974b) Flowering phenology and diversity in tropical Bignoniaceae. Biotropica 6:54-68. DOI: https://doi.org/10.2307/2989698

Gill FB (1988) Trapline foraging by hermit hummingbirds: competition for an undefended, renewable resource. Ecology 69:1933-1942. DOI: https://doi.org/10.2307/1941170

Graves GR (1982) Pollination of Tristerix mistletoe (Loranthaceae) by Diglossa (Aves, Thraupidae). Biotropica 14:316-317. DOI: https://doi.org/10.2307/2388094

Gross C (2005) Pollination efficiency and pollinator effectiveness. In: Dafni A, Kevan P, Husband B (eds). Practical Pollination Biology. Ontario Enviroquest, Cambridge, pp 354–363 .

Hainsworth FR, Tardiff M, Wolf LL (1981) Proportional control for daily energy regulation in hummingbirds. Physiological Zoology 54:452-462. DOI: https://doi.org/10.1086/physzool.54.4.30155838

Harder LD, Jordan CY, Gross WE, Routley MB (2004) Beyond floricentrism: The pollination function of inflorescences. Plant Species Biology 19:137-148. DOI: https://doi.org/10.1111/j.1442-1984.2004.00110.x

Horvitz CC, Schemske DW (1990) Spatio temporal variation in insect mutualism of a neotropical herb. Ecology 71:1085-1097. DOI: https://doi.org/10.2307/1937377

Hubbell SP, Johnson LK (1978) Comparative foraging behaviour of six stingless bee species exploiting a standardized resource. Ecology 59:1123-1136. DOI: https://doi.org/10.2307/1938227

Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251-1253. DOI: https://doi.org/10.2307/1936841

Janzen DH (1975) Ecology of plants in the tropics. Edward Arnold, London.

Kress WJ (1990) The diversity and distribution of Heliconia (Heliconiaceae) in Brazil. Acta Botanica Brasilica 4:159-167.. DOI: https://doi.org/10.1590/S0102-33061990000100011

Krömer T, Kessler M, Lohaus G, Schmidt-Lebuhn AN (2008) Nectar sugar composition and concentration in relation to pollination syndromes in Bromeliaceae. Plant Biology 10:502-511. DOI: https://doi.org/10.1111/j.1438-8677.2008.00058.x

Kurtz BC, de Araújo DSD (2000) Composição florística e estrutura do componente arbóreo de um trecho de Mata Atlântica na Estaoção Ecológica Estadual do Paraíso, Cachoeiras de Macacu, Rio de Janeiro, Brasil. Rodriguésia 51:69-112. DOI: https://doi.org/10.1590/2175-7860200051787903

McDade LA, Kinsman S (1980) The impact of floral parasitism in two neotropical hummingbird-pollinated plant species. Evolution 34:944-958. DOI: https://doi.org/10.1111/j.1558-5646.1980.tb04033.x

Michener CD (1979) Biogeography of the bees. Annals of the Missouri Botanical Garden 66:277-347. DOI: https://doi.org/10.2307/2398833

Mitchell RJ, Karron JD, Holmquist KG, Bell JM (2004) The influence of Mimulus ringens floral display size on pollinator visitation patterns. Functional Ecology 18:116-124. DOI: https://doi.org/10.1111/j.1365-2435.2004.00812.x

Morellato LPC, Haddad CFP (2000) Introduction: The Brazilian Atlantic Forest. Biotropica 32:786-792. DOI: https://doi.org/10.1111/j.1744-7429.2000.tb00618.x

Oliveira-Filho AT, Fontes MAL (2000) Patterns of floristic differentiation among Atlantic Forests in southeastern Brazil and influence of climate. Biotropica 32:793-810. DOI: https://doi.org/10.1111/j.1744-7429.2000.tb00619.x

Ollerton J, Alarcón R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, Rottenberry J (2009) A global test of the pollination syndrome hypothesis. Annals of Botany 103:1471-1480. DOI: https://doi.org/10.1093/aob/mcp031

Ollerton J, Johnson SD, Cranmer L, Kellie S (2003) The pollination ecology of an assemblage of grassland Asclepiads in South Africa. Annals of Botany 92:807-834. DOI: https://doi.org/10.1093/aob/mcg206

Pereboom JJM, Biesmeijer JC (2003) Thermal constraints for stingless bee foragers: the importance of body size and coloration. Oecologia 137:42-50. DOI: https://doi.org/10.1007/s00442-003-1324-2

Perret M, Chautems A, Spichiger R, Peixoto M, Savolainen V (2001) Nectar sugar composition in relation to pollination syndromes in Sinningieae (Gesneriaceae). Annals of Botany 87:267-273. DOI: https://doi.org/10.1006/anbo.2000.1331

Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, Portland.

Ramalho M, Kleinert-Giovannini A, Imperatriz-Fonseca VL (1990) Important bee plants for stingless bees (Melipona and Trigonini) and Africanised honeybees (Apis mellifera) in neotropical habitats: a review. Apidologie 21:469-488. DOI: https://doi.org/10.1051/apido:19900508

Renner S (1983) The widespread occurrence of anther destruction by Trigona bees in Melastomataceae. Biotropica 15:251-256. DOI: https://doi.org/10.2307/2387649

Robertson AW, Ladley JI, Kelly D (2005) Effectiveness of short-tongued bees as pollinators of apparently ornithophilous New Zealand mistletoes. Austral Ecology 30:298-309. DOI: https://doi.org/10.1111/j.1442-9993.2005.01474.x

Rodriguez-Robles JA, Melendez EJ, Ackermann JD (1992) Effects of display size, flowering phenology, and nectar availability on effective visitation frequency in Comparettia falcata (Orchidaceae). American Journal of Botany 79:1009-1017. DOI: https://doi.org/10.1002/j.1537-2197.1992.tb13690.x

Roubik DW, Yanega D, Aluja SM, Buchmann SL, Inouye DW (1995) On optimal nectar foraging by some tropical bees (Hymenoptera: Apidae). Apidologie 26:197-211. DOI: https://doi.org/10.1051/apido:19950303

Roubik DW (1989) Ecology and Natural History of Tropical Bees. Cambridge University Press, Cambridge. DOI: https://doi.org/10.1017/CBO9780511574641

Roubik DW, Buchmann SL (1984) Nectar selection by Melipona and Apis mellifera (Hymenoptera: Apidae) and the ecology of nectar intake by bee colonies in a tropical forest. Oecologia 61:1-10. DOI: https://doi.org/10.1007/BF00379082

Roubik DW (1982) The ecological impact of nectar-robbing bees and pollinating hummingbirds on a tropical shrub. Ecology 63:354-360. DOI: https://doi.org/10.2307/1938953

Sazima I, Buzato S, Sazima M (1995) The Saw-billed Hermit Ramphodon naevius and its flowers in southeastern Brazil. Journal of Ornithology 136:195-206. DOI: https://doi.org/10.1007/BF01651241

Schmid S, Schmid VS, Zillikens A, Harter-Marques B., Steiner J (2011) Bimodal pollination system of the bromeliad Aechmea nudicaulis involving hummingbirds and bees. Plant Biology 13:41-50. DOI: https://doi.org/10.1111/j.1438-8677.2010.00348.x

Schwerdtfeger, M (1996). Die Nektarzusammensetzung der Asteridae und ihre Beziehung zu Blütenökologie und Systematik. Dissertationes Botanicae 264..

Singer RB, Sazima M (2001) Flower morphology and pollination mechanism in three sympatric Goodyerinae Orchids from Southeastern Brazil. Annals of Botany 88:989-997. DOI: https://doi.org/10.1006/anbo.2001.1534

Singer RB, Sazima M (2000) The pollination of Stenorrhynchos lanceolatus (Aublet) L.C. Rich. (Orchidaceae: Spiranthinae) by hummingbirds in southeastern Brazil. Plant Systematics and Evolution 223:221-227. DOI: https://doi.org/10.1007/BF00985281

Simão DG, Scatena VL (2001) Morphology and anatomy in Heliconia angusta Vell. and H. velloziana L. Emygd. (Zingiberales: Heliconiaceae) from the Atlantic forest of southeastern Brazil. Revista Brasileira de Botânica 24:415-424. DOI: https://doi.org/10.1590/S0100-84042001000400007

Slaa EJ, Sánchez Chaves LA, Malagodi-Braga KS, Hofstede FE (2006) Stingless bees in applied pollination: practice and perspectives. Apidologie 37:293-315. DOI: https://doi.org/10.1051/apido:2006022

Smith CE, Stevens JT, Temeles EJ, Ewald PW, Hebert RJ, Bonkovsky RL (1996) Effect of floral orifice width and shape on hummingbird-flower interactions. Oecologia 106:482-492. DOI: https://doi.org/10.1007/BF00329706

Steven JC, Rooney TP, Boyle OD, Waller DM (2003) Density-dependent pollinator visitation and self-incompatibility in upper Great Lakes populations of Trillium grandiflorum. Journal of the Torrey Botanical Society 130:23-29. DOI: https://doi.org/10.2307/3557522

Stiles FG, Freeman CE (1993) Patterns in floral nectar characteristics of some bird-visited plant species from Costa Rica. Biotropica 25:191-205. DOI: https://doi.org/10.2307/2389183

Stiles FG, Wolf LL (1979) Ecology and evolution of lek mating behaviour in the long-tailed hermit hummingbird. Ornithological Monographs 27:1-78. DOI: https://doi.org/10.2307/40166760

Stiles FG (1975) Ecology, flowering phenology, and hummingbird pollination of some Costa Rican Heliconia Species. Ecology 56:285-301. DOI: https://doi.org/10.2307/1934961

Stone JL, Jenkins EG (2008) Pollinator abundance and pollen limitation of a solanaceous shrub at premontane and lower montane sites. Biotropica 40:55-61. DOI: https://doi.org/10.1111/j.1744-7429.2007.00339.x

Thompson JN, Pellmyr O (1992) Mutualism with pollinating seed parasites amid co-pollinators: constraints on specialization. Ecology 73:1780-1791. DOI: https://doi.org/10.2307/1940029

Tiebout HM (1992) Comparative energetics of divergent foraging modes: a doubly labelled water experiment on hummingbird competition. Animal Behaviour 44:895-906. DOI: https://doi.org/10.1016/S0003-3472(05)80585-8

Tomimatsu H, Ohara M (2003) Floral visitors of Trillium camschatcense (Trilliaceae) in fragmented forests. Plant Species Biology 18:123-127. DOI: https://doi.org/10.1111/j.1442-1984.2003.00090.doc.x

Veloso HP, Rangel-Filho AL, Lima JCA (1991) Classificação da vegetação brasileira, adaptada a um sistema universal. IBGE/CDDI, Departamento de Documentação e Biblioteca, Rio de Janeiro.

Vicens N, Bosch J (2000) Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae). Environmental Entomology 29:413-420. DOI: https://doi.org/10.1603/0046-225X-29.3.413

Vogel S (1996) Christian Konrad Sprengel´s theory of the flower: The cradle of floral ecology. In: Lloyd DG, Barrett SCH (eds). Floral ecology, studies on floral evolution in animal-pollinated plants. Chapman and Hall, New York, pp 44-62. DOI: https://doi.org/10.1007/978-1-4613-1165-2_2

Waser NM (2006) Specialization and Generalization in Plant-Pollinator Interactions: A Historical Perspective. In: Waser NM, Ollerton J (eds). Plant-Pollinator Interactions: from Specialization to Generalization. The University of Chicago Press, Chicago, pp 3-17.

Waser NM, Ollerton J (2006) Plant-pollinator interactions: from specialization to generalization. The University of Chicago Press, Chicago.

Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043-1056. DOI: https://doi.org/10.2307/2265575

Waser NM, Price MV (1990) Pollination efficiency and effectiveness of bumble bees and hummingbirds visiting Delphinium nelsonii. Collectanea Botanica 19:9-20. DOI: https://doi.org/10.3989/collectbot.1990.v19.114

Willmer PG, Corbet SA (1981) Temporal and microclimatic partitioning of the floral resources of Justicia aurea amongst a concourse of pollen vectors and nectar robbers. Oecologia 51:67-78. DOI: https://doi.org/10.1007/BF00344655

Willmott AP, Búrquez A (1996) The pollination of Merremia palmeri (Convolvulaceae): can hawk moths be trusted? American Journal of Botany 83:1050-1056. DOI: https://doi.org/10.1002/j.1537-2197.1996.tb12802.x