The pollination ecology of Rhododendron floccigerum Franchet (Ericaceae) in Weixi, Yunnan Province, China

Elizabeth Georgian; Zhendong Fang; Eve Emshwiller; Anna Pidgeon

doi:10.26786/1920-7603(2015)11

Authors

Elizabeth Georgian Vilnius University, Vilnius, Lithuania
Zhendong Fang Shangri-La Alpine Botanical Garden
Eve Emshwiller University of Wisconsin Madison
Anna Pidgeon University of Wisconsin-Madison

DOI:

https://doi.org/10.26786/1920-7603(2015)11

Abstract

Identifying the pollinators of Rhododendron species is of great interest due to potential conservation threats in the native range of the genus, but the pollinators of species in Rhododendron subgenus Hymenanthes section Pontica subsection Neriiflora are unknown. Bees (Hymenoptera; family Apidae) are thought to be the pollinators of many Rhododendron species; however, species in subsection Neriiflora have ornithophilous floral morphology. We studied R. floccigerum (subsection Neriiflora) to determine the identities of visiting, potentially pollinating, and robbing species through in-person and time lapsed camera trap observations. We compared floral morphological characteristics of R. floccigerum with visitor morphological measurements to determine if visitors could fit inside the corolla. Thirteen species were observed visiting R. floccigerum (two insects, two mammals, and nine birds) and this study provides the first empirical evidence of both bird and mammal visitors to Rhododendron species. We determined that the following species are potential pollinators: Bombus sp. (an insect genus), Aethopyga gouldiae, Garrulax affinis, Heterophasia melanoleuca, and Yuhina diademata (all bird species), and we suspect that Apis sp. (an insect genus), Dremomys pernyi, Tamiops swinhoei (two mammal species), Minla ignotincta, M. strigula, Parus major, and Phylloscopus affinis (four bird species) likely rob R. floccigerum. All visitors were able to fit their heads/bodies into the corolla. We also found that though predation is frequent, the number of robbers and variety of robbing methods is unlikely to contribute to floral morphological evolution or speciation. Further understanding of the pollination biology of species in subgenus Hymenanthes will allow for effective conservation.

Author Biographies

Elizabeth Georgian, Vilnius University, Vilnius, Lithuania

Department of Botany and Genetics, Lecturer

Eve Emshwiller, University of Wisconsin Madison

Botany Department

Anna Pidgeon, University of Wisconsin-Madison

Department of Forest and Wildlife Ecology

References

Adler LS (2000) The ecological significance of toxic nectar. Oikos 91: 409-420. DOI: https://doi.org/10.1034/j.1600-0706.2000.910301.x

Argent GCG, Lamb A, Phillipps A, Collenette IS (1988) Rhododendrons of Sabah.

Sabah National Parks Publication, 8. Sabah, Borneo.

Arizmendi MDC (2001) Multiple ecological interactions: nectar robbers and hummingbirds in a highland forest in Mexico. Canadian Journal of Zoology 79: 997-1006. DOI: https://doi.org/10.1139/z01-066

Arizmendi MDC, Dominguez 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 (1): 119-127. DOI: https://doi.org/10.2307/2390270

Berry PE, Hahn WJ, Sytsma KJ, Hall JC, Mast A (2004) Phylogenetic relationships and biogeography of Fuchsia (Onagraceae) based on non-coding nuclear and chloroplast DNA data. American Journal of Botany 91: 601-614. DOI: https://doi.org/10.3732/ajb.91.4.601

Cronk Q and Ojeda I (2008) Bird pollinated flowers in an evolutionary and molecular context. Journal of Experimental Biology 59 (4): 715-727. DOI: https://doi.org/10.1093/jxb/ern009

Cruttwell NEG (1988) Natural hybridization among rhododendrons in Papua New Guinea. Journal of the Australian Rhododendron Society 27 (3).

Deng XB, Ren PY, Gao JY, Li QJ (2004) The striped squirrel (Tamiops swinhoei hainanus) as a nectar robber of ginger (Alpina kwangsiensis). Biotropica 36 (4): 633-636. DOI: https://doi.org/10.1111/j.1744-7429.2004.tb00357.x

De Waal C, Anderson B, Barrett SCH (2011) The natural history of pollination and mating in bird-pollinated Babiana (Iridaceae). Annals of Botany 1-13. DOI: https://doi.org/10.1093/aob/mcr172

Escaravage N, Wagner J (2004) Pollination effectiveness and pollen dispersal in a Rhododendron ferrugineum (Ericaceae) population. Plant Biology 6: 606-615. DOI: https://doi.org/10.1055/s-2004-821143

Galen C, Cuba J (2001) Down the tube: pollinators, predators, and the evolution of flower shape in the alpine skypilot, Polemonium viscosum. Evolution 55 (10): 1963-1971. DOI: https://doi.org/10.1111/j.0014-3820.2001.tb01313.x

Georgian E (2014) Biodiversity and cultural diversity conservation in the Himalayas of Yunnan Province, China. Dissertation, University of Wisconsin-Madison.

Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology and Systematics 36: 47-79. DOI: https://doi.org/10.1146/annurev.ecolsys.36.091704.175539

Grindeland JM, Sletvold N, Ims RA (2005) Effects of floral display size and plant density on pollinator visitation rate in a natural population of Digitalis purpurea. Functional Ecology 19 (3): 383-390. DOI: https://doi.org/10.1111/j.1365-2435.2005.00988.x

Hu WK (1990) A study on the genus Rhododendron L. subsection Neriiflora Sleumer in China. Acta Phytotaxonmica Sinica 28 (5): 379-383.

Irwin RE, Brody AK, Waser NM (2001) The impact of floral larceny on individuals, populations, and communities. Oecologia 116: 519-527. DOI: https://doi.org/10.1007/s004420050617

Irwin RE, Bronstein JL, Manson JS, Richardson L (2010) Nectar robbing: ecological and evolutionary perspectives. Annual Review Ecol. Evol. Syst. 41: 271-292. DOI: https://doi.org/10.1146/annurev.ecolsys.110308.120330

Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Niwot, Colorado.

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 in Ecology and Evolution 4: 811-818. DOI: https://doi.org/10.1111/2041-210X.12074

Kingdon-Ward F (2007) Return to the Irrawaddy. Second Ed. Orchid Press, Bangkok, Thailand.

Klassen J (1989) The visitation rate of bees to spotted knapweed as a function of floral density. Biological Station, University of Michigan.

Koca I, Koca AF (2007) Poisoning by mad honey: a brief review. Food Chemistry Toxicology 45 (8): 1315-1318. DOI: https://doi.org/10.1016/j.fct.2007.04.006

Kudo G (1993) Relationships between flowering time and fruit set of the entomophilous alpine shrub, Rhododendron aureum (Ericaceae), inhabiting snow patches. American Journal of Botany 80 (11): 1300-1304. DOI: https://doi.org/10.1002/j.1537-2197.1993.tb15368.x

Lara C, Ornelas JF (2001) Preferential nectar robbing of flowers with long corollas: experimental studies of two hummingbird species visiting three plant species. Acta Oecologica 128 (2): 263-273. DOI: https://doi.org/10.1007/s004420100640

Liu ZJ, Chen LZ, Liu KW, Li LQ, Rao WH, Zhang ZT, Tan GT, Huan LQ (2013) Adding perches for cross-pollination ensures the reproduction of a self-incompatible orchid. Plos One 8 (1). DOI: https://doi.org/10.1371/journal.pone.0053695

Ma YP, Milne RI, Zhang CQ, Yang JB (2010) Unusual patterns of hybridization involving a narrow endemic Rhododendron species (Ericaceae). American Journal of Botany 97 (10): 1749-1757. DOI: https://doi.org/10.3732/ajb.1000018

Ma YP, Nielsen J, Chamberlain DF, Li XY, Sun WB (2014) The conservation of Rhododendrons is of greater urgency than has been previously acknowledged in China. Biodiversity Conservation 23: 3149-2154. DOI: https://doi.org/10.1007/s10531-014-0764-9

McQuire JFF, Robinson MLA (2009) Pocket guide to Rhododendron species based on the descriptions by H.H. Davidian. Kew Publishing, London, UK.

Milne RI, Davies C, Prickett R, Inns LH, Chamberlain DF (2010) Phylogeny of Rhododendron subgenus Hymenanthes based on chloroplast DNA markers: between-lineage hybridization during adaptive radiation? Plant Systematic Evolution 285: 233-244. DOI: https://doi.org/10.1007/s00606-010-0269-2

Ng SC, Corlett RT (2000) Comparative reproductive biology of the six species of Rhododendron (Ericaceae) in Hong Kong, South China. Canadian Journal of Botany 78: 221-229. DOI: https://doi.org/10.1139/b99-181

Ono A, Dohzono I, Sugawara T (2008) Bumblebee pollination and reproductive biology of Rhododendron semibarbatum (Ericaceae). Journal of Plant Resources 121: 319-327. DOI: https://doi.org/10.1007/s10265-008-0155-y

Owen EL, Bale JS, Hayward SAL (2013) Can winter-active bumble bees survive the cold? Assessing the cold tolerance of Bombus terrestris audax and the effects of pollen feeding. PLOS ONE 8 (11). DOI: https://doi.org/10.1371/journal.pone.0080061

Parsche S, Fründ J, Tscharntke T (2011) Experimental environmental change and mutualistic vs. antagonistic plant flower-visitor interactions. Perspectives in Plant Ecology, Evolution and Systematics 13: 27-35. DOI: https://doi.org/10.1016/j.ppees.2010.12.001

R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org.

Steinheimer FD (1999) The mountain black-eye Chlorocharis emiliae (Zosteropidae) as a rhododendron flower visitor on Mt Kinabalu, Sabah, Malaysia. Forktail 15: 100.

Stevens P (1976) The altitudinal and geographical distributions of flower types in Rhododendron section Vireya, especially in the Papuasian species, and their significance. Botanical Journal of the Linnean Society 72: 1-33. DOI: https://doi.org/10.1111/j.1095-8339.1976.tb01392.x

Stevens P (1985) Malesian vireya rhododendrons-towards an understanding of their evolution. Notes from the Royal Botanic Garden Edinburgh 43 (1).

Stein K, Hensen I (2011) Potential pollinators and robbers: a study of the floral visitors of Heliconia angusta (Heliconiaceae) and their behavior. Journal of Pollination Ecology 4 (6): 39-47. DOI: https://doi.org/10.26786/1920-7603(2011)7

Sugiura S (2012) Flower-visiting insect communities on two closely related Rhododendron species flowering in different seasons. Anthropod-Plant Interactions 6: 333-344. DOI: https://doi.org/10.1007/s11829-012-9187-2

Wong J, Youde E, Dickinson B, Hale M (2002) Report of the Rhododendron feasibility study. School of Agriculture and Forest Studies. University of Wales, Bangor.

Wu ZY, Raven PH, Hong DY (Ed) (2005) Flora of China. (Vol. 14) (Apiaceae through Ericaceae). Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis.