Ornithophily or bird pollination is the pollination of flowering plants by birds. This sometimes (but not always) coevolutionary association is derived from insect pollination (entomophily) and is particularly well developed in some parts of the world, especially in the tropics, Southern Africa, and on some island chains. The association involves several distinctive plant adaptations forming a "pollination syndrome". The plants typically have colourful, often red, flowers with long tubular structures holding ample nectar and orientations of the stamen and stigma that ensure contact with the pollinator. Birds involved in ornithophily tend to be specialist nectarivores with brushy tongues and long bills, that are either capable of hovering flight or light enough to perch on the flower structures.
Plant adaptations for ornithophily can be grouped primarily into those that attract and facilitate pollen transfer by birds, and those that exclude other groups, primarily insects, protecting against 'theft' of nectar and pollen. The ovules of bird flowers also tend to have adaptations that protect them from damage during vigorous foraging by hard bird bills.
The flowers of generalist bird-pollinated plant species differ from those pollinated by specialized birds, such as hummingbirds or sunbirds by lacking long corolla tubes and having brush-like, exserted stamens. Most bird pollinated flowers are red and have a lot of nectar. They also tend to be unscented. Flowers with generalist pollinators tend to have dilute nectar but those that have specialist pollinators such as hummingbirds or sunbirds tend to have more concentrated nectar. The nectar of ornithophilous flowers vary in the sugar composition, with hexoses being high in passerine pollinated species while those that are insect pollinated tend to be sucrose rich. Hummingbird pollinated flowers however tend to be sucrose rich.
Different plants have also developed specific adaptations for bird pollination. Many plants of the family Loranthaceae have explosive flowers that shower pollen on a bird that forages near it. They are associated mainly with flowerpeckers in the family Dicaeidae. In Australia, some species of Banksia have flowers that open in response to bird actions thereby reducing the wastage of pollen. In tropical dry forests in southern India, ornithophilous flowers were found to bloom mainly in the hot dry season. Calceolaria uniflora, a species of Scrophularaceae from South America, has a special fleshy appendage on the lower lip of the flower that is rich in sugar. This is fed on by the least seedsnipe (Thinocorus rumicivorus) and in the process the birds brush pollen onto their head and transfer them to other flowers.
The rat's tail babiana (Babiana ringens) produces a strong stalk within the inflorescence that serves as a perch for the malachite sunbird as it visits the flower. Heliconias have special sticky threads that help in the adhesion of pollen to smooth structures such as the bill of a hummingbird. Some African orchids of the genus Disa have pollinaria that stick to the feet of visiting sunbirds.
Plants need to protect against nectar and pollen being taken by non-pollinators. Such animals are sometimes classified as thieves, which simply remove resources without pollinating, and robbers, which damage the flower to access resources. Flowers specialized for pollination by long-billed birds may be especially vulnerable to theft. For example, some bees and birds that cannot reach down the long tubes of bird pollinated flowers simply pierce the flower at the base to obtain nectar, without pollinating.
The main families of specialized nectar feeding birds that are involved in ornithophily are the hummingbirds (Trochilidae), sunbirds (Nectariniidae), and the honey-eaters (Meliphagidae). Other important bird groups include those in the families the Icteridae, the honeycreepers (Thraupidae, Drepanidae), white-eyes (Zosteropidae) and the South African sugar-birds (Promeropidae). Birds may obtain nectar either by perching or by hovering with the latter mainly found in the hummingbirds and sunbirds. Within the hummingbirds, two kinds of foraging are noted with territorial "hermit" hummingbirds and the non-hermits which forage longer distances 
Hummingbirds have the ability to digest sucrose unlike many passerines that prefer hexoses (fructose and glucose). Starlings and their relatives will completely avoid sucrose. Nectar feeding birds typically have a mechanism to quickly excrete excess water. They may have to drink four to five times their body mass of liquid during the day to obtain enough energy. Hummingbirds are capable of excreting nitrogenous wastes as ammonia since they can afford more water loss than birds that feed on low-moisture food sources. Hummingbirds and sunbirds also have special anatomical and physiological adaptations that allow them to quickly excrete excess water. Hummingbirds are also able to turn off their kidney function at night.
Patterns in the evolution of ornithophilyEdit
About 7000 neotropical plant species are hummingbird-pollinated in contrast to about 129 species of North American plants that have evolved ornithophilous associations. Nearly a fourth of the 900 species of the genus Salvia are bird-pollinated in Central and South America and a few also occur in South Africa. Tropical China and the adjacent Indochinese countries harbor relatively few bird-pollinated flowers, among them is Rhodoleia championii, a member of the family Hamamelidaceae, which at any one site can be visited and pollinated by up to seven species of nectar-foraging birds, including Japanese white-eyes (Zosterops japonicus, Zosteropidae) and fork-tailed sunbirds (Aethopyga christinae, Nectariniidae).
Bird pollination is considered as a costly strategy for plants and it evolves only where there are particular benefits for the plant. High altitude ecosystems that lack insect pollinators, those in dry regions or isolated islands tend to favour the evolution of ornithophily, most by specialized nectarivorous birds, such as hummingbirds or sunbirds. Plants pollinated by generalist birds are most diverse in tropical and subtropical lowlands with a pronounced climatic seasonality. These plants are mostly large, woody species that produce a large number of open flowers at the same time in contrast to the mostly small shrubs and herbs that are pollinated by specialized nectarivorous birds. Since generalist bird-pollinated plants are mostly self-incompatible they needed to adapt to pollinators that mostly provide outcrossing, such as generalist birds. These birds mostly feed on arthropods, fruits or seeds even if lots of nectar is available and therefore move a lot through the forest. By this activity they often move between nectar-providing plants and provide outcrossing. Generalist bird-pollinated plants even evolved deterring mechanisms against specialized nectarivorous birds and bees since these groups tend to establish feeding territories within one tree and thus most conduct self-pollination.
On islands however, generalist bird pollination did not evolve to avoid self-pollination but adapted to a reliable pollinator since bees and butterflies are rare just as on montane forests.
Several mite species (mainly in the genera Proctolaelaps, Tropicoseius and Rhinoseius, family Ascidae) have evolved a phoretic mode of life, climbing into the nostrils of hummingbirds that visit flowers and hitching a ride to other flowers where they can feed on the nectar. Hummingbird flower mites favour plants in the families of Heliconiaceae, Costaceae, Zingiberaceae, Amaryllidaceae, Rubiaceae, Apocynaceae, Bromeliaceae, Gesneriaceae, Lobeliaceae and Ericaceae, members of which are associated with hummingbirds.
- Valido A, Dupont YL, Olesen JM (2004). "Bird–flower interactions in the Macaronesian islands" (PDF). J. Biogeogr. 31 (12): 1945–1953. doi:10.1111/j.1365-2699.2004.01116.x.
- Cotton PA (2001). "The Behavior and Interactions of Birds Visiting Erythrina fusca Flowers in the Colombian Amazon". Biotropica. 33 (4): 662–669. doi:10.1646/0006-3606(2001)033[0662:tbaiob]2.0.co;2.
- Tandon R, Shivanna KR, Mohan Ram HY (November 2003). "Reproductive biology of Butea monosperma (Fabaceae)". Annals of Botany. 92 (5): 715–23. doi:10.1093/aob/mcg193. PMC 4244857. PMID 14500327.
- Castellanos MC, Wilson P, Thomson JD (July 2004). "'Anti-bee' and 'pro-bird' changes during the evolution of hummingbird pollination in Penstemon flowers" (PDF). Journal of Evolutionary Biology. 17 (4): 876–85. doi:10.1111/j.1420-9101.2004.00729.x. PMID 15271088.
- Cronk Q, Ojeda I (2008). "Bird-pollinated flowers in an evolutionary and molecular context". Journal of Experimental Botany. 59 (4): 715–27. doi:10.1093/jxb/ern009. PMID 18326865.
- Grant V (1950). "The Protection of the Ovules in Flowering Plants". Evolution. 4 (3): 179–201. doi:10.2307/2405331. JSTOR 2405331.
- Rocca, M. A. & Sazima, M. (2010). "Beyond humminbird-flowers: the other side of ornithophily in the Neotropics". Oecologia Australis. 14: 67–99. doi:10.4257/oeco.2010.1401.03.CS1 maint: multiple names: authors list (link)
- Knudsen JT, Tollsten L, Groth I, Bergström G, Raguso RA (2004). "Trends in floral scent chemistry in pollination syndromes: floral scent composition in hummingbird-pollinated taxa". Botanical Journal of the Linnean Society. 146 (2): 191–199. doi:10.1111/j.1095-8339.2004.00329.x.
- Johnson SD, Nicolson SW (February 2008). "Evolutionary associations between nectar properties and specificity in bird pollination systems". Biology Letters. 4 (1): 49–52. doi:10.1098/rsbl.2007.0496. PMC 2412932. PMID 17999944.
- Rodríguez-Gironés MA, Santamaría L (October 2004). "Why are so many bird flowers red?". PLoS Biology. 2 (10): e350. doi:10.1371/journal.pbio.0020350. PMC 521733. PMID 15486585.
- Dupont YL, Hansen DM, Rasmussen JT, Olesen JM (2004). "Evolutionary changes in nectar sugar composition associated with switches between bird and insect pollination: the Canarian bird-flower element revisited". Functional Ecology. 18 (5): 670–676. doi:10.1111/j.0269-8463.2004.00891.x.
- Feehan J (1985). "Explosive flower-opening in ornithophily: A study of pollination mechanisms in some Central African Loranthaceae". Botanical Journal of the Linnean Society. 90 (2): 129–144. doi:10.1111/j.1095-8339.1985.tb02205.x.
- Ramsey MW (1988). "Floret Opening in Banksia menziesii R.Br.; The Importance of Nectarivorous Birds". Australian Journal of Botany. 36 (2): 225–232. doi:10.1071/BT9880225.
- Murali KS, Sukumar R (1994). "Reproductive Phenology of a Tropical Dry Forest in Mudumalai, Southern India". Journal of Ecology. 82 (4): 759–767. doi:10.2307/2261441. JSTOR 2261441.
- Sérsic AN, Cocucci AA (1996). "A Remarkable Case of Ornithophily in Calceolaria: Food Bodies as Rewards for a Non-nectarivorous Bird*". Botanica Acta. 109 (2): 172–176. doi:10.1111/j.1438-8677.1996.tb00558.x.
- "Bird pollinated plant mixes it up when it comes to sex". phys.org. Retrieved 2019-03-20.
- Rose MJ, Barthlott W (1995). "Pollen-connecting threads in Heliconia (Heliconiaceae)". Plant Systematics and Evolution. 195 (1): 61–65. doi:10.1007/BF00982315.
- Johnson SD, Brown M (2004). "Transfer of pollinaria on birds' feet: a new pollination system in orchids". Plant Systematics and Evolution. 244 (3): 181–188. doi:10.1007/s00606-003-0106-y.
- Hargreaves AL, Harder LD, Johnson SD (May 2009). "Consumptive emasculation: the ecological and evolutionary consequences of pollen theft". Biological Reviews of the Cambridge Philosophical Society. 84 (2): 259–76. doi:10.1111/j.1469-185X.2008.00074.x. PMID 19382932.
- Hargreaves AL, Harder LD, Johnson SD (March 2012). "Floral traits mediate the vulnerability of aloes to pollen theft and inefficient pollination by bees". Annals of Botany. 109 (4): 761–72. doi:10.1093/aob/mcr324. PMC 3286288. PMID 22278414.
- Valdivia CE, González-Gómez PL (2006). "A trade-off between the amount and distance of pollen dispersal triggered by the mixed foraging behaviour of Sephanoides sephaniodes (Trochilidae) on Lapageria rosea (Philesiaceae)" (PDF). Acta Oecologica. 29 (3): 324–327. doi:10.1016/j.actao.2005.12.005.
- Fleming PA, Xie S, Napier K, McWhorter TJ, Nicolson SW (2008). "Nectar concentration affects sugar preferences in two Australian honeyeaters and a lorikeet" (PDF). Functional Ecology. 22 (4): 599–605. doi:10.1111/j.1365-2435.2008.01401.x.
- Fleming PA, Nicolson SW (June 2003). "Osmoregulation in an avian nectarivore, the whitebellied sunbird Nectarinia talatala: response to extremes of diet concentration". The Journal of Experimental Biology. 206 (Pt 11): 1845–54. doi:10.1242/jeb.00351. PMID 12728006.
- McWhorter TJ, Powers DR, Martínez Del Rio C (2003). "Are hummingbirds facultatively ammonotelic? Nitrogen excretion and requirements as a function of body size". Physiological and Biochemical Zoology. 76 (5): 731–43. doi:10.1086/376917. PMID 14671720.
- Tsahar E, Martínez del Rio C, Izhaki I, Arad Z (March 2005). "Can birds be ammonotelic? Nitrogen balance and excretion in two frugivores". The Journal of Experimental Biology. 208 (Pt 6): 1025–34. doi:10.1242/jeb.01495. PMID 15767304.
- Bakken BH, McWhorter TJ, Tsahar E, Del Rio CM (December 2004). "Hummingbirds arrest their kidneys at night: diel variation in glomerular filtration rate in Selasphorus platycercus". The Journal of Experimental Biology. 207 (Pt 25): 4383–91. doi:10.1242/jeb.01238. PMID 15557024.
- Craig AJ, Hulley PE (1995). "Supplementary head molt in Cape White-eyes: a consequence of nectar feeding?" (PDF). J. Field Ornithol. 67 (3): 358–359.
- Abrahamczyk, S. & Kessler, M. (2015). "Morphological and behavioural adaptations to feed on nectar: how feeding ecology determines the diversity and composition of hummingbird assemblages". Journal of Ornithology. 156: 333–347. doi:10.1007/s10336-014-1146-5.CS1 maint: multiple names: authors list (link)
- Grant V (October 1994). "Historical development of ornithophily in the western North American flora". Proceedings of the National Academy of Sciences of the United States of America. 91 (22): 10407–11. doi:10.1073/pnas.91.22.10407. PMC 45029. PMID 7937964.
- Wester P, Claßen-Bockhoff R (2006). "Bird pollination in South African Salvia species". Flora – Morphology, Distribution, Functional Ecology of Plants. 201 (5): 396–406. doi:10.1016/j.flora.2005.07.016.
- Gu L, Luo Z, Zhang D, Renner SS (2010). "Passerine pollination of Rhodoleia championii (Hamamelidaceae) in subtropical China". Biotropica. 42 (3): 336–341. doi:10.1111/j.1744-7429.2009.00585.x.
- Stiles GF (1978). "Ecological and Evolutionary Implications of Bird Pollination". American Zoologist. 18 (4): 715–727. doi:10.1093/icb/18.4.715.
- Abrahamczyk, S. (2019). "Comparison of the ecology and evolution of plants with a generalist bird pollination system between continents and islands worldwide". Biological Reviews. doi: 10.1111/brv.12520.
- Da Cruz DD, Righetti De Abreu VH, Van Sluys M (September 2007). "The effect of hummingbird flower mites on nectar availability of two sympatric Heliconia species in a Brazilian Atlantic forest". Annals of Botany. 100 (3): 581–8. doi:10.1093/aob/mcm135. PMC 2533618. PMID 17638712.