Biology:Ornithophily

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Short description: Pollination by birds
Hummingbird Phaethornis longirostris on an Etlingera inflorescence

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.[1] 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

A lesser violetear

thumb|Inflorescences of [[Butea allow birds to perch on the stalk[2][3]]]

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,[4] protecting against 'theft' of nectar and pollen.[5] The ovules of bird flowers also tend to have adaptations that protect them from damage during vigorous foraging by hard bird bills.[6]

One of the general adaptation patterns is the red flower color for many plant species. The pollinator, birds, are tetrachromats, and one type of the single cone has specific opsin to detect long-wavelength light (below about 600 nm).[7] Therefore, birds have red photoreceptors and are sensitive to red color, and red flower colors can have a strong contrast with green leaf background. Better bird attraction is thus the primary reason behind the red color adaptation. Moreover, flowers of generalist bird-pollinated species from the New World have purer red colors than those from the Old World, which often have a secondary reflectance peak around shorter-wavelength region. The secondary peak reduces the contrast of red color with the background and the avoidance of insects (higher risk of nectar robbing), decreasing the efficiency of pollination.[8][9]

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.[10] Most bird pollinated flowers are red and have a lot of nectar. They also tend to be unscented.[11] 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.[12][13] 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.[14]

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.[15] In Australia, some species of Banksia have flowers that open in response to bird actions thereby reducing the wastage of pollen.[16] In tropical dry forests in southern India, ornithophilous flowers were found to bloom mainly in the hot dry season.[17] 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.[18]

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.[19] Heliconias have special sticky threads that help in the adhesion of pollen to smooth structures such as the bill of a hummingbird.[20] Some African orchids of the genus Disa have pollinaria that stick to the feet of visiting sunbirds.[21]

Plants need to protect against nectar and pollen being taken by non-pollinators.[22] 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.[23] 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.[24]

Bird adaptations

Ruby-throated hummingbird (Archilochus colubris) at scarlet beebalm flowers (Monarda didyma)

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, Carduelinae), 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 non-territorial "hermit" hummingbirds which forage longer distances and the territorial non-hermits.[5]

Hummingbirds have the ability to digest sucrose unlike many passerines that prefer hexoses (fructose and glucose). Starlings and their relatives will completely avoid sucrose.[25] 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.[26] 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.[27][28] 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.[29]

In some birds such as white-eyes, the pollen dusted by the plants on the forehead of the birds may increase the wear of these feathers leading to increased moulting and replacement.[30]

Patterns in the evolution of ornithophily

About 7000 neotropical plant species are hummingbird-pollinated[31] in contrast to about 129 species of North American plants that have evolved ornithophilous associations.[32] 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.[33] 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).[34]

Hummingbirds rely on nectar for energy, and ornithophilous flowers need hummingbirds’ assistance with pollination in order to reproduce. While the birds are feeding, pollen sticks to their beaks, which will rub off on the next flower they visit, pollinating it.[35] Over time, the co-dependence on one another causes the co-evolution of pollination syndromes.[36] For example, different species of hummingbirds have differently shaped beaks, presumably to allow them to drink nectar from the flowers around them.[37] It is widely believed that short-billed hummingbirds drink from wider flowers with short petals, and hummingbirds with longer bills have close relationships with flowers with long, narrow corollas. Most of the time, long-billed species have access to both short and long flowers, but they often avoid short flowers to avoid competition.[38] Further, hummingbirds with curved bills will forage at straight-petaled flowers, but  straight-billed birds are less likely to visit curved flowers.[39] Ornithophilous flowers pollinated by hummingbirds often have reproductive structures that are vertically oriented. This creates a favorable upright body position for hummingbirds during feeding, one that allows them to sufficiently flap their wings for hovering.[40] Hummingbirds prefer to visit larger and taller floral displays, and it has been proven and confirmed through many studies that birds prefer flowers with red or pink petals over other colors.[41]

Bird pollination is considered as a costly strategy for plants and it evolves only where there are particular benefits for the plant.[42] 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.[5] 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 much nectar is available and therefore move a lot through the forest. By this activity they often move between nectar-providing plants and provide outcrossing.[43] 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.[43]

Migration and flowering synchrony

Time of flowering is often used to mark the start of spring in temperate climate zones. Recently, studies have consistently found that plants respond to increasing temperatures by flowering earlier.[44] Strong coevolution between hummingbirds and flowers has led to an adaptive specialization outcome in which important behaviors of both hummingbirds and flowers become synchronized. Because hummingbirds depend heavily on nectar, it is very possible that their migration is correlated with the time of flowering of flower species.[45] For specialist hummingbird species, flowering phenology is extremely important for survival during and following fall migration. For example, the migratory route of the S. rufus is linked to the florescence of a unique collection of flower species.[46] S. rufus prefer S. iodantha flowers.[47][46] Studies have found that the presence of S. rufus is coupled with the flowering of S. iodantha in specific locations. Time of flowering is therefore significant for the survival of S. rufus during fall migration. Similarly, peak flowering of Impatiens biflora flowers corresponds to the peak migration time of the Ruby-Throated Hummingbird.[46]

Other associations

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.[48]

See also

References

  1. ↑ "Bird–flower interactions in the Macaronesian islands". J. Biogeogr. 31 (12): 1945–1953. 2004. doi:10.1111/j.1365-2699.2004.01116.x. http://www.biosci.ohio-state.edu/~awolfe/class/Biogeography/Readings/Culver.pdf. Retrieved 2009-04-15. 
  2. ↑ Cotton, Peter A. (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:tbaiob2.0.co;2]. 
  3. ↑ "Reproductive biology of Butea monosperma (Fabaceae)". Annals of Botany 92 (5): 715–23. November 2003. doi:10.1093/aob/mcg193. PMID 14500327. 
  4. ↑ "'Anti-bee' and 'pro-bird' changes during the evolution of hummingbird pollination in Penstemon flowers". Journal of Evolutionary Biology 17 (4): 876–85. July 2004. doi:10.1111/j.1420-9101.2004.00729.x. PMID 15271088. https://www.csun.edu/~hcbio028/JEBCastellanos.pdf. 
  5. ↑ 5.0 5.1 5.2 "Bird-pollinated flowers in an evolutionary and molecular context". Journal of Experimental Botany 59 (4): 715–27. 2008. doi:10.1093/jxb/ern009. PMID 18326865. 
  6. ↑ Grant, Verne (1950). "The Protection of the Ovules in Flowering Plants". Evolution 4 (3): 179–201. doi:10.2307/2405331. 
  7. ↑ Hart, Nathan S; Hunt, David M (2007). Andrew, T.D.Bennett; Marc. eds. "Avian Visual Pigments: Characteristics, Spectral Tuning, and Evolution". The American Naturalist 169 (S1): S7–S26. doi:10.1086/510141. PMID 19426092. https://www.jstor.org/stable/10.1086/510141. 
  8. ↑ Chen, Zhe; Niu, Yang; Liu, Chang-Qiu; Sun, Hang (2020-10-06). "Red flowers differ in shades between pollination systems and across continents" (in en). Annals of Botany 126 (5): 837–848. doi:10.1093/aob/mcaa103. ISSN 0305-7364. PMID 32478385. 
  9. ↑ Irwin, Rebecca E.; Bronstein, Judith L.; Manson, Jessamyn S.; Richardson, Leif (2010-11-02). "Nectar Robbing: Ecological and Evolutionary Perspectives". Annual Review of Ecology, Evolution, and Systematics 41 (1): 271–292. doi:10.1146/annurev.ecolsys.110308.120330. ISSN 1543-592X. https://www.annualreviews.org/doi/10.1146/annurev.ecolsys.110308.120330. 
  10. ↑ 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. 
  11. ↑ "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. 2004. doi:10.1111/j.1095-8339.2004.00329.x. 
  12. ↑ "Evolutionary associations between nectar properties and specificity in bird pollination systems". Biology Letters 4 (1): 49–52. February 2008. doi:10.1098/rsbl.2007.0496. PMID 17999944. 
  13. ↑ "Why are so many bird flowers red?". PLOS Biology 2 (10): e350. October 2004. doi:10.1371/journal.pbio.0020350. PMID 15486585. 
  14. ↑ "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. 2004. doi:10.1111/j.0269-8463.2004.00891.x. 
  15. ↑ "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. 1985. doi:10.1111/j.1095-8339.1985.tb02205.x. 
  16. ↑ "Floret Opening in Banksia menziesii R.Br.; The Importance of Nectarivorous Birds". Australian Journal of Botany 36 (2): 225–232. 1988. doi:10.1071/BT9880225. 
  17. ↑ "Reproductive Phenology of a Tropical Dry Forest in Mudumalai, Southern India". Journal of Ecology 82 (4): 759–767. 1994. doi:10.2307/2261441. 
  18. ↑ "A Remarkable Case of Ornithophily in Calceolaria: Food Bodies as Rewards for a Non-nectarivorous Bird*" (in en). Botanica Acta 109 (2): 172–176. 1996. doi:10.1111/j.1438-8677.1996.tb00558.x. 
  19. ↑ "Bird pollinated plant mixes it up when it comes to sex" (in en-us). https://phys.org/news/2011-09-bird-pollinated-sex.html. 
  20. ↑ "Pollen-connecting threads in Heliconia (Heliconiaceae)". Plant Systematics and Evolution 195 (1): 61–65. 1995. doi:10.1007/BF00982315. 
  21. ↑ "Transfer of pollinaria on birds' feet: a new pollination system in orchids". Plant Systematics and Evolution 244 (3): 181–188. 2004. doi:10.1007/s00606-003-0106-y. 
  22. ↑ "Consumptive emasculation: the ecological and evolutionary consequences of pollen theft". Biological Reviews of the Cambridge Philosophical Society 84 (2): 259–76. May 2009. doi:10.1111/j.1469-185X.2008.00074.x. PMID 19382932. 
  23. ↑ "Floral traits mediate the vulnerability of aloes to pollen theft and inefficient pollination by bees". Annals of Botany 109 (4): 761–72. March 2012. doi:10.1093/aob/mcr324. PMID 22278414. 
  24. ↑ "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)". Acta Oecologica 29 (3): 324–327. 2006. doi:10.1016/j.actao.2005.12.005. Bibcode: 2006AcO....29..324V. http://captura.uchile.cl/dspace/bitstream/2250/2772/1/Valdivia%20CE-Trade.pdf. 
  25. ↑ "Nectar concentration affects sugar preferences in two Australian honeyeaters and a lorikeet". Functional Ecology 22 (4): 599–605. 2008. doi:10.1111/j.1365-2435.2008.01401.x. 
  26. ↑ "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. June 2003. doi:10.1242/jeb.00351. PMID 12728006. 
  27. ↑ "Are hummingbirds facultatively ammonotelic? Nitrogen excretion and requirements as a function of body size". Physiological and Biochemical Zoology 76 (5): 731–43. 2003. doi:10.1086/376917. PMID 14671720. https://works.bepress.com/carlos_delrio/4/download/. 
  28. ↑ "Can birds be ammonotelic? Nitrogen balance and excretion in two frugivores". The Journal of Experimental Biology 208 (Pt 6): 1025–34. March 2005. doi:10.1242/jeb.01495. PMID 15767304. 
  29. ↑ "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. December 2004. doi:10.1242/jeb.01238. PMID 15557024. 
  30. ↑ "Supplementary head molt in Cape White-eyes: a consequence of nectar feeding?". J. Field Ornithol. 67 (3): 358–359. 1995. http://sora.unm.edu/sites/default/files/journals/jfo/v067n03/p0358-p0359.pdf. 
  31. ↑ 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 (2): 333–347. doi:10.1007/s10336-014-1146-5. https://www.zora.uzh.ch/id/eprint/102036/8/ZORA_NL_102036.pdf. 
  32. ↑ "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. October 1994. doi:10.1073/pnas.91.22.10407. PMID 7937964. Bibcode: 1994PNAS...9110407G. 
  33. ↑ "Bird pollination in South African Salvia species". Flora – Morphology, Distribution, Functional Ecology of Plants 201 (5): 396–406. 2006. doi:10.1016/j.flora.2005.07.016. 
  34. ↑ "Passerine pollination of Rhodoleia championii (Hamamelidaceae) in subtropical China". Biotropica 42 (3): 336–341. 2010. doi:10.1111/j.1744-7429.2009.00585.x. 
  35. ↑ kazilek (2014-05-20). "Hummingbird Evolution" (in en). https://askabiologist.asu.edu/hummingbird-evolution. 
  36. ↑ Bruneau, Anne (1997). "Evolution and Homology of Bird Pollination Syndromes in Erythrina (Leguminosae)". American Journal of Botany 84 (1): 54–71. doi:10.2307/2445883. ISSN 0002-9122. 
  37. ↑ Temeles, Ethan J.; Linhart, Yan B.; Masonjones, Michael; Masonjones, Heather D. (2002). [0068:trofwi2.0.co;2 "The Role of Flower Width in Hummingbird Bill Length–Flower Length Relationships1"]. Biotropica 34 (1): 68. doi:10.1646/0006-3606(2002)034[0068:trofwi2.0.co;2]. ISSN 0006-3606. http://dx.doi.org/10.1646/0006-3606(2002)034[0068:trofwi]2.0.co;2. 
  38. ↑ Bergamo, Pedro Joaquim; Wolowski, Marina; Maruyama, Pietro Kiyoshi; Vizentin-Bugoni, Jeferson; Carvalheiro, Luísa G.; Sazima, Marlies (2017-06-12). "The potential indirect effects among plants via shared hummingbird pollinators are structured by phenotypic similarity". Ecology 98 (7): 1849–1858. doi:10.1002/ecy.1859. ISSN 0012-9658. PMID 28402583. http://dx.doi.org/10.1002/ecy.1859. 
  39. ↑ Maglianesi, María A.; Böhning-Gaese, Katrin; Schleuning, Matthias (2014-12-17). "Different foraging preferences of hummingbirds on artificial and natural flowers reveal mechanisms structuring plant-pollinator interactions". Journal of Animal Ecology 84 (3): 655–664. doi:10.1111/1365-2656.12319. ISSN 0021-8790. PMID 25400277. 
  40. ↑ Sapir, Nir; Dudley, Robert (2012-11-21). "Implications of floral orientation for flight kinematics and metabolic expenditure of hover-feeding hummingbirds". Functional Ecology 27 (1): 227–235. doi:10.1111/1365-2435.12024. ISSN 0269-8463. 
  41. ↑ Dudash, Michele R.; Hassler, Cynthia; Stevens, Peter M.; Fenster, Charles B. (February 2011). "Experimental floral and inflorescence trait manipulations affect pollinator preference and function in a hummingbird-pollinated plant". American Journal of Botany 98 (2): 275–282. doi:10.3732/ajb.1000350. ISSN 0002-9122. PMID 21613116. http://dx.doi.org/10.3732/ajb.1000350. 
  42. ↑ "Ecological and Evolutionary Implications of Bird Pollination". American Zoologist 18 (4): 715–727. 1978. doi:10.1093/icb/18.4.715. 
  43. ↑ 43.0 43.1 Abrahamczyk, S. (2019). "Comparison of the ecology and evolution of plants with a generalist bird pollination system between continents and islands worldwide.". Biological Reviews 94 (5): 1658–1671. doi:10.1111/brv.12520. PMID 31050144. 
  44. ↑ Fitter, A. H. (2002-05-31). "Rapid Changes in Flowering Time in British Plants". Science 296 (5573): 1689–1691. doi:10.1126/science.1071617. ISSN 0036-8075. PMID 12040195. Bibcode: 2002Sci...296.1689F. http://dx.doi.org/10.1126/science.1071617. 
  45. ↑ Hegland, Stein Joar; Nielsen, Anders; Lázaro, Amparo; Bjerknes, Anne-Line; Totland, Ørjan (February 2009). "How does climate warming affect plant-pollinator interactions?". Ecology Letters 12 (2): 184–195. doi:10.1111/j.1461-0248.2008.01269.x. ISSN 1461-023X. PMID 19049509. 
  46. ↑ 46.0 46.1 46.2 López-Segoviano, Gabriel; Arenas-Navarro, Maribel; Vega, Ernesto; Arizmendi, Maria del Coro (2018-07-06). "Hummingbird migration and flowering synchrony in the temperate forests of northwestern Mexico". PeerJ 6: e5131. doi:10.7717/peerj.5131. ISSN 2167-8359. PMID 30002968. 
  47. ↑ Arizmendi, María del Coro (2001-06-01). "Multiple ecological interactions: nectar robbers and hummingbirds in a highland forest in Mexico". Canadian Journal of Zoology 79 (6): 997–1006. doi:10.1139/z01-066. ISSN 0008-4301. http://dx.doi.org/10.1139/z01-066. 
  48. ↑ "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. September 2007. doi:10.1093/aob/mcm135. PMID 17638712. 

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