Don’t forget the flies: dipteran diversity and its consequences for floral ecology and evolution
Tóm tắt
The attention of the global pollination community has been drawn to food safety and other ecosystem services provided by pollinators, in light of decline in social bee populations. Despite intensified research on bees, recent studies have revealed important contributions of flies to pollination success, reproductive isolation and floral diversification. Diptera is a highly diverse insect order, comprising over 125,000 described species in 110 families and representing a broad spectrum of ecological niches beyond the well-known agricultural pests and blood-feeding vectors of human and animal diseases. Flies are most appreciated as generalized pollinators in alpine habitats (anthomyiids and tachinids) and as specialized pollinators in brood-site deceptive plants that mimic fungi (drosophilids), feces (muscids) or carrion (sarcophagids and calliphorids). Syrphid and bombyliid flies visit many of the same flowers as bees and butterflies do, but with different impacts on plant fitness. Guilds of South African plants have evolved specialized relationships with long-tongued nemestrinid and tabanid flies, thanks to geographic isolation and climatic stability. Studies in Japan highlight the evolution of another plant guild, pollinated by sciarid and mycetophilid fungus gnats, whereas Zygothrica flies (Drosophilidae) pollinate mushroom-like Dracula orchids in Andean cloud forests.
Tài liệu tham khảo
Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19:915–918. https://doi.org/10.1111/gcb.14736
Anderson B, Johnson SD (2009) Geographical covariation and local convergence of flower depth in a guild of fly-pollinated plants. New Phytol 182:533–540. https://doi.org/10.1111/j.1469-8137.2009.02764.x
Angioy AM, Stensmyr MC, Urru I, Puliafito M, Collu I, Hansson BS (2004) Function of the heater: the dead horse arum revisited. P Roy SocB-Biol Sci 271:S13–S15. https://doi.org/10.1098/rsbl.2003.0111
Bartomeus I, Ascher JS, Wagner D, Danforth BN, Colla S, Kornbluth S, Winfree R (2011) Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proc Natl Acad Sci USA 108:20645–20649. https://doi.org/10.1073/pnas.1115559108
Berjano R, Ortiz PL, Arista M, Talavera S (2009) Pollinators, flowering phenology and floral longevity in two Mediterranean Aristolochia species, with a review of flower visitor records for the genus. Plant Biol 11:6–16. https://doi.org/10.1111/j.1438-8677.2008.00131.x
Bernhardt P (2000) Convergent evolution and adaptive radiation of beetle-pollinated angiosperms. In: Dafni A, Hesse M, Pacini E (eds) Pollen and pollination. Springer, Vienna, pp 293–320. https://doi.org/10.1007/978-3-7091-6306-1_16
Blanco MA, Barboza G (2005) Pseudocopulatory pollination in Lepanthes (Orchidaceae: Pleurothallidinae) by fungus gnats. Ann Bot Lond 95:763–772. https://doi.org/10.1093/aob/mci090
Bogarín D, Fernández M, Borkent A, Heemskerk A, Pupulin F, Ramírez S, Smets E, Gravendeel B (2018) Pollination of Trichosalpinx (Orchidaceae: Pleurothallidinae) by biting midges (Diptera: Ceratopogonidae). Bot J Linn Soc 186:510–543. https://doi.org/10.1093/botlinnean/box087
Borba EL, Semir J (1998) Wind assisted fly pollination in three Bulbophyllum (Orchidaceae) species occurring in the Brazilian Campos Rupestres. Lindleyana 13:203–218
Borba EL, Semir J (2001) Pollinator specificity and convergence in fly-pollinated Pleurothallis (Orchidaceae) species: a multiple population approach. Ann Bot Lond 88:75–88. https://doi.org/10.1006/anbo.2001.1434
Bower CC, Towle B, Bickel D (2015) Reproductive success and pollination of the Tuncurry midge orchid (Genoplesium littorale)(Orchidaceae) by chloropid flies. Telopea 18:43–55
Buchmann SL, Nabhan GP (1996) The forgotten pollinators. Island Press, Washington
Burgess KS, Singfield J, Melendez V, Kevan PG (2004) Pollination biology of Aristolochia grandiflora (Aristolochiaceae) in Veracruz, Mexico. Ann MO Bot Gard 91:346–356. https://www.jstor.org/stable/3298612
Chartier M, Gibernau M, Renner SS (2014) The evolution of pollinator—plant interaction types in the Araceae. Evolution 68:1533–1543. https://doi.org/10.1111/evo.12318
Ellis AG, Johnson SD (2010) Floral mimicry enhances pollen export: the evolution of pollination by sexual deceit outside of the Orchidaceae. Am Nat 176: E143–E151. https://www.journals.uchicago.edu/doi/full/10.1086/656487
Endara L, Grimaldi D, Roy BA (2010) Lord of the flies: pollination of Dracula orchids. Lankesteriana 10:1–11
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol S 35:375–403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347
Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Harder LD, Afik O, Bartomeus I et al (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611. https://doi.org/10.1126/science.1230200
Gervasi DD, Schiestl FP (2017) Real-time divergent evolution in plants driven by pollinators. Nat Commun 8:14691. https://www.nature.com/articles/ncomms14691
Goldblatt P, Manning JC (2000) The long-proboscid fly pollination system in Southern Africa. Ann Mo Bot Gard 87:146–170. https://doi.org/10.2307/2666158
Goulson D, Wright NP (1998) Flower constancy in the hoverflies Episyrphus balteatus (Degeer) and Syrphus ribesii (L.)(Syrphidae). Behav Ecol 9:213–219. https://doi.org/10.1093/beheco/9.3.213
Grant V, Grant KA (1965) Flower pollination in the Phlox family. Columbia University Press, New York, p 224
Hansen DM, Van der Niet T, Johnson SD (2011) Floral signposts: testing the significance of visual ‘nectar guides’ for pollinator behaviour and plant fitness. P Roy Soc B-Biol Sci 279:634–639. https://doi.org/10.1098/rspb.2011.1349
Heiduk A, Kong H, Brake I, von Tschirnhaus M, Tolasch T, Tröger A, Wittenberg E, Francke W, Meve U, Dötterl S (2015) Deceptive Ceropegia dolichophylla fools its kleptoparasitic fly pollinators with exceptional floral scent. Front Ecol Evol 3:66. https://doi.org/10.3389/fevo.2015.00066
Hetherington-Rauth MC, Ramírez SR (2016) Evolution and diversity of floral scent chemistry in the euglossine bee-pollinated orchid genus Gongora. Ann Bot London 118:135–148. https://doi.org/10.1093/aob/mcw072
Hossaert-McKey M, Soler C, Schatz B, Proffit M (2010) Floral scents: their roles in nursery pollination mutualisms. Chemoecology 20:75–88. https://doi.org/10.1007/s00049-010-0043-5
Ibanez S, Dötterl S, Anstett MC, Baudino S, Caissard JC, Gallet C, Després L (2010) The role of volatile organic compounds, morphology and pigments of globeflowers in the attraction of their specific pollinating flies. New Phytol 188:451–463. https://doi.org/10.1111/j.1469-8137.2010.03317.x
Inouye DW, Larson BM, Ssymank A, Kevan PG (2015) Flies and flowers III: ecology of foraging and pollination. J Pollinat Ecol 16:115–133. https://doi.org/10.26786/1920-7603%282015%2915
Jandér KC, Herre EA (2010) Host sanctions and pollinator cheating in the fig tree—fig wasp mutualism. P Roy Soc B-Biol Sci 277:1481–1488. https://doi.org/10.1098/rspb.2009.2157
Jauker F, Wolters V (2008) Hover flies are efficient pollinators of oilseed rape. Oecologia 156:819. https://doi.org/10.1007/s00442-008-1034-x
Jersáková J, Johnson SD (2006) Lack of floral nectar reduces self-pollination in a fly-pollinated orchid. Oecologia 147:60–68. https://doi.org/10.1007/s00442-005-0254-6
Jogesh T, Zangerl A, Stanley M, Berenbaum M (2014) Implications of enemy escape on chemically mediated interactions with mutualists: wild parsnip pollination in two hemispheres. J Pollinat Ecol 11:57–67. https://doi.org/10.26786/1920-7603%282013%296
Johnson SD, Dafni A (1998) Response of bee-flies to the shape and pattern of model flowers: implications for floral evolution in a Mediterranean herb. Funct Ecol 12:289–297. https://doi.org/10.1046/j.1365-2435.1998.00175.x
Johnson SD, Midgley JJ (1997) Fly pollination of Gorteria diffusa (Asteraceae), and a possible mimetic function for dark spots on the capitulum. Am J Bot 84:429–436. https://doi.org/10.2307/2446018
Johnson SD, Morita S (2006) Lying to Pinocchio: floral deception in an orchid pollinated by long-proboscid flies. Bot J Linn Soc 152:271–278. https://doi.org/10.1111/j.1095-8339.2006.00571.x
Johnson SD, Schiestl FP (2016) Floral mimicry. Oxford University Press, Oxford, UK
Johnson SD, Steiner KE (1997) Long-tongued fly pollination and evolution of floral spur length in the Disa draconis complex (Orchidaceae). Evolution 51:45–53. https://doi.org/10.1111/j.1558-5646.1997.tb02387.x
Johnson SD, Hargreaves AL, Brown M (2006) Dark, bitter-tasting nectar functions as a filter of flower visitors in a bird-pollinated plant. Ecology 87:2709–2716. https://doi.org/10.1890/0012-9658(2006)87%5b2709:DBNFAA%5d2.0.CO;2
Jürgens A, Wee SL, Shuttleworth A, Johnson SD (2013) Chemical mimicry of insect oviposition sites: a global analysis of convergence in angiosperms. Ecol Lett 16:1157–1167. https://doi.org/10.1111/ele.12152
Kearns CA (1992) Anthophilous fly distribution across an elevation gradient. Am Midl Nat 127:172–182. https://doi.org/10.2307/2426332
Larson BMH, Kevan PG, Inouye DW (2001) Flies and flowers: taxonomic diversity of anthophiles and pollinators. Can Entomol 133:439–465. https://doi.org/10.4039/Ent133439-4
Lunau K (2014) Visual ecology of flies with particular reference to colour vision and colour preferences. J Comp Physiol A 200:497–512. https://doi.org/10.1007/s00359-014-0895-1
Lunau K, Wacht S (1994) Optical releasers of the innate proboscis extension in the hoverfly Eristalis tenax L. (Syrphidae, Diptera). J Comp Physiol A 174:575–579. https://doi.org/10.1007/BF00217378
Martel C, Cairampoma L, Stauffer FW, Ayasse M (2016) Telipogon peruvianus (Orchidaceae) flowers elicit pre-mating behaviour in Eudejeania (Tachinidae) males for pollination. PLoS One 11:e0165896. https://doi.org/10.1371/journal.pone.0165896
Martel C, Francke W, Ayasse M (2019) The chemical and visual basis in the pollination of the neotropical sexually deceptive orchid Telipogon peruvianus (Orchidaceae). New Phytol 223:1989–2001. https://doi.org/10.1111/nph.15902
Martos F, Cariou ML, Pailler T, Fournel J, Bytebier B, Johnson SD (2015) Chemical and morphological filters in a specialized floral mimicry system. New Phytol 207:225–234. https://doi.org/10.1111/nph.13350
Meve U, Liede S (1994) Floral biology and pollination in stapeliads—new results and a literature review. Pl Syst Evol 192:99–116. https://doi.org/10.1007/BF00985911
Miller TJ, Raguso RA, Kay KM (2013) Novel adaptation to hawkmoth pollinators in Clarkia reduces efficiency, not attraction of diurnal visitors. Ann Bot Lond 113:317–329. https://doi.org/10.1093/aob/mct237
Mitra B, Banerjee D (2007) Fly pollinators: assessing their value in biodiversity conservation and food security in India. Rec Zool Surv India 107:33–48
Miyake T, Yafuso M (2003) Floral scents affect reproductive success in fly-pollinated Alocasia odora (Araceae). Am J Bot 90:370–376. https://doi.org/10.3732/ajb.90.3.370
Mochizuki K, Kawakita A (2017) Pollination by fungus gnats and associated floral characteristics in five families of the Japanese flora. Ann Bot London 121:651–663. https://doi.org/10.1093/aob/mcx196
Nakahira M, Ono H, Wee SL, Tan KH, Nishida R (2018) Floral synomone diversification of Bulbophyllum sibling species (Orchidaceae) in attracting fruit fly pollinators. BiochemSyst Ecol 81:86–95. https://doi.org/10.1016/j.bse.2018.10.002
Nordström K, Dahlbom J, Pragadheesh VS, Ghosh S, Olsson A, Dyakova O, Suresh SK, Olsson SB (2017) In situ modeling of multimodal floral cues attracting wild pollinators across environments. Proc Nat Acad Sci USA 114:13218–13223. https://doi.org/10.1073/pnas.1714414114
Oelschlägel B, Nuss M, von Tschirnhaus M, Pätzold C, Neinhuis C, Dötterl S, Wanke S (2015) The betrayed thief–the extraordinary strategy of Aristolochia rotunda to deceive its pollinators. New Phytol 206:342–351. https://doi.org/10.1111/nph.13210
Okamoto T, Okuyama Y, Goto R, Tokoro M, Kato M (2015) Parallel chemical switches underlying pollinator isolation in Asian Mitella. J Evolution Biol 28:590–600. https://doi.org/10.1111/jeb.12591
Ollerton J, Dötterl S, Ghorpadé K, Heiduk A, Liede-Schumann S, Masinde S, Meve U, Peter CI, Prieto-Benítez S, Punekar S, Thulin M (2017) Diversity of Diptera families that pollinate Ceropegia (Apocynaceae) trap flowers: an update in light of new data and phylogenetic analyses. Flora 234:233–244. https://doi.org/10.1016/j.flora.2017.07.013
Orford KA, Vaughan IP, Memmott J (2015) The forgotten flies: the importance of non-syrphid Diptera as pollinators. P R Soc B-Biol Sci 282:20142934. https://doi.org/10.1098/rspb.2014.2934
Patt JM, French JC, Schal C, Lech J, Hartman TG (1995) The pollination biology of Tuckahoe, Peltandra virginica (Araceae). Am J Bot 82:1230–1240. https://doi.org/10.1002/j.1537-2197.1995.tb12656.x
Pellmyr O, Thien LB (1986) Insect reproduction and floral fragrances: keys to the evolution of the angiosperms? Taxon 35:76–85. https://doi.org/10.2307/1221036
Policha T, Davis A, Barnadas M, Dentinger BT, Raguso RA, Roy BA (2016) Disentangling visual and olfactory signals in mushroom-mimicking Dracula orchids using realistic three-dimensional printed flowers. New Phytol 210:1058–1071. https://doi.org/10.1111/nph.13855
Policha T, Grimaldi DA, Manobanda R, Troya A, Ludden A, Dentinger BT, Roy BA (2019) Dracula orchids exploit guilds of fungus visiting flies: new perspectives on a mushroom mimic. Ecol Entomol 44:457–470. https://doi.org/10.1111/een.12720
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007
Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD, Dicks LV, Garibaldi LA, Hill R, Settele J, Vanbergen AJ (2016) Safeguarding pollinators and their values to human well-being. Nature 540:220–229. https://doi.org/10.1038/nature20588
Rader R, Edwards W, Westcott DA, Cunningham SA, Howlett BG (2013) Diurnal effectiveness of pollination by bees and flies in agricultural Brassica rapa: Implications for ecosystem resilience. Basic Appl Ecol 14:20–27. https://doi.org/10.1016/j.baae.2012.10.011
Rader R, Bartomeus I, Garibaldi LA, Garratt MP, Howlett BG, Winfree R, Cunningham SA, Mayfield MM, Arthur AD, Andersson GK, Bommarco R et al (2016) Non-bee insects are important contributors to global crop pollination. Proc Nat Acad Sci USA 113:146–151. https://doi.org/10.1073/pnas.1517092112
Rader R, Cunningham SA, Howlett BG, Inouye DW (2019) Non-bee insects as visitors and pollinators of crops: biology, ecology and management. Annu Rev Entomol 65:20.1–20.17. https://doi.org/10.1146/annurev-ento-011019-025055
Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol S 39:549–569. https://doi.org/10.1146/annurev.ecolsys.38.091206.095601
Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515. https://doi.org/10.1111/j.1461-0248.2008.01157.x
Sakai S (2002) A review of brood-site pollination mutualism: plants providing breeding sites for their pollinators. J Plant Res 115:0161–0168. https://doi.org/10.1007/s102650200
Sakai S, Kato M, Nagamasu H (2000) Artocarpus (Moraceae)–gall midge pollination mutualism mediated by a male-flower parasitic fungus. Am J Bot 87:440–445. https://doi.org/10.2307/2656640
Saunders ME, Rader R (2019) Network modularity influences plant reproduction in a mosaic tropical agroecosystem. P Roy Soc B-Biol Sci 286:20190296. https://doi.org/10.1098/rspb.2019.0296
Schiestl FP (2017) Innate receiver bias: its role in the ecology and evolution of plant—animal interactions. Ann Rev Ecol Evol S 48:585–603. https://doi.org/10.1146/annurev-ecolsys-110316-023039
Shuttleworth A, Johnson SD, Jürgens A (2017) Entering through the narrow gate: a morphological filter explains specialized pollination of a carrion-scented stapeliad. Flora 232:92–103. https://doi.org/10.1016/j.flora.2016.09.003
Spaethe J, Moser WH, Paulus HF (2007) Increase of pollinator attraction by means of a visual signal in the sexually deceptive orchid, Ophrys heldreichii (Orchidaceae). Pl Syst Evol 264:31–40. https://doi.org/10.1007/s00606-006-0503-0
Ssymank A, Kearns CA, Pape T, Thompson FC (2008) Pollinating flies (Diptera): a major contribution to plant diversity and agricultural production. Biodiversity 9:86–89. https://doi.org/10.1080/14888386.2008.9712892
Stökl J, Strutz A, Dafni A, Svatos A, Doubsky J, Knaden M, Sachse S, Hansson BS, Stensmyr MC (2010) A deceptive pollination system targeting drosophilids through olfactory mimicry of yeast. Curr Biol 20:1846–1852. https://doi.org/10.1016/j.cub.2010.09.033
Stökl J, Brodmann J, Dafni A, Ayasse M, Hansson BS (2011) Smells like aphids: orchid flowers mimic aphid alarm pheromones to attract hoverflies for pollination. P R Soc B-Biol Sci 278:1216–1222. https://doi.org/10.1098/rspb.2010.1770
Tan KH, Nishida R (2000) Mutual reproductive benefits between a wild orchid, Bulbophyllum patens, and Bactrocera fruit flies via a floral synomone. J Chem Ecol 26:533–546. https://doi.org/10.1023/A:1005477926244
Thompson JN, Cunningham BM (2002) Geographic structure and dynamics of coevolutionary selection. Nature 417:735–738. https://doi.org/10.1038/nature00810
Thompson JN, Pellmyr O (1992) Mutualism with pollinating seed parasites amid co-pollinators: constraints on specialization. Ecology 73:1780–1791. https://doi.org/10.2307/1940029
Urru I, Stensmyr MC, Hansson BS (2011) Pollination by brood-site deception. Phytochemistry 72:1655–1666. https://doi.org/10.1016/j.phytochem.2011.02.014
van der Pijl L, Dodson CH (1966) Orchid flowers: their pollination and evolution. Fairchild Tropical Garden and Miami University Press, Coral Gables
Wiegmann BM, Trautwein MD, Winkler IS, Barr NB, Kim JW, Lambkin C, Bertone MA, Cassel BK, Bayless KM, Heimberg AM, Wheeler BM et al (2011) Episodic radiations in the fly tree of life. Proc Nat Acad Sci USA 108:5690–5695. https://doi.org/10.1073/pnas.1012675108
Woodcock TS, Larson BM, Kevan PG, Inouye DW, Lunau K (2014) Flies and flowers II: floral attractants and rewards. J Pollinat Ecol 12:63–94. https://doi.org/10.26786/1920-7603%282014%295
Zimmermann Y, Ramírez SR, Eltz T (2009) Chemical niche differentiation among sympatric species of orchid bees. Ecology 90:2994–3008. https://doi.org/10.1890/08-1858.1