Evidence of introduced honeybees (Apis mellifera) as pollen wasters in orchid pollination.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
18 Jun 2024
Historique:
received: 03 04 2024
accepted: 06 06 2024
medline: 19 6 2024
pubmed: 19 6 2024
entrez: 18 6 2024
Statut: epublish

Résumé

Biological invasions threaten global biodiversity, altering landscapes, ecosystems, and mutualistic relationships like pollination. Orchids are one of the most threatened plant families, yet the impact of invasive bees on their reproduction remains poorly understood. We conduct a global literature survey on the incidence of invasive honeybees (Apis mellifera) on orchid pollination, followed by a study case on Australian orchids. Our literature survey shows that Apis mellifera is the primary alien bee visiting orchids worldwide. However, in most cases, introduced honeybees do not deposit orchid pollen. We also test the extent to which introduced honeybees affect orchid pollination using Diuris brumalis and D. magnifica. Diuris brumalis shows higher fruit set and pollination in habitats with both native and invasive bees compared to habitats with only introduced bees. Male and female reproductive success in D. magnifica increases with native bee abundance, while conversely pollinator efficiency decreases with honeybee abundance and rises with habitat size. Our results suggest that introduced honeybees are likely involved in pollen removal but do not effectively deposit orchid pollen, acting as pollen wasters. However, Apis mellifera may still contribute to pollination of Diuris where native bees no longer exist. Given the global occurrence of introduced honeybees, we warn that certain orchids may suffer from pollen depletion by these invaders, especially in altered habitats with compromised pollination communities.

Identifiants

pubmed: 38890342
doi: 10.1038/s41598-024-64218-x
pii: 10.1038/s41598-024-64218-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

14076

Subventions

Organisme : Endeavor Fellowship Program
ID : [5117_2016]
Organisme : Short Mobility Program
ID : D.M. 976_2017
Organisme : Talent Young Scientist Program of Yunnan Province
ID : YNWRQNBJ-2019-055

Informations de copyright

© 2024. The Author(s).

Références

Bellard, C., Cassey, P. & Blackburn, T. M. Alien species as a driver of recent extinctions. Biol. Lett. 12, 20150623. https://doi.org/10.1098/rsbl.2015.0623 (2016).
doi: 10.1098/rsbl.2015.0623 pubmed: 26888913 pmcid: 4780541
Traveset, A. & Richardson, D. M. Mutualistic interactions and biological invasions. Ann. Rev. Ecol. Evol. Syst. 45, 89–113. https://doi.org/10.1146/annurev-ecolsys-120213-091857 (2014).
doi: 10.1146/annurev-ecolsys-120213-091857
Agüero, J. I., Pérez-Méndez, N., Torretta, J. P. & Garibaldi, L. A. Impact of invasive bees on plant-pollinator interactions and reproductive success of plant species in mixed Nothofagus Antarctica forests. Neotrop. Entomol. 49, 557–567. https://doi.org/10.1007/s13744-020-00787-6 (2020).
doi: 10.1007/s13744-020-00787-6 pubmed: 32734552
Goulson, D. Effects of introduced bees on native ecosystems. Ann. Rev. Ecol. Evol. Syst. 34, 1–26. https://doi.org/10.1146/annurev.ecolsys.34.011802.132355 (2003).
doi: 10.1146/annurev.ecolsys.34.011802.132355
Agüero, J. I. et al. Impactos de la abeja melífera sobre plantas y abejas silvestres en hábitats naturales. Ecosistemas 27, 60–69. https://doi.org/10.7818/ECOS.1365 (2018).
doi: 10.7818/ECOS.1365
Thomson, D. M. & Page, M. L. The importance of competition between insect pollinators in the Anthropocene. Curr. Opin. Insect Sci. 38, 55–62. https://doi.org/10.1016/j.cois.2019.11.001 (2020).
doi: 10.1016/j.cois.2019.11.001 pubmed: 32145696
Thomson, D. Competitive interactions between the invasive European honeybee and native bumble bees. Ecology 85, 458–470. https://doi.org/10.1890/02-0626 (2004).
doi: 10.1890/02-0626
Paini, D. R. & Roberts, J. D. Commercial honey bees (Apis mellifera) reduce the fecundity of an Australian native bee (Hylaeus alcyoneus). Biol. Conserv. 123, 103–112. https://doi.org/10.1016/j.biocon.2004.11.001 (2005).
doi: 10.1016/j.biocon.2004.11.001
Hudewenz, A. & Klein, A. M. Red mason bees cannot compete with honeybees for floral resources in a cage experiment. Ecol. Evol. 5, 5049–5056. https://doi.org/10.1002/ece3.1762 (2015).
doi: 10.1002/ece3.1762 pubmed: 26640681 pmcid: 4662317
Dohzono, I. & Yokoyama, J. Impacts of alien bees on native plant-pollinator relationships: A review with special emphasis on plant reproduction. Appl. Entomol. Zool. 45, 37–47. https://doi.org/10.1303/aez.2010.37 (2010).
doi: 10.1303/aez.2010.37
Do Carmo, R. M., Franceschinelli, E. V. & da Silveira, F. A. Introduced honeybees (Apis mellifera) reduce pollination success without affecting the floral resource taken by native pollinators. Biotropica 36, 371–376. https://doi.org/10.1111/j.1744-7429.2004.tb00329.x (2004).
doi: 10.1111/j.1744-7429.2004.tb00329.x
Marrero, H. J., Medan, D., Zarlavsky, G. E. & Torretta, J. P. Agricultural land management negatively affects pollination service in Pampean agro-ecosystems. Agric Ecosyst. Environ. 218, 28–32. https://doi.org/10.1016/j.agee.2015.10.024 (2016).
doi: 10.1016/j.agee.2015.10.024
Herrera, C. M. Gradual replacement of wild bees by honeybees in flowers of the Mediterranean Basin over the last 50 years. Proc. R. Soc. B 287, 20192657. https://doi.org/10.1098/rspb.2019.2657 (2020).
doi: 10.1098/rspb.2019.2657 pubmed: 32097590 pmcid: 7062015
Page, M. L. & Williams, N. M. Honey bee introductions displace native bees and decrease pollination of a native wildflower. Ecology 104, e3939. https://doi.org/10.1002/ecy.3939 (2022).
doi: 10.1002/ecy.3939
Ollerton, J. et al. Overplaying the role of honeybees as pollinators: A comment on Aebi and Neumann. Trends Ecol. Evol. 27, 141–142. https://doi.org/10.1016/j.tree.2011.12.001 (2012).
doi: 10.1016/j.tree.2011.12.001 pubmed: 22209078
Page, M. L. et al. A meta-analysis of single visit pollination effectiveness comparing honeybees and other floral visitors. Am. J. Bot. 108, 2196–2207. https://doi.org/10.1002/ajb2.1764 (2021).
doi: 10.1002/ajb2.1764 pubmed: 34622948
Lomov, B., Keith, D. A. & Hochuli, D. F. Pollination and plant reproductive success in restored urban landscapes dominated by a pervasive exotic pollinator. Landsc. Urban Plan. 96, 232–239. https://doi.org/10.1016/j.landurbplan.2010.03.009 (2010).
doi: 10.1016/j.landurbplan.2010.03.009
Hanna, C., Foote, D. & Kremen, C. Invasive species management restores a plant–pollinator mutualism in Hawaii. J Appl. Ecol. 50, 147–155. https://doi.org/10.1111/1365-2664.12027 (2013).
doi: 10.1111/1365-2664.12027
Dick, W. C. Genetic rescue of remnant tropical trees by an alien pollinator. Proc. R. Soc. B 268, 2391–2396. https://doi.org/10.1098/rspb.2001.1781 (2001).
doi: 10.1098/rspb.2001.1781 pubmed: 11703880 pmcid: 1088891
Van der Pijl, L. & Dodson, H. Orchid Flowers: Their Pollination and Evolution 1st edn. (The Fairchild Tropical Garden and the University of Miami Press, Coral Gable, 1966).
Dressler, R. L. The Orchids: Natural History and Classification (Harvard University Press, Cambridge, 1981).
Dafni, A. Mimicry and deception in pollination. Ann. Rev. Ecol. Evol. Syst. 15, 259–278. https://doi.org/10.1146/annurev.es.15.110184.001355 (1984).
doi: 10.1146/annurev.es.15.110184.001355
Schiestl, F. P. On the success of a swindle: pollination by deception in orchids. Sci. Nat. 92, 255–264. https://doi.org/10.1007/s00114-005-0636-y (2005).
doi: 10.1007/s00114-005-0636-y
Jersáková, J., Johnson, S. D. & Kindlmann, P. Mechanisms and evolution of deceptive pollination in orchids. Biol. Rev. 81, 219–235. https://doi.org/10.1017/S1464793105006986 (2006).
doi: 10.1017/S1464793105006986 pubmed: 16677433
Shrestha, M., Dyer, A. G., Dorin, A., Ren, Z. X. & Burd, M. Rewardlessness in orchids: How frequent and how rewardless?. Plant Biol. 22, 555–561. https://doi.org/10.1111/plb.13113 (2020).
doi: 10.1111/plb.13113 pubmed: 32181557
Ackerman, J. D. et al. Beyond the various contrivances by which orchids are pollinated: global patterns in orchid pollination biology. Bot. J. Linn. Soc. 202, 295–324. https://doi.org/10.1093/botlinnean/boac082 (2023).
doi: 10.1093/botlinnean/boac082
Scopece, G., Cozzolino, S., Johnson, S. D. & Schiestl, F. P. Pollination efficiency and the evolution of specialized deceptive pollination systems. Am. Nat. 175, 98–105. https://doi.org/10.1086/648555 (2010).
doi: 10.1086/648555 pubmed: 19909087
Brundrett, M. Identification and Ecology of Southwest Australian Orchids (Western Australian Naturalists’ Club Inc, Perth, 2014).
Johnson, S. D. & Edwards, T. J. The structure and function of orchid pollinaria. Plant Syst. Evol. 222, 243–269. https://doi.org/10.1007/BF00984105 (2000).
doi: 10.1007/BF00984105
Johnson, S. D., Peter, C. I. & Ågren, J. The effects of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio. Proc. R. Soc. B 271, 803–809. https://doi.org/10.1098/rspb.2003.2659 (2004).
doi: 10.1098/rspb.2003.2659 pubmed: 15255098 pmcid: 1691667
Tremblay, R. L., Ackerman, J. D., Zimmerman, J. K. & Calvo, R. N. Variation in sexual reproduction in orchids and its evolutionary consequences: A spasmodic journey to diversification. Biol. J. Linn. Soc. 84, 1–54. https://doi.org/10.1515/biorc-2015-0024 (2005).
doi: 10.1515/biorc-2015-0024
Cozzolino, S. et al. Evidence for pollinator sharing in Mediterranean nectar-mimic orchids: absence of premating barriers?. Proc. R. Soc. B 272, 1271–1278. https://doi.org/10.1098/rspb.2005.3069 (2005).
doi: 10.1098/rspb.2005.3069 pubmed: 16024392 pmcid: 1564100
Schemske, D. W. Evolution of floral display in the orchid Brassavola nodosa. Evolution 1, 489–493. https://doi.org/10.1111/j.1558-5646.1980.tb04838.x (1980).
doi: 10.1111/j.1558-5646.1980.tb04838.x
Ackerman, J. D. & Montalvo, A. M. Short-and long-term limitations to fruit production in a tropical orchid. Ecology 71, 263–272. https://doi.org/10.2307/1940265 (1990).
doi: 10.2307/1940265
Li, P., Huang, B. Q., Pemberton, R. W., Luo, Y. B. & Cheng, J. Floral display influences male and female reproductive success of the deceptive orchid Phaius delavayi. Plant Syst. Evol. 296, 21–27 (2011).
doi: 10.1007/s00606-011-0473-8
Scaccabarozzi, D. et al. Masquerading as pea plants: Behavioural and morphological evidence for mimicry of multiple models in an Australian orchid. Ann. Bot. 122, 1061–1073. https://doi.org/10.1093/aob/mcy166 (2018).
doi: 10.1093/aob/mcy166 pubmed: 30184161 pmcid: 6266105
Scaccabarozzi, D., Galimberti, A., Dixon, K. W. & Cozzolino, S. Rotating arrays of orchid flowers: a simple and effective method for studying pollination in food deceptive plants. Diversity 12, 286. https://doi.org/10.3390/d12080286 (2020).
doi: 10.3390/d12080286
Scaccabarozzi, D. et al. Ecological factors driving pollination success in an orchid that mimics a range of Fabaceae. Bot. J. Linn. Soc. 194, 253–269. https://doi.org/10.1093/botlinnean/boaa039 (2020).
doi: 10.1093/botlinnean/boaa039
Ackerman, J. D. Island invasions by introduced honeybees: What can be expected for Puerto Rico and the Caribbean?. Front. Ecol. Evol. 8, 556744. https://doi.org/10.3389/fevo.2020.556744 (2021).
doi: 10.3389/fevo.2020.556744
Sugiura, N. Pollination and floral ecology of Arundina graminifolia (Orchidaceae) at the northern border of the species’ natural distribution. J. Plant Res. 127, 131–139. https://doi.org/10.1007/s10265-013-0587-x (2014).
doi: 10.1007/s10265-013-0587-x pubmed: 23917792
Sugiura, N. The pollination ecology of Bletilla striata (Orchidaceae). Ecol. Res. 10, 171–177. https://doi.org/10.1007/BF02347939 (1995).
doi: 10.1007/BF02347939
Ogawa, Y. & Miyake, T. How do rewardless Bletilla striata flowers attract pollinators to achieve pollination?. Plant Syst. Evol. 306, 78. https://doi.org/10.1007/s00606-020-01709-0 (2020).
doi: 10.1007/s00606-020-01709-0
Sanguinetti, A. & Singer, R. B. Invasive bees promote high reproductive success in Andean orchids. Biol. Conserv. 175, 10–20. https://doi.org/10.1016/j.biocon.2014.04.011 (2014).
doi: 10.1016/j.biocon.2014.04.011
Adams, P. B. & Lawson, S. D. Pollination in Australian Orchids: A Critical-Assessment of the Literature 1882–1992. Aust. J. Bot. 41, 553–575. https://doi.org/10.1071/BT9930553 (1993).
doi: 10.1071/BT9930553
Brundrett, M., Ladd, P. & Keighery, G. Pollination strategies are exceptionally complex in Southwestern Australia—A globally significant ancient biodiversity hotspot. Aust. J. Bot. 72, 1–70 (2024).
doi: 10.1071/BT23007
Luer, C. A. The Native Orchids of the United States and Canada Excluding Florida (New York Botanical Garden, New York, 1975).
Argue, G. L. The Pollination Biology of North American Orchids Vol. 2 (Springer, New York, 2012).
doi: 10.1007/978-1-4614-0622-8
Thien, L. B. & Marcks, B. G. The floral biology of Arethusa bulbosa, Calopogon tuberosus and Pogonia ophioglossoides (Orchidaceae). Can. J. Bot. 50, 2319–2325 (1972).
doi: 10.1139/b72-300
Heinrich, B. Bumblebee Economics (Harvard University Press, Cambridge, 1979).
Gregg, K. B. Reproductive biology of the orchid Cleistes divaricata (L.) Ames var. bifaria growing in a West Virginia meadow. Castañea 54, 57–78 (1989).
Gregg, K. B. Reproductive strategy of Cleistes divaricata (Orchidaceae). Am. J. Bot. 78, 350–360 (1991).
doi: 10.1002/j.1537-2197.1991.tb15197.x
Attri, L. K. & Kant, R. Orchid Pollination: An observation on pollination-pollinator interaction in Cymbidium pendulum (Sw.) Roxb.. Curr. Bot. 2, 05–08 (2011).
Verma, J. et al. Pollination in Cymbidium pendulum (Roxb.) Sw. (Orchidaceae). Vegetos 25, 298–302 (2012).
Sugiura, N., Fujie, T., Inoue, K. & Kitamura, K. Flowering phenology, pollination, and fruit set of Cypripedium macranthos var. rebunense, a threatened Lady’s Slipper (Orchidaceae). J. Plant Res. 114, 171–176 (2001).
doi: 10.1007/PL00013980
Sugiura, N., Goubara, M., Kitamura, K. & Inoue, K. Bumblebee pollination of Cypripedium macranthos var. rebunense (Orchidaceae); a possible case of floral mimicry of Pedicularis schistostegia (Orobanchaceae). Plant Syst. Evol. 235, 189–195 (2002).
doi: 10.1007/s00606-002-0229-6
Pearn, M. A. Pollination and comparative reproductive success of lady's slipper orchids Cypripedium candidum, C. parviflorum, and their hybrids in southern Manitoba. Dissertation (University of Manitoba, 2013).
Grantham, M. A., Ford, B. A. & Worley, A. C. Pollination and fruit set in two rewardless slipper orchids and their hybrids (Cypripedium, Orchidaceae): Large yellow flowers outperform small white flowers in the northern tall grass prairie. Plant Biol. 21, 997–1007. https://doi.org/10.1111/plb.13026 (2019).
doi: 10.1111/plb.13026 pubmed: 31276285
Edens-Meier, R., Arduser, M., Westhus, E. & Bernhardt, P. Pollination ecology of Cypripedium reginae Walter (Orchidaceae): Size matters. Telopea 13, 327–340 (2011).
doi: 10.7751/telopea20116024
Miranda-Molina, Y. M., Gonzalez, E. J., Marquez-Guzman, J., Meave, J. A. & Perez-Garcia, E. A. Pollination success in three tropical dry forest orchid species from Mexico: insights from floral display, visitation rates, and flower micromorphology. Bot. Sci. 99, 771–790. https://doi.org/10.17129/botsci.2785 (2021).
doi: 10.17129/botsci.2785
Liu, H. & Pemberton, R. Pollination of an invasive orchid, Cyrtopodium polyphyllum (Orchidaceae), by an invasive oil-collecting bee, Centris nitida, in southern Florida. Botany 88, 290–295. https://doi.org/10.1139/B10-017 (2010).
doi: 10.1139/B10-017
Pansarin, L. M., Pansarin, E. R. & Sazima, M. Reproductive biology of Cyrtopodium polyphyllum (Orchidaceae): A Cyrtopodiinae pollinated by deceit. Plant Biol. 10, 650–659. https://doi.org/10.1111/j.1438-8677.2008.00060.x (2008).
doi: 10.1111/j.1438-8677.2008.00060.x pubmed: 18761503
Pemberton, R. W. & Liu, H. Potential of invasive and native solitary specialist bee pollinators to help restore the rare cowhorn orchid (Cyrtopodium punctatum) in Florida. Biol. Conserv. 141, 1758–1764. https://doi.org/10.1016/j.biocon.2008.04.016 (2008).
doi: 10.1016/j.biocon.2008.04.016
Dutra, D., Kane, M. E., Adams, C. R. & Richardson, L. Reproductive biology of Cyrtopodium punctatum in situ: implications for conservation of an endangered Florida orchid. Plant Species Biol. 24, 92–103. https://doi.org/10.1111/j.1442-1984.2009.00242.x (2009).
doi: 10.1111/j.1442-1984.2009.00242.x
Leong, T. M. & Yeow, C. W. Observations of pollination in the pigeon orchid, Dendrobium crumenatum Swartz (Orchidaceae) in Singapore. Nat. Singap. 6, 91–96 (2013).
Meurgey, F. Bee species and their associated flowers in the French West Indies (Guadeloupe, Les Saintes, La Désirade, Marie Galante, St Barthelemy and Martinique) (Hymenoptera: Anthophila: Apoidea). Ann. Soc. Entomol. Fr. 52, 209–232. https://doi.org/10.1080/00379271.2016.1244490 (2016).
doi: 10.1080/00379271.2016.1244490
Ackerman, J. D. Orchidées invasives: accélération de la colonization et de la propagation. L’Orchidophile 213, 167–173 (2017).
Slater, A. T. & Calder, D. M. The pollination biology of Dendrobium speciosum Smith: A case of false advertising?. Aust. J. Bot. 36, 145–158. https://doi.org/10.1071/BT9880145 (1988).
doi: 10.1071/BT9880145
Beardsell, D. V., Clements, M. A., Hutchinson, J. F. & Williams, E. G. Pollination of Diuris maculata R Br (Orchidaceae) by Floral Mimicry of the Native Legumes Daviesia spp and Pultenaea scabra R Br. Aust. J. Bot. 34, 165–173. https://doi.org/10.1071/BT9860165 (1986).
doi: 10.1071/BT9860165
Indsto, J. O. et al. Pollination of Diuris maculata (Orchidaceae) by male Trichocolletes venustus bees. Aust. J. Bot. 54, 669–679. https://doi.org/10.1071/BT05146 (2006).
doi: 10.1071/BT05146
Rayment, T. Two orchids and a bee. Vic. Nat. 49, 140–140 (1932).
Kuiter, H. R. Orchid Pollinators of Victoria 5th edn. (Aquatic Photographics, Victoria, 2023).
Aguiar, J. M. R. B. V. & Pansarin, E. R. Deceptive pollination of Ionopsis utricularioides (Oncidiinae: Orchidaceae). Flora 250, 72–78. https://doi.org/10.1016/j.flora.2018.11.018 (2019).
doi: 10.1016/j.flora.2018.11.018
Rose-Smyth, M. C. Investigating the pollination biology of a long-lived island endemic epiphyte in the presence of an adventive alien pollinator. In Proceedings of the 22nd World Orchid Conference (eds Pridgeon, A. M. & Arosemena, A.) 80–91 (Asociación Ecuatoriana de Orquideología, Guayaquil, 2019).
Smith, G. R. & Snow, G. E. Pollination ecology of Platanthera (Habenaria) ciliaris and P. blephariglottis (Orchidaceae). Bot. Gaz. 137, 133–140 (1976).
doi: 10.1086/336852
Cole, F. R. & Firmage, D. H. The floral ecology of Platanthera blephariglottis. Am. J. Bot. 71, 700–710 (1984).
doi: 10.1002/j.1537-2197.1984.tb14177.x
Jones, D. L. The pollination of Prasophyllum alpinum R.Br.. Vic. Nat. 89, 260–263 (1972).
Johnson, S. D. et al. Diverse pollination systems of the twin-spurred orchid genus Satyrium in African grasslands. Plant Syst. Evol. 292, 95–103. https://doi.org/10.1007/s00606-010-0411-1 (2011).
doi: 10.1007/s00606-010-0411-1
Ellis, A. G. & Johnson, S. D. Do pollinators determine hybridization patterns in sympatric Satyrium (Orchidaceae) species?. Plant Syst. Evol. 219, 137–150 (1999).
doi: 10.1007/BF00985575
Botes, C., van der Niet, T., Cowling, R. M. & Johnson, S. D. Is biodiversity underestimated by classical her arium-based taxonomy? A multi-disciplinary case study in Satyrium (Orchidaceae). Bot. J. Linn. Soc. 194, 342–357. https://doi.org/10.1093/botlinnean/boaa041/5867273 (2020).
doi: 10.1093/botlinnean/boaa041/5867273
Van der Niet, T., Jürgens, A. & Johnson, S. D. Pollinators, floral morphology and scent chemistry in the southern African orchid genus Schizochilus. S. Afr. J. Bot. 76, 726–738 (2010).
doi: 10.1016/j.sajb.2010.07.004
Suetsugu, K. & Abe, Y. Unexpected contribution of the introduced honeybee Apis mellifera to high fruit set in Spiranthes australis (Orchidaceae). Entomol. News 129, 559–563. https://doi.org/10.3157/021.129.0511 (2021).
doi: 10.3157/021.129.0511
Iwata, T., Nagasaki, O., Ishii, H. S. & Ushimaru, A. Inflorescence architecture affects pollinator behaviour and mating success in Spiranthes sinensis (Orchidaceae). New Phytol. 193, 196–203. https://doi.org/10.1111/j.1469-8137.2011.03892.x (2012).
doi: 10.1111/j.1469-8137.2011.03892.x pubmed: 21919912
Coleman, E. Further notes on the pollination of Spiranthes sinensis (Pers.) Ames. Vic. Nat. 50, 61–64 (1933).
Catling, P. Pollination of northeastern North American Spiranthe (Orchidaceae). Can. J. Bot. 61, 1080–1093. https://doi.org/10.1139/b83-116 (1983).
doi: 10.1139/b83-116
Van der Cingel, N. A. An Atlas Of Orchid Pollination: America, Africa, Asia And Australia (Balkema, A.A., ed) (Rotterdam, 2001).
Ackerman, J. D. et al. Beyond the various contrivances by which orchids are pollinated: Global patterns in orchid pollination biology. Bot. J. Linn. Soc. https://doi.org/10.5281/zenodo.7263689 (2023).
Michener, C. D. The Bees of the World (2 ed.) xvi + 953 (Johns Hopkins University Press, Baltimore, 2007).
Valido, A., Rodríguez-Rodríguez, M. C. & Jordano, P. Honeybees disrupt the structure and functionality of plant-pollinator networks. Sci. Rep. 9, 4711 (2019).
doi: 10.1038/s41598-019-41271-5 pubmed: 30886227 pmcid: 6423295
Joffard, N., Massol, F., Grenié, M., Montgelard, C. & Schatz, B. Effect of pollination strategy, phylogeny and distribution on pollination niches of Euro-Mediterranean orchids. J. Ecol. 107, 478–490. https://doi.org/10.1111/1365-2745.13013 (2019).
doi: 10.1111/1365-2745.13013
De Luca, P. A. & Vallejo-Marín, M. What’s the ‘buzz’about? The ecology and evolutionary significance of buzz-pollination. Curr. Opin. Plant Biol. 16, 429–435. https://doi.org/10.1016/j.pbi.2013.05.002 (2013).
doi: 10.1016/j.pbi.2013.05.002 pubmed: 23751734
Zhang, H. P. et al. Reproductive isolation among three nocturnal moth-pollinated sympatric Habenaria species (Orchidaceae). Front. Plant Sci. 13, 908852 (2022).
doi: 10.3389/fpls.2022.908852 pubmed: 35812980 pmcid: 9257206
Lussu, M., De Agostini, A., Cogoni, A., Marignani, M. & Cortis, P. Does size really matter? A comparative study on floral traits in orchids with two different pollination strategies. Plant Biol. 21, 961–966 (2019).
doi: 10.1111/plb.12993 pubmed: 30945419
Klein, A. M., Steffan-Dewenter, I. & Tscharntke, T. Fruit set of highland coffee increases with the diversity of pollinating bees. Proc. R. Soc. B 270, 955–961. https://doi.org/10.1098/rspb.2002.2306 (2003).
doi: 10.1098/rspb.2002.2306 pubmed: 12803911 pmcid: 1691323
Hung, K. L. J., Kingston, J. M., Albrecht, M., Holway, D. A. & Kohn, J. R. The worldwide importance of honeybees as pollinators in natural habitats. Proc. R. Soc. B 285, 20172140 (2018).
doi: 10.1098/rspb.2017.2140 pubmed: 29321298 pmcid: 5784195
Aizen, M. A. et al. When mutualism goes bad: Density-dependent impacts of introduced bees on plant reproduction. New Phytol. 12, e8697. https://doi.org/10.1002/ece3.8697 (2014).
doi: 10.1002/ece3.8697
Scheper, J. et al. Museum specimens reveal loss of pollen host plants as key factor driving wild bee decline in The Netherlands. Proc. Natl. Acad. Sci. U S A 111, 17552–17557 (2014).
doi: 10.1073/pnas.1412973111 pubmed: 25422416 pmcid: 4267333
Houston, T. F., Dods, K., Milne, L. A. & Scaccabarozzi, D. New insights into the unusual nesting biology of the bee Trichocolletes orientalis (Hymenoptera: Colletidae, Neopasiphaeinae), particularly its larval ‘oil bath’. Apidologie 54, 11. https://doi.org/10.1007/s13592-022-00981-y (2023).
doi: 10.1007/s13592-022-00981-y
Potts, S. G. et al. Global pollinator declines: Trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353 (2010).
doi: 10.1016/j.tree.2010.01.007 pubmed: 20188434
Biesmeijer, J. C. et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313(5785), 351–354 (2006).
doi: 10.1126/science.1127863 pubmed: 16857940
Baude, M. et al. Historical nectar assessment reveals the fall and rise of floral resources in Britain. Nature 530(7588), 85–88 (2016).
doi: 10.1038/nature16532 pubmed: 26842058 pmcid: 4756436
Johnson, S. D. & Schiestl, F. P. Floral Mimicry (Oxford University Press, Oxford, 2016).
doi: 10.1093/acprof:oso/9780198732693.001.0001
Blaauw, B. R. & Isaacs, R. Larger patches of diverse floral resources increase insect pollinator density, diversity, and their pollination of native wildflowers. Basic Appl. Ecol. 15, 701–711. https://doi.org/10.1016/j.baae.2014.10.001 (2014).
doi: 10.1016/j.baae.2014.10.001
Backhouse, G. N., Copeland, L. M., Brown, A. P. & Bates, R. J. Checklist of the Orchids of Australia Including its Island Territories (Melbourne, 2019).
Jones, D. L. A Complete Guide to Native Orchids of Australia, Including the Island Territories 2nd edn. (Frenchs Forest, Reed New Holland, 2006).
Hoffman, N. & Brown, A. Orchids of South-West Australia 3rd edn. (Gooseberry Hill, Perth, 2011).
Wickham, H. & Wickham, H. Getting Started with ggplot2. ggplot2: Elegant graphics for data analysis 11–31. (2016).
Barton, K. MuMIn: multi-model inference. R package version 1. 0. 0. http://r-forge.r-project.org/projects/mumin/ (2009).
Wilkinson, L. ggplot2: elegant graphics for data analysis (2011).
Ripley, B. et al. Package ‘mass’. Cran r 538, 113–120 (2013).

Auteurs

Daniela Scaccabarozzi (D)

Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18 D, 752 36, Uppsala, Sweden. daniela.scaccabarozzi@ebc.uu.se.
School of Molecular and Life Sciences, Curtin University, Perth, Australia. daniela.scaccabarozzi@ebc.uu.se.

Lorenzo Guzzetti (L)

ZooPlantLab, Department of Biotechnology and Biosciences, University of Milano-Bicocca, Milan, Italy.

Emiliano Pioltelli (E)

ZooPlantLab, Department of Biotechnology and Biosciences, University of Milano-Bicocca, Milan, Italy.

Mark Brundrett (M)

School of Biological Sciences, University of Western Australia, Crawley, Australia.

Andrea Aromatisi (A)

Earth to Be, Consulting Group, Perth, Australia.

Giovanni Polverino (G)

Department of Ecological and Biological Sciences, University of Tuscia, Viterbo, Italy.

Mario Vallejo-Marin (M)

Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18 D, 752 36, Uppsala, Sweden.

Salvatore Cozzolino (S)

Department of Biology, University of Naples Federico II, Naples, Italy.

Zong-Xin Ren (ZX)

Kunming Institute of Botany, Chinese Academy of Sciences (CAS), Kunming, China.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH