Abstract
Crinum asiaticum is phenotypically specialised with white, scented, very long-tubed flowers, suggesting that only long-proboscid hawkmoths may be effective pollinators. However, this species has frequently escaped cultivation in many tropical and subtropical regions. We therefore investigated the reproductive biology of C. asiaticum to understand how it is able to naturalise, despite phenotypic specialisation. We examined the ability for autonomous selfing and reliance on sexual versus vegetative reproduction in C. asiaticum var. sinicum, using a group individuals growing and propagating naturally in a suburban botanical garden. We also analysed the floral syndrome, recorded floral visitors, determined the pollination effectiveness of floral visitors, and reviewed records of floral visitors at different observation sites. Sexual reproduction provides a much greater potential for dispersal than vegetative reproduction in C. asiaticum var. sinicum. This plant does not perform autonomous selfing and shows poor self-compatibility. The floral syndrome strongly points to long-proboscid hawkmoth pollination, whereas both hawkmoths and swallowtail butterflies with varied tongue lengths were observed as floral visitors because the nectar can accumulate to high levels and therefore fills the majority or all of the perianth tube. Both butterflies and hawkmoths effectively deposited pollen on stigmas. Thus, natural propagation should be attributed to sufficient cross pollination by local lepidopterans. Our findings suggest that autonomous selfing and vegetative reproduction may not be necessary for naturalisation and long-term persistence of plant populations in highly disturbed habitats or new ranges, even if the plants exhibit an extremely specialised floral syndrome.
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References
Armbruster WS (2006) Evolutionary and ecological aspects of specialized pollination: Views from the Arctic to the Tropics. In: Waser NM, Ollerton J (eds) Plant–pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, pp 260–282
Balducci MG, Martins DJ, Johnson SD (2019a) Pollination of the long-spurred African terrestrial orchid Bonatea steudneri by long-tongued hawkmoths, notably Xanthopan morganii. Pl Syst Evol 305:765–775. https://doi.org/10.1007/s00606-019-01605-2
Balducci MG, Martins DJ, Johnson SD (2019b) Pollination of the long-spurred African terrestrial orchid Bonatea steudneri by long-proboscid hawkmoths, notably Xanthopan morganii. Pl Syst Evol 305:765–775. https://doi.org/10.1007/s00606-019-01605-2
Bjorå CS, Kwembeya EG, Nordal I (2006) Crinum jasoniia: a new endemic pan species of the Luangwa Valley in Zambia with notes on different seed structures in the genus. Kew Bull 61:569–577
Celep F, Atalay Z, Dikmen F, Doğan M, Classen-Bockhoff R (2014) Flies as pollinators of melittophilous Salvia species (Lamiaceae). Amer J Bot 101:2148–2159. https://doi.org/10.3732/ajb.1400422
Clark-Tapia R, Molina-Freaner F (2004) Reproductive ecology of the rare clonal cactus Stenocereus eruca in the Sonoran desert. Pl Syst Evol 247:155–164. https://doi.org/10.1007/s00606-003-0118-7
Dobson HEM (2006) Relationship between floral fragrance composition and type of pollinator. In: Dudareva N, Pichersky E (eds) Biology of floral scent. Taylor & Francis, Boca Raton, pp 147–198
Epps MJ, Allison SE, Wolfe LM (2015) Reproduction in Flame Azalea (Ericaceae): a rare case of insect wing pollination. Am Nat 186(2):294–301
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annual Rev Ecol Syst 35:375–403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347
Gardner RO, Early JW (1996) The naturalization of Banyan figs (Ficus spp. Moraceae) and their pollinating wasps (Hymenoptera: Agaonidae) in New Zealand. New Zealand J Bot 34:103–110. https://doi.org/10.1080/0028825X.1996.10412697
Geerts S, Pauw A (2009) African sunbirds hover to pollinate an invasive hummingbird-pollinated plant. Oikos 118:573–579. https://doi.org/10.1111/j.1600-0706.2008.17167.x
Haber A, Frankie GW (1989) A tropical hawkmoth community: Costa Rican dry forest Sphingidae. Biotropica 21:155–172. https://doi.org/10.2307/2388706
Herrera I, Nassar JM (2009) Reproductive and recruitment traits as indicators of the invasive potential of Kalanchoe daigremontiana (Crassulaceae) and Stapelia gigantea (Apocynaceae) in a Neotropical arid zone. J Arid Environm 73:978–986. https://doi.org/10.1016/j.jaridenv.2009.05.004
Hirota SK, Nitta K, Suyama Y, Kawakubo N, Yasumoto AA, Yahara T (2013) Pollinator-mediated selection on flower color, flower scent and flower morphology of Hemerocallis: evidence from genotyping individual pollen grains on the stigma. PLoS ONE 8:e85601. https://doi.org/10.1371/journal.pone.0085601
Hirota SK, Miki N, Yasumoto AA, Yahara T (2019) UV bullseye contrast of Hemerocallis flowers attracts hawkmoths but not swallowtail butterflies. Ecol Evol 9:52–64. https://doi.org/10.1002/ece3.4604
Ji Z-H, Meerow A-W (2000) Amaryllidaceae Jaume Saint Hilaire. In: Wu ZY, Raven PH & Hong DY (Eds.), Flora of China, vol. 24. Science Press, Beijing & Missouri Botanical Garden Press, St. Louis
Johnson SD, Moré M, Amorim FW, Haber WA, Frankie GW, Stanley DA, Cocucci AA, Raguso RA (2017) The long and the short of it: a global analysis of hawkmoth pollination niches and interaction networks. Funct Ecol 31:101–115. https://doi.org/10.1111/1365-2435.12753
Johnson SD, Neal PR, Peter CI, Edwards TJ (2004) Fruiting failure and limited recruitment in remnant populations of the hawkmoth-pollinated tree Oxyanthus pyriformis subsp. pyriformis (Rubiaceae). Biol Conserv 120:31–39. https://doi.org/10.1016/j.biocon.2004.01.028
Johnson SD, Raguso RA (2016) The long-proboscid hawkmoth pollinator niche for native and invasive plants in Africa. Ann Bot (Oxford) 117:25–36. https://doi.org/10.1093/aob/mcv137
Kiepiel I, Johnson SD (2014) Shift from bird to butterfly pollination in Clivia (Amaryllidaceae). Am J Bot 101(1):190–200
van Kleunen M, Manning JC, Pasqualetto V, Johnson SD (2008) Phylogenetically independent associations between autonomous self-fertilization and plant invasiveness. Amer Naturalist 171:195–201. https://doi.org/10.1086/525057
Klimes L, Klimesová J, Hendriks R, van Groenendael J (1997) Clonal plant architecture: Clonal plant architecture: a comparative analysis of form and function. In: de Kroon H, van Groenendael J (eds) The Ecology and Evolution of Clonal Plants. Backhuys Publishers, Leiden, pp 1–30
Knuth P, Loew E (1904–1905) Handbuch der blütenbiologie, vol 3. Wilhem Engelmann, Leipzig
Liu J, Dong M, Miao S-L, Li ZY, Song MH, Wang RQ (2006) Invasive alien plants in China: role of clonality and geographical origin. Biol Invasions 8:1461–1470. https://doi.org/10.1007/s10530-005-5838-x
Liu C-Q, Gao Y-D, Niu Y, Xiong Y-Z, Sun H (2019) Floral adaptations of two lilies: implications for the evolution and pollination ecology of huge trumpet-shaped flowers. Amer J Bot 106:1–11. https://doi.org/10.1002/ajb2.1275
Liu H, Pemberton R (2010) 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
Manning JC, Goldblatt P (2005) Radiation of pollination systems in the Cape genus Tritoniopsis (Iridaceae: Crocoideae) and the development of bimodal pollination strategies. Int J Pl Sci 166:459–474. https://doi.org/10.1086/428703
Martins DJ, Johnson SD (2013) Interactions between hawkmoths and flowering plants in East Africa: polyphagy and evolutionary specialization in an ecological context. Biol J Linn Soc 110:199–213. https://doi.org/10.1111/bij.12107
Matyot P (2005) The hawkmoths (Lepidoptera: Sphingidae) of Seychelles: identification, historical background, distribution, food plants and ecological considerations. Phelsuma 13:55–80
Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc Roy Soc London B 271:2605–2611. https://doi.org/10.1098/rspb.2004.2909
Miller WE (1997) Diversity and evolution of tongue length in hawkmoths (Sphingidae). J Lepid Soc 51:9–31
Miyake T, Yamaoka R, Yahara T (1998) Roral scents of hawkmoth-pollinated flowers in Japan. J Pl Res 111:199–205. https://doi.org/10.1007/BF02512170
Miyake T, Yahara T (1998) Why does the flower of Lonicera japonica open at dusk? Canad J Bot 76:1806–1811. https://doi.org/10.1139/b98-119
Morinaga SI, Kumano Y, Ota A, Yamaoka R, Sakai S (2009) Day-night fluctuations in floral scent and their effects on reproductive success in Lilium auratum. Populat Ecol 51:187–195. https://doi.org/10.1007/s10144-008-0097-1
Nakajima R, Okamiya H, Shimokawa S, Yamamoto K, Kato H, Murakami N (2018) Comparison of floral traits and pollinator assemblages of insular and mainland varieties of Lilium auratum. Pl Spec Biol 33:276–288. https://doi.org/10.1111/1442-1984.12222
Nienhuis C, Stout JC (2009) Effectiveness of native bumblebees as pollinators of the alien invasive plant Impatiens glandulifera. J Pollinat Ecol 1:1–11. https://doi.org/10.26786/1920-7603(2009)1
Ollerton J, Watts S, Connerty S, Lock J, Parker L, Wilson I, Schueller SK, Nattero J, Cocucci AA, Izhaki I, Geerts S, Pauw A, Stout JC (2012) Pollination ecology of the invasive tree tobacco Nicotiana glauca: comparisons across native and non-native ranges. J Pollinat Ecol 9:85–95
Ollerton J, Killick A, Lamborn E, Watts S, Whiston M (2007) Multiple meanings and modes: on the many ways to be a generalist flower. Taxon 56:717–728. https://doi.org/10.2307/25065855
Paudel BR, Shrestha M, Burd M, Adhikari S, Sun Y-S, Li Q-J (2016) Coevolutionary elaboration of pollination-related traits in an alpine ginger (Roscoea purpurea) and a tabanid fly in the Nepalese Himalayas. New Phytol 211:1402–1411. https://doi.org/10.1111/nph.13974
Pittaway AR, Kitching IJ (2020) Sphingidae of the Eastern Palaearctic (including Siberia, the Russian Far East, Mongolia, China, Taiwan, the Korean Peninsula and Japan), The Natural History Museum, London. Available at: http://tpittaway.tripod.com/china/china.htm
Reiter N, Vlcek K, O’Brien N, Gibson M, Pitts D, Brown GR, Bower CC, Phillips RD (2017) Pollinator rarity limits reintroduction sites in an endangered sexually deceptive orchid (Caladenia hastata): implications for plants with specialized pollination systems. Biol J Linn Soc 184:122–136. https://doi.org/10.1093/botlinnean/box017
Richardson DM (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93
Rodger JG, van Kleunen M, Johnson SD (2010) Does specialized pollination impede plant invasions? Int J Pl Sci 171:382–391. https://doi.org/10.1086/651226
Skogen KA, Jogesh T, Hilpman ET, Todd SL, Rhodes MK, Still SM, Fant JB (2016) Land-use change has no detectable effect on reproduction of a disturbance-adapted, hawkmoth-pollinated plant species. Amer J Bot 103:1950–1963. https://doi.org/10.3732/ajb.1600302
Van der Niet T, Johson SD (2012) Phylogenetic evidence for pollinator-driven diversification of angiosperms. Trends Ecol Evol 27:353–361. https://doi.org/10.1016/j.tree.2012.02.002
Walsha SK, Pender RJ, Junker RR, Daehlerb CC, Morden CW, Lorence DH (2019) Pollination biology reveals challenges to restoring populations of Brighamia insignis (Campanulaceae), a critically endangered plant species from Hawai‘i. Flora 259:151448. https://doi.org/10.1016/j.flora.2019.151448
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060. https://doi.org/10.2307/2265575
Waser NM, Ollerton J, Erhardt A (2011) Typology in pollination biology: lessons from an historical critique. J Pollinat Ecol 3:1–7. https://doi.org/10.26786/1920-7603(2011)2
WCSP (2016) World checklist of selected plant families, The Royal Botanic Gardens, Kew. Available at: http://apps.kew.org/wcsp/
Acknowledgements
We thank Ji-Bai He and Zhuo-Heng Jiang for the identification of lepidopterans and Zhuo-Heng Jiang for providing the photo of a Papilio helenus specimen used in Fig. 5. We thank Ying-Ze Xiong and Ze-Yu Tong for advice on statistical analysis. This study was supported by National Natural Science Foundation of China (Grant No. 31971563 to C.-Q. Liu and 31560068 to X.-H. Hu), the Science and Technology Basic Resources Investigation Program of China (Grant No. 2017FY100100) and Elevation of Talent Program of Guangxi Karst Ecological Construction and Sustainable Utilization of Plant Resources in 2018.
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Chang-Qiu Liu devised this study, revised the draft critically and took the photographs of the insects visiting flowers. The remaining authors were responsible for observing floral visitors and measuring nectar and flower and insect morphologies. Yang Huang and Lan-Ying Liu conducted the pollination treatments. Huang Yang wrote the first draft of the manuscript. Qing-Biao Lu helped Yang Huang conduct statistical analysis. Bo Cai helped Yang Huang prepare the figures. All authors read and approved the final manuscript.
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. The three hawkmoth visitors not included in Fig. 2. a. Agrius convolvuli. b. Acosmeryx pseudomissa. c. Psilogramma increta. See the yellow pollen attached to these moths.
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Online Resource 1. The three hawkmoth visitors not included in Fig. 2. a. Agrius convolvuli. b. Acosmeryx pseudomissa. c. Psilogramma increta. See the yellow pollen attached to these moths.
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Huang, Y., Liu, LY., Liu, CQ. et al. Diverse large lepidopteran pollinators promote the naturalisation of Crinum asiaticum in invaded and disturbed habitats, despite apparent floral specialisation. Plant Syst Evol 307, 23 (2021). https://doi.org/10.1007/s00606-021-01748-1
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DOI: https://doi.org/10.1007/s00606-021-01748-1