被子植物蜜距的多样性及进化生态学研究
收稿日期: 2022-11-04
录用日期: 2023-03-01
网络出版日期: 2023-03-16
基金资助
国家自然科学基金(32160054);国家自然科学基金(31800193)
Diversity and evolutionary ecology of nectar spurs in angiosperms
Received date: 2022-11-04
Accepted date: 2023-03-01
Online published: 2023-03-16
Supported by
National Natural Science Foundation of China(32160054);National Natural Science Foundation of China(31800193)
蜜距将花蜜隐藏在距的深处, 多样的蜜距形态和长度吸引各种喙长的传粉动物访花, 促进传粉生态位形成, 这对造就物种多样性起到了重要作用。因此蜜距被认为是促进物种形成的关键创新性状, 是研究被子植物花部结构演化、植物-传粉者协同进化的理想材料。系统地总结蜜距植物及其形态特征和传粉/盗蜜者, 有助于全面了解这一性状在被子植物中的系统发育分布和进化生态学意义。该文对国内外植物分类数据库(检索词“距”或“spur”)和已发表文章(检索词“有距植物属中文名+传粉”或“属拉丁名+ pollinator/nectar robber”)进行系统的梳理和总结, 收集蜜距植物、距长、蜜距形态、传粉者、盗蜜者等信息。整理出具有蜜距的植物分布在被子植物13个目23个科271个属, 共计3 427种。其中蜜距植物种数最多的科为兰科(1 536种)、罂粟科(487种)、毛茛科(351种)、凤仙花科(284种)、堇菜科(197种), 它们占所有蜜距植物种数的83.3%。根据蜜距的发育来源, 蜜距可分为6种类型: 花被片蜜距、花瓣蜜距、萼片蜜距、被丝托蜜距、花萼蜜距和花冠蜜距。花瓣蜜距分布于212个属, 显著高于其他类型。对2 546种植物的蜜距长度分析发现: 凤仙花科的蜜距平均长度最长, 达23.8 mm; 千屈菜科的蜜距最短, 平均仅1.6 mm。形态上, 大部分蜜距具有不同程度的弯曲, 这可能有助于筛选合适的传粉者, 提高访花者的传粉效率; 单花蜜距数量有1-6个, 大部分为1个, 多个蜜距可能增加传粉者的访花时间; 部分兰科和堇菜科植物蜜距内部具有可能分泌花蜜的附属物。蜜距植物的传粉者主要为膜翅目、鳞翅目、部分长喙双翅目昆虫及鸟类; 盗蜜者主要为膜翅目昆虫。蜜距的长度和传粉者的喙长普遍存在地理镶嵌的协同进化关系, 进化生态学家提出了“达尔文机械模型”的假说来解释这种现象; 而当传粉者喙长不变, 距长随着传粉者种类改变时则用“传粉者转变模型”来解释蜜距的伸长。未来在蜜距的进化生态学研究中, 不仅要关注蜜距植物的距长和传粉者喙长的形态学特征及传粉生态学研究, 还应借助发育解剖学和基因组学, 以及新的技术手段, 从细胞的分裂、伸长, 功能基因, 非生物因子等各个方面, 探索蜜距演化的驱动因素。
杨明威, 金晓芳 . 被子植物蜜距的多样性及进化生态学研究[J]. 植物生态学报, 2023 , 47(9) : 1193 -1210 . DOI: 10.17521/cjpe.2022.0445
For many plants, nectar is hidden in the depth of nectar spurs. The diverse morphology and length of nectar spurs can attract pollinators with various proboscis lengths and promote the differentiation of pollination niche, which plays an important role in the formation of species diversity. Therefore, nectar spur is considered as a key innovation trait in promoting speciation and an ideal trait for studying floral evolution and plant-pollinator coevolution in angiosperm. This review systematically summarizes the worldwide plant taxonomic databases and published articles, classifies the nectar spur plants, and reviews the diversity and evolutionary mechanisms of nectar spur plants. We investigated 3 427 nectar spur species belonging to 13 orders, 23 families and 271 genera of angiosperm. Among them, Orchidaceae has the largest number of species, with 1 536 species, following by Papaveraceae with 487 species, Ranunculaceae with 351 species, Balsaminaceae with 284 species and Violaceae with 197 species, accounting for 83.3% of all the species. According to the sources of the development of nectar spurs, the nectar spurs can be divided into six types: petal spur, corolla spur, sepal spur, calyx spur, tepal spur and hypanthium spur. The petal spurs are the predominant type, detected in 212 genera. The average length of nectar spurs in Balsaminaceae is the longest (23.8 mm) among the 2 546 species whose nectar spurs have been measured. The shortest nectar spurs are reported in Lycelandaceae, which are only 1.6 mm on average. Most nectar spurs have different degrees of curvature, likely helping to improve the pollination efficiency. The number of nectar spur(s) in a flower ranges from 1 to 6, and most species have only one nectar spur in a flower. Multiple nectar spurs may increase the visiting time of pollinators. Some plants in Orchidaceae and Violaceae have appendages inside the nectar spurs, which may have the function of nectar secretion. The pollinators of plants with nectar spur mainly comprise insects from Hymenoptera, Lepidoptera, and some long-proboscis species from Diptera and birds. Nectar robbers are mainly bees and birds. There is a general association of geographic mosaic theory of coevolution between the length of nectar spur and the length of pollinator proboscis. Evolutionary ecologists have proposed the hypothesis of “Darwin’s Mechanistic Model” and “The Pollinator Shift Model” to explain this phenomenon. In future studies of the mechanisms of nectar spur evolution, we should not only focus on the morphological characteristics of spur length and proboscis length and the pollination ecology, but also explore the driving forces of nectar spurs evolution from cell division/elongation, functional genes, abiotic factors, with the help of novel technological approaches including developmental anatomy and genomics.
| [1] | Almouslem AB, Tilney-Bassett RAE (1989). The inheritance of flower doubleness and nectary spur in Pelargonium × hortorum Bailey. Euphytica, 41, 23-29. |
| [2] | Antoń S, Kamińska M (2015). Comparative floral spur anatomy and nectar secretion in four representatives of Ranunculaceae. Protoplasma, 252, 1587-1601. |
| [3] | Ayers TJ (1987). Four species from western Mexico new to Lobelia (Campanulaceae: Lobelioideae). Brittonia, 39, 417-422. |
| [4] | Ayers TJ (1990). Systematics of Heterotoma (Campanulaceae) and the evolution of nectar spurs in the New World Lobelioideae. Systematic Botany, 15, 296-327. |
| [5] | Bateman RM, Rudall PJ, James KE (2006). Phylogenetic context, generic affinities and evolutionary origin of the enigmatic Balkan orchid Gymnadenia frivaldii Hampe ex Griseb. Taxon, 55, 107-118. |
| [6] | Bateman RM, Sexton R (2008). Is spur length of Platanthera species in the British Isles adaptively optimized or an evolutionary red herring? Watsonia, 27, 1-22. |
| [7] | Bell AK, Roberts DL, Hawkins JA, Rudall PJ, Box MS, Bateman RM (2009). Comparative micromorphology of nectariferous and nectarless labellar spurs in selected clades of subtribe Orchidinae (Orchidaceae). Botanical Journal of the Linnean Society, 160, 369-387. |
| [8] | Blaxland K (2004). A new species of Viola (Violaceae) from south-west Turkey. Botanical Journal of the Linnean Society, 145, 505-509. |
| [9] | Boberg E, Alexandersson R, Jonsson M, Maad J, ?gren J, Nilsson LA (2014). Pollinator shifts and the evolution of spur length in the moth-pollinated orchid Platanthera bifolia. Annals of Botany, 113, 267-275. |
| [10] | Boehm MMA, Jankowski JE, Cronk QCB (2022). Plant- pollinator specialization: origin and measurement of curvature. The American Naturalist, 199, 206-222. |
| [11] | Box MS (2010). Role of KNOX Genes in the Evolution and Development of Floral Nectar Spurs. PhD dissertation, University of Cambridge, Cambridge, UK. |
| [12] | Box MS, Bateman RM, Glover BJ, Rudall PJ (2008). Floral ontogenetic evidence of repeated speciation via paedomorphosis in subtribe Orchidinae (Orchidaceae). Botanical Journal of the Linnean Society, 157, 429-454. |
| [13] | Box MS, Dodsworth S, Rudall PJ, Bateman RM, Glover BJ (2011). Characterization of Linaria KNOX genes suggests a role in petal-spur development. The Plant Journal, 68, 703-714. |
| [14] | Bruce EA (1953). Notes on African Pedaliaceae. Kew Bulletin, 8, 417-429. |
| [15] | Brunet J, van Etten ML (2019). The response of floral traits associated with pollinator attraction to environmental changes expected under anthropogenic climate change in high-altitude habitats. International Journal of Plant Sciences, 180, 954-964. |
| [16] | Carmo-Oliveira R, Oliveira PE, Lange de Morretes B (2017). Appendicular origin and structure of the spur of Vochysiaceae flowers. Acta Botanica Brasilica, 31, 433-444. |
| [17] | Chapurlat E, ?gren J, Sletvold N (2015). Spatial variation in pollinator-mediated selection on phenology, floral display and spur length in the orchid Gymnadenia conopsea. New Phytologist, 208, 1264-1275. |
| [18] | Chowlu K, Angela N, Rao AN, Vij SP (2012). Two new additions to the orchid flora of Manipur, India. Kew Bull, 16, 1. |
| [19] | Cole TCH, Hilger HH, Stevens P (2019). Angiosperm phylogeny poster (APP)—Flowering plant systematics, 2019. PeerJ Preprints. DOI: 10.7287/peerj.preprints.2320v6. |
| [20] | Cronk QCB, Bateman RM, Hawkins JA (2002). Developmental Genetics and Plant Evolution. CRC Press, Boca Raton. |
| [21] | Cullen E (2020). The Evolution and Development of Nectar Spurs. PhD dissertation, University of Cambridge, Cambridge, UK. |
| [22] | Cullen E, Fernández-Mazuecos M, Glover BJ (2018). Evolution of nectar spur length in a clade of Linaria reflects changes in cell division rather than in cell expansion. Annals of Botany, 122, 801-809. |
| [23] | Dodsworth S (2017). Petal, sepal, or tepal? B-genes and monocot flowers. Trends in Plant Science, 22, 8-10. |
| [24] | Don D (1841). A monograph of the genus Disporum. Transactions of the Linnean Society of London, 18, 513-524. |
| [25] | Dransfield J, Comber JB, Smith G (1986). A synopsis of Corybas (Orchidaceae) in west Malesia and Asia. Kew Bulletin, 41, 575-613. |
| [26] | Edwards MB, Ballerini ES, Kramer EM (2022). Complex developmental and transcriptional dynamics underlie pollinator-driven evolutionary transitions in nectar spur morphology in Aquilegia (columbine). American Journal of Botany, 109, 1360-1381. |
| [27] | Ellis AG, Johnson SD (1999). Do pollinators determine hybridization patterns in sympatric Satyrium (Orchidaceae) species? Plant Systematics and Evolution, 219, 137-150. |
| [28] | Endress PK, Matthews ML (2006). Elaborate petals and staminodes in eudicots: diversity, function, and evolution. Organisms Diversity & Evolution, 6, 257-293. |
| [29] | Fernández-Mazuecos M, Blanco-Pastor JL, Juan AN, Carnicero P, Forrest A, Alarcón M, Vargas P, Glover BJ (2019). Macroevolutionary dynamics of nectar spurs, a key evolutionary innovation. New Phytologist, 222, 1123-1138. |
| [30] | Fleischmann A (2018). Systematics and Evolution of Lentibulariaceae: II. Genlisea. Oxford University Press, Oxford. |
| [31] | Fulton M, Hodges SA (1999). Floral isolation between Aquilegia formosa and Aquilegia pubescens. Proceedings of the Royal Society of London. Series B: Biological Sciences, 266, 2247-2252. |
| [32] | Graham SA (1990). New species of Cuphea section Melvilla (Lythraceae) and an annotated key to the section. Brittonia, 42, 12-32. |
| [33] | Grant V, Grant KA (1965). Flower Pollination in the Phlox Family. Columbia University Press, New York. |
| [34] | Grant V, Temeles EJ (1992). Foraging ability of rufous hummingbirds on hummingbird flowers and hawkmoth flowers. Proceedings of the National Academy of Sciences of the United States of America, 89, 9400-9404. |
| [35] | Guo MY, Pang XH, Xu YQ, Jiang WJ, Liao BS, Yu JS, Xu J, Song JY, Chen SL (2022). Plastid genome data provide new insights into the phylogeny and evolution of the genus Epimedium. Journal of Advanced Research, 36, 175-185. |
| [36] | Hagen KB, Kadereit JW (2003). The diversification of Halenia (Gentianaceae): ecological opportunity versus key innovation. Evolution, 57, 2507-2518. |
| [37] | Hilton LD, Harder SC (2006). Ecology and Evolution of Flowers. Oxford University Press, Oxford. |
| [38] | Hobbhahn N, Johnson SD, Bytebier B, Yeung LD, Harder LD (2013). The evolution of floral nectaries in Disa (Orchidaceae: Disinae): recapitulation or diversifying innovation? Annals of Botany, 112, 1303-1319. |
| [39] | Hodges SA (1995). The influence of nectar production on hawkmoth behavior, self pollination, and seed production in Mirabilis multiflora (Nyctaginaceae). American Journal of Botany, 82, 197-204. |
| [40] | Hodges SA (1997). Floral nectar spurs and diversification. International Journal of Plant Sciences, 158, S81-S88. |
| [41] | Hodges SA, Arnold ML (1995). Spurring plant diversification: Are floral nectar spurs a key innovation? Proceedings of the Royal Society of London. Series B: Biological Sciences, 262, 343-348. |
| [42] | Hodges SA, Fulton M, Yang JY, Whittall JB (2004). Verne Grant and evolutionary studies of Aquilegia. New Phytologist, 161, 113-120. |
| [43] | Holmgren NH (1992). Two new species of Viola (Violaceae) from the Intermountain West, USA. Brittonia, 44, 300-305. |
| [44] | Ho?ák D, Jane?ek ? (2021). A geographical perspective on the relationship between Impatiens spur lengths and bill lengths of sunbirds in Afrotropical Mountains. Ecology and Evolution, 11, 3120-3129. |
| [45] | Inouye DW (1980). The terminology of floral larceny. Ecology, 61, 1251-1253. |
| [46] | Irwin RE, Brody AK (1998). Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia, 116, 519-527. |
| [47] | Irwin RE, Bronstein JL, Manson JS, Richardson L (2010). Nectar robbing: ecological and evolutionary perspectives. Annual Review of Ecology, Evolution, and Systematics, 41, 271-292. |
| [48] | Irwin RE, Maloof JE (2002). Variation in nectar robbing over time, space, and species. Oecologia, 133, 525-533. |
| [49] | Jabbour F, Renner SS (2012). Spurs in a spur: perianth evolution in the Delphinieae (Ranunculaceae). International Journal of Plant Sciences, 173, 1036-1054. |
| [50] | Jane?ek ?, Barto? M, Njabo KY (2015). Convergent evolution of sunbird pollination systems of Impatiens species in tropical Africa and hummingbird systems of the New World. Biological Journal of the Linnean Society, 115, 127-133. |
| [51] | Janssens SB, Smets EF, Vrijdaghs A (2012). Floral development of Hydrocera and Impatiens reveals evolutionary trends in the most early diverged lineages of the Balsaminaceae. Annals of Botany, 109, 1285-1296. |
| [52] | Johnson SD (1996). Bird pollination in South African species of Satyrium (Orchidaceae). Plant Systematics and Evolution, 203, 91-98. |
| [53] | Johnson SD, Anderson B (2010). Coevolution between food-rewarding flowers and their pollinators. Evolution, 3, 32-39. |
| [54] | Johnson SD, Ellis A, D?tterl S (2007). Specialization for pollination by beetles and wasps: the role of lollipop hairs and fragrance in Satyrium microrrhynchum (Orchidaceae). American Journal of Botany, 94, 47-55. |
| [55] | Johnson SD, Peter CI, Ellis AG, Boberg E, Botes C, van der Niet T (2011). Diverse pollination systems of the twin-spurred orchid genus Satyrium in African grasslands. Plant Systematics and Evolution, 292, 95-103. |
| [56] | 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. |
| [57] | Kawasaki ML (1992). Systematics of Erisma (Vochysiaceae). Wiley Press, Hoboken, USA. |
| [58] | Kil JH, Park SH, Kim YH, Lee DB (2009). Unrecorded and introduced taxon in Korea: Cymbalaria muralis P. Gaetrn. (Scrophulariaceae). Korean Journal of Plant Taxonomy, 39, 120-123. |
| [59] | Koehler S, Williams NH, Whitten WM, do Carmo E do Amaral M (2002). Phylogeny of the Bifrenaria (Orchidaceae) complex based on morphology and sequence data from nuclear rDNA internal transcribed spacers (ITS) and chloroplast trnL-trnF region. International Journal of Plant Sciences, 163, 1055-1066. |
| [60] | Koopman MM, Ayers TJ (2005). Nectar spur evolution in the Mexican lobelias (Campanulaceae: Lobelioideae). American Journal of Botany, 92, 558-562. |
| [61] | Kowalkowska A, Margońska H, Kozieradzka-Kiszkurno M (2010). Comparative anatomy of the lip spur and additional lateral sepal spurs in a three-spurred form (f. fumeauxiana) of Anacamptis pyramidalis. Acta Biologica Cracoviensia Series Botanica, 52, 13-18. |
| [62] | Kowalkowska AK, Margońska HB, Kozieradzka-Kiszkurno M, Bohdanowicz J (2012). Studies on the ultrastructure of a three-spurred fumeauxiana form of Anacamptis pyramidalis. Plant Systematics and Evolution, 298, 1025-1035. |
| [63] | Krishna S, Keasar T (2018). Morphological complexity as a floral signal: from perception by insect pollinators to co-evolutionary implications. International Journal of Molecular Sciences, 19, 1681. DOI: 10.3390/ijms19061681. |
| [64] | Kurzweil H, Manning JC (2005). A synopsis of the genus Disperis Sw. (Orchidaceae). Adansonia, 27, 155-207. |
| [65] | Li DF, Yan XC, Lin Y, Wang L, Wang Q (2021). Do flowers removed of either nectar or pollen attract fewer bumblebee pollinators? An experimental test in Impatiens oxyanthera. AoB Plants, 13, plab029. DOI: 10.1093/aobpla/plab029. |
| [66] | Li MH, Zhang GQ, Lan SR, Liu ZJ, Consortium CP (2016). A molecular phylogeny of Chinese orchids. Journal of Systematics and Evolution, 54, 349-362. |
| [67] | Li YX, Quan QM, Sun GL (2009). Effect of floral morphology on fruit set in Epimedium sagittatum (Berberidaceae). Plant Systematics and Evolution, 279, 51-58. |
| [68] | Louis P, Decraene R, Smets EF (2001). Floral developmental evidence for the systematic relationships of Tropaeolum (Tropaeolaceae). Annals of Botany, 88, 879-892. |
| [69] | Lustofin K, ?wi?tek P, Miranda VFO, P?achno BJ (2020). Flower nectar trichome structure of carnivorous plants from the genus butterworts Pinguicula L. (Lentibulariaceae). Protoplasma, 257, 245-259. |
| [70] | Ma WL (2018). Fine Structure and Morphology of Plants in China. Higher Education Press, Beijing. |
| [70] | [马炜梁 (2018). 中国植物精细解剖. 高等教育出版社, 北京.] |
| [71] | Macior LW (1970). The pollination ecology of Dicentra cucullaria. American Journal of Botany, 57, 6-11. |
| [72] | Macior LW (1975). The pollination ecology of Delphinium tricorne (Ranunculaceae). American Journal of Botany, 62, 1009-1016. |
| [73] | Macior LW (1978). Pollination interactions in sympatric Dicentra species. American Journal of Botany, 65, 57-62. |
| [74] | Mack JLK, Davis AR (2015). The relationship between cell division and elongation during development of the nectar- yielding petal spur in Centranthus ruber (Valerianaceae). Annals of Botany, 115, 641-649. |
| [75] | Manning JC, Goldblatt P, Forest F (2009). A revision of Fumariaceae (Fumarioideae) in southern Africa, including naturalized taxa. Bothalia, 39, 45-65. |
| [76] | Miller RB (1978). The pollination ecology of Aquilegia elegantula and A. caerulea (Ranunculaceae) in Colorado. American Journal of Botany, 65, 406-414. |
| [77] | Miller RB (1981). Hawkmoths and the geographic patterns of floral variation in Aquilegia caerulea. Evolution, 35, 763-774. |
| [78] | Miller RB, Willard CL (1983). The pollination ecology of Aquilegia micrantha (Ranunculaceae) in Colorado. The Southwestern Naturalist, 28, 157-164. |
| [79] | Minelli A (2016). Species diversity vs. morphological disparity in the light of evolutionary developmental biology. Annals of Botany, 117, 781-794. |
| [80] | Newman DA, Thomson JD (2005). Effects of nectar robbing on nectar dynamics and bumblebee foraging strategies in Linaria vulgaris (Scrophulariaceae). Oikos, 110, 309-320. |
| [81] | Nguyen VC, Averyanov LV, Maisak TV, Nguyen TLT, Nguyen VK, Truong BV (2022). Gastrochilus pankajkumarii, (Aeridinae, Epidendroideae, Orchidaceae), a new lithophytic orchid from southern Vietnam. Taiwania, 67, 35-39. |
| [82] | Orellana MR, Rovira AM, Blanché C, Bosch M (2008). Effects of local abundance on pollination and reproduction in the narrow endemic endangered species Delphinium bolosii (Ranunculaceae). Orsis, 23, 027-046. |
| [83] | Pansarin ER, Pansarin LM, Alves-dos-Santos I (2015). Floral features, pollination biology, and breeding system of Comparettia coccinea (Orchidaceae: Oncidiinae). Flora- Morphology, Distribution, Functional Ecology of Plants, 217, 57-63. |
| [84] | Paton A (1997). Classification and species of Platostoma and its relationship with Haumaniastrum (Labiatae). Kew Bulletin, 52, 257-292. |
| [85] | Peter CI, Johnson SD (2009). Pollination by flower chafer beetles in Eulophia ensata and Eulophia welwitschii (Orchidaceae). South African Journal of Botany, 75, 762-770. |
| [86] | P?achno BJ, Stpiczyńska M, Adamec L, Miranda VFO, ?wi?tek P (2018). Nectar trichome structure of aquatic bladderworts from the section Utricularia (Lentibulariaceae) with observation of flower visitors and pollinators. Protoplasma, 255, 1053-1064. |
| [87] | Puzey JR, Gerbode SJ, Hodges SA, Kramer EM, Mahadevan L (2012). Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy. Proceedings of the Royal Society B: Biological Sciences, 279, 1640-1645. |
| [88] | Rebocho AB, Southam P, Kennaway JR, Bangham JA, Coen E (2017). Generation of shape complexity through tissue conflict resolution. Elife, 6, e20156. DOI: 10.7554/eLife.20156. |
| [89] | Robertson JL, Wyatt R (1990). Evidence for pollination ecotypes in the yellow-fringed orchid, Platanthera ciliaris. Evolution, 44, 121-133. |
| [90] | Rudall PJ, Manning JC, Goldblatt P (2003). Evolution of floral nectaries in Iridaceae. Annals of the Missouri Botanical Garden, 90, 613-631. |
| [91] | Rust RW (1979). Pollination of Impatiens capensis: pollinators and nectar robbers. Journal of the Kansas Entomological Society, 52, 297-308. |
| [92] | Shivanna KR (2014). Biotic pollination: How plants achieve conflicting demands of attraction and restriction of potential pollinators//Ramawat KG, Merillon JM, Shivanna KR. Reproductive Biology of Plants. CRC Press, Baca Raton. |
| [93] | Stebbins GL (1970). Adaptive radiation of reproductive characteristics in angiosperms, I: Pollination mechanisms. Annual Review of Ecology and Systematics, 1, 307-326. |
| [94] | Steiner KE (1996). Chromosome numbers and relationships in tribe Hemimerideae (Scrophulariaceae). Systematic Botany, 21, 63-76. |
| [95] | Steiner KE, Whitehead VB (1988). The association between oil-producing flowers and oil-collecting bees in the Drakensberg of southern Africa. Monogr. Monographs in Systematic Botany from the Missouri Botanical Garden, 25, 259-277. |
| [96] | Steiner KE, Whitehead VB (1990). Pollinator adaptation to oil-secreting flowers—Rediviva and Diascia. Evolution, 44, 1701-1707. |
| [97] | Stpiczyńska M, Matusiewicz J (2001). Anatomy and ultrastructure of spur nectary of Gymnadenia conopsea (L.) Orchidaceae. Acta Societatis Botanicorum Poloniae, 70, 267-272. |
| [98] | Suddee S, Paton A, Parnell J, Puudjaa P, Keiwbang W, Rueangruea S (2019). Five new species of Platostoma (Lamiaceae) from North-Eastern Thailand. Thai Forest Bulletin (Botany), 47, 226-240. |
| [99] | Suetsugu K, Fukushima S (2014). Bee pollination of the endangered orchid Calanthe discolor through a generalized food-deceptive system. Plant Systematics and Evolution, 300, 453-459. |
| [100] | Suetsugu K, Naito RS, Fukushima S, Kawakita A, Kato M (2015). Pollination system and the effect of inflorescence size on fruit set in the deceptive orchid Cephalanthera falcata. Journal of Plant Research, 128, 585-594. |
| [101] | Sutton DA (1988). A Revision of the Tribe Antirrhineae. Oxford University Press, Oxford. |
| [102] | Svensson MG, Rydell J, T?ve J (1998). Deep flowers for long tongues. Trends in Ecology & Evolution, 13, 259-260. |
| [103] | Szlachetko DL (1995). Eltroplectris brachycentron Szlachetko (Orchidaceae), a new orchid species from Bolivia. Novon, 5, 375-378. |
| [104] | Teoh ES (2022). Orchid Species from Himalaya and Southeast Asia Vol. 3 (R-Z). Springer Press, Berlin. |
| [105] | The Angiosperm Phylogeny Group (2016). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181, 1-20. |
| [106] | Thompson JN (1999). Specific hypotheses on the geographic mosaic of coevolution. The American Naturalist, 153, S1-S14. |
| [107] | Travers SE, Temeles EJ, Pan I (2003). The relationship between nectar spur curvature in jewelweed (Impatiens capensis) and pollen removal by hummingbird pollinators. Canadian Journal of Botany, 81, 164-170. |
| [108] | van der Niet, Jürgens A, Johnson SD (2010). Pollinators, floral morphology and scent chemistry in the southern African orchid genus Schizochilus. South African Journal of Botany, 76, 726-738. |
| [109] | Vandelook F, Janssens SB, Gijbels P, Fischer E, van den Ende W, Honnay O, Abrahamczyk S (2019). Nectar traits differ between pollination syndromes in Balsaminaceae. Annals of Botany, 124, 269-279. |
| [110] | Vargas P, Liberal I, Ornosa C, Gómez JM (2017). Flower specialisation: the occluded corolla of snapdragons (Antirrhinum) exhibits two pollinator niches of large long-tongued bees. Plant Biology, 19, 787-797. |
| [111] | Venter H, Johannes T (1979). A Monograph of Monsonia L. (Geraniaceae). Springer Press, Berlin. |
| [112] | Vogel S (1984). The Diascia flower and its bee—An oil-based symbiosis in southern Africa. Acta Botanica Neerlandica, 33, 509-518. |
| [113] | Wang Q, Li YX, Pu XZ, Zhu LY, Tang Z, Liu Q (2013). Pollinators and nectar robbers cause directional selection for large spur circle in Impatiens oxyanthera (Balsaminaceae). Plant Systematics and Evolution, 299, 1263-1274. |
| [114] | Wang XY, Tang XX, Tong ZY, Huang SQ (2019). Geographic mosaic theory of coevolution in plant and pollinator interaction: process, evidence, prospect. Chinese Science Bulletin, 64, 1702-1710. |
| [114] | [王晓月, 汤晓辛, 童泽宇, 黄双全 (2019). 植物与传粉者地理镶嵌的协同演化: 过程、证据与展望. 科学通报, 64, 1702-1710.] |
| [115] | Waser NM (1988). Comparative pollen and dye transfer by pollinators of Delphinium nelsonii. Functional Ecology, 2, 41-48. |
| [116] | Wasserthal LT (1997). The pollinators of the Malagasy star orchids Angraecum sesquipedale, A. sororium and A. compactum and the evolution of extremely long spurs by pollinator shift. Botanica Acta, 110, 343-359. |
| [117] | Watthana S (2007). The genus Pomatocalpa (Orchidaceae) a taxonomic monograph. Harvard Papers in Botany, 11, 207-256. |
| [118] | Weryszko-Chmielewska E, Bo?ek M (2008). Structure of trichomatous nectaries in flowers of Lonicera kamtschatica (Sevast.) Pojark. Acta Agrobotanica, 61, 13-26. |
| [119] | Whittall JB, Hodges SA (2007). Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature, 447, 706-709. |
| [120] | Xie SY, Hou XQ, Zhang XH (2022). Are the spurs more complex than other petal types in Epimedium? Evidence from development, micromorphology, and nectary structure. Flora, 293, 152101. DOI: 10.1016/j.flora.2022.152101. |
| [121] | Yang ML, Wang LL, Zhang GP, Meng LH, Yang YP, Duan YW (2018). Equipped for migrations across high latitude regions? Reduced spur length and outcrossing rate in a biennial Halenia elliptica (Gentianaceae) with mixed mating system along a latitude gradient. Frontiers in Genetics, 9, 223. DOI: 10.3389/fgene.2018.00223. |
| [122] | Young HJ (2008). Selection on spur shape in Impatiens capensis. Oecologia, 156, 535-543. |
| [123] | Yousefi N, Zarre S, Heubl G (2016). Molecular phylogeny of the mainly Mediterranean genera Chaenorhinum, Kickxia and Nanorrhinum (Plantaginaceae, tribe Antirrhineae), with focus on taxa in the Flora Iranica region. Nordic Journal of Botany, 34, 455-463. |
| [124] | Zhang R, Min Y, Holappa LD, Walcher-Chevillet CL, Duan XS, Donaldson E, Kong HZ, Kramer EM (2020). A role for the Auxin Response Factors ARF6 and ARF8 homologs in petal spur elongation and nectary maturation in Aquilegia. New Phytologist, 227, 1392-1405. |
| [125] | Zhang YW, Wang Y, Guo YH (2006). The effects of nectar robbing on plant reproduction and evolution. Chinese Journal of Plant Ecology (Chinese Version), 30, 695-702. |
| [125] | [张彦文, 王勇, 郭友好 (2006). 盗蜜行为在植物繁殖生态学中的意义. 植物生态学报, 30, 695-702.] |
| [126] | Zhao L, Gong JZ, Zhang XH, Liu TQ, Ma X, Ren Y (2016). Floral organogenesis in Urophysa rockii, a rediscovered endangered and rare species of Ranunculaceae. Botany, 94, 215-224. |
| [127] | Zou X, Fountain DW, Morgan ER (2001). Anatomical and morphological studies of seed development in Sandersonia aurantiaca (Hook.). South African Journal of Botany, 67, 183-192. |
/
| 〈 |
|
〉 |
