A review for the pollinators of Papilionaceous flowers

Öz

The evolution of keel flowers within Fabaceae, Polygalaceae and some other clades of angiosperms is attributed to skilled and strong bees. However, whether this is true or not, is still an open question. Therefore, the literature is surveyed for the Hymenopteran pollinators of keel flowers, for 119 sources and for 112 species, six genera and two tribes for five characters which are the size of the flowers, Hymenopteran flower visitors/pollinators, size of the Hymenopteran pollinators, pollen and nectar robbers/thieves and size of the Hymenopteran thieves/robbers. The results suggest that Fabales keel flowers are mainly pollinated by long-tongued bees, from Apidae and Megachilidae families; and the most common pollinators of the keel flowers are small Megachile and Osmia; medium-sized Apis, Anthophora and Eucera; and large Xylocopa, Bombus and Centris. While the literature suggests that keel flowers are pollinated by skilled and strong bees, the results of the current review have shown that this is not the whole case in terms of flower size and bee size. There is no difference between pollinator diversity and flower size. While floral robbers/thieves are mostly up to 2 cm, among them honey-bees (Apis mellifera) both pollinate and rob the keel flowers. Keel flowers of Polygalaceae and other angiosperm lineages are somehow similar to the keel flowers of Papilionoideae.

Anahtar Kelimeler

• Bee pollination
• flower type
• pollinator size
• Polygalaceae
• Fabaceae

Kelebek şeklinde çiçek açan çiçeklerin tozlayıcıları için bir inceleme

Öz

Baklagil çiçek tipinin Fabaceae, Polygalaceae ve diğer angiosperm gruplarındaki evriminin becerikli ve güçlü arılar sayesinde olduğu fikri ortaya atılmıştır. Ancak, bunun doğruluğu tartışmalıdır. Bu nedenle, bu derlemede toplam 119 kaynak (112 tür, altı cins ve iki tribe) beş karakter (çiçek büyüklüğü, Hymenoptoran polinatörleri, Hymenoptoran polinatörlerinin büyüklüğü, polen ve nektar hırsızları, Hymenoptoran polen ve nektar hırsızlarının büyüklüğü) açısından değerlendirilmiştir. Derlemenin sonuçları göstermiştir ki, Fabales baklagil çiçekleri temelde Apidae and Megachilidae familyalarından uzun dilli arılar ile döllenmekte, ve en yaygın polinatörler ise küçük Megachile ve Osmia; orta boylu Apis, Anthophora ve Eucera; ve büyük Xylocopa, Bombus ve Centris’dir. Literatur, baklagil çiçeklerinin becerikli ve büyük arılarla döllendiğini önerirken, bu derlemenin sonuçları çiçek ve polinatör büyüklüğü açısından bunun tam anlamıyla doğru olmadığını göstermiştir. Ayrıca, çiçek büyüklüğü ve polinatör çeşitliliği arasında da bir bağlantı görülmemiştir. Çiçek hırsızları genelde 2 cm’ye kadar olurken, bunların arasında bal arılarının (Apis mellifera) hem hırsız hem de polinatör olarak işlev gördüğü anlaşılmıştır. Diğer taraftan, Polygalaceae ve diğer angiosperm baklagil benzeri çiçeklerin gerçek baklagil çiçeklerine polinatör açısından benzer olduğu görülmüştür.

Anahtar Kelimeler

• Arı tozlaşması,
• çiçek tipi,
• Fabaceae,
• tozlayıcı boyutu,
• Polygalaceae

Kaynakça

1. Alemán M, Figueroa-Fleming T, Etcheverry Á, Sühring S, Ortega-Baes P (2014). The explosive pollination mechanism in Papilionoideae (Leguminosae): An analysis with three Desmodium species. Plant Systematics and Evolution, 300(1): 177–186. https://doi.org/10.1007/s00606-013-0869-8
2. Amaral-Neto LP, Westerkamp C, Melo GA (2015). From keel to inverted keel flowers: functional morphology of “upside down” papilionoid flowers and the behavior of their bee visitors. Plant Systematics and Evolution, 301(9): 2161-2178.
3. Aouar-Sadli M, Louadi K, Doum SE (2008). Pollination of the broad bean (Vicia faba L. var. major) (Fabaceae) by wild bees and honey bees (Hymenoptera: Apoidea) and its impact on the seed production in the Tizi-Ouzou area (Algeria). African Journal of Agricultural Research, 3(4): 266-272.
4. Arceo-Gómez G, Martínez ML, Parra-Tabla V, García-Franco JG (2012). Floral and reproductive biology of the Mexican endemic Chamaecrista chamaecvistoides (Fabaceae). The Journal of the Torrey Botanical Society, 260-269.
5. Armbruster WS (1980). Pollination relationships between four sympatric species of Collinsia (Scrophulariaceae). Botanical Society of America Miscellaneous Series, 158(8).
6. Armbruster WS (1993). Evolution of plant pollination systems: hypotheses and tests with the neotropical vine Dalechampia. Evolution, 47(5): 1480-1505.
7. Armbruster WS, Mulder CPH, Baldwin BG, Kalisz S, Wessa B, Nute H (2002). Comparative analysis of late floral development and mating‐system evolution in tribe Collinsieae (Scrophulariaceae s.l.). American Journal of Botany, 89(1): 37–49.
8. Aronne G, Giovanetti M, De Micco V (2012). Morphofunctional traits and pollination mechanisms of Coronilla emerus L. flowers (Fabaceae) . The Scientific World Journal, 1–8. https://doi.org/10.1100/2012/381575

9. Arroyo K (1981). Breeding systems and pollination biology in Leguminosae. In: Polhill RM and Raven PH, eds. Advances in Legume Systematics. Part 2, Royal Botanic Gardens, Kew, 723-769.
10. Asmussen CB (1993). Pollination biology of the sea pea, Lathyrus japonicus: floral characters and activity and flight patterns of bumblebees. Flora (Jena), 188(2): 227–237. https://doi.org/10.1016/S0367-2530(17)32270-3
11. Bauer AA, Clayton MK, Brunet J (2017). Floral traits influencing plant attractiveness to three bee species: Consequences for plant reproductive success. American Journal of Botany, 104(5): 772–781. https://doi.org/10.3732/ajb.1600405
12. Bello MA, Hawkins JA, Rudall PJ (2007). Floral morphology and development in Quillajaceae and Surianaceae (Fabales), the species-poor relatives of Leguminosae and Polygalaceae. Annals of Botany, 100(7): 1491–1505. https://doi.org/10.1093/aob/mcm228
13. Bello MA, Hawkins JA, Rudall PJ (2010). Floral ontogeny in Polygalaceae and its bearing on the homologies of keeled flowers in Fabales. International Journal of Plant Sciences, 171(5): 482–498. https://doi.org/10.1086/651945
14. Bello MA, Rudall PJ, Hawkins JA (2012). Combined phylogenetic analyses reveal interfamilial relationships and patterns of floral evolution in the eudicot order Fabales. Cladistics, 28(4): 393-421.
15. Benitez-Vieyra S, De Ibarra NH, Wertlen AM, Cocucci AA (2007). How to look like a mallow: Evidence of floral mimicry between Turneraceae and Malvaceae. Proceedings of the Royal Society B: Biological Sciences, 274(1623): 2239–2248. https://doi.org/10.1098/rspb.2007.0588
16. Bernhardt CE, Mitchell RJ, Michaels HJ (2008). Effects of population size and density on pollinator visitation, pollinator behavior, and pollen tube abundance in Lupinus perennis. International Journal of Plant Sciences, 169(7): 944–953. https://doi.org/10.1086/589698
17. Breteler FJ, Smissaert Houwing AAS (1977). Revision of Atroxima Stapf and Carpolobia G. Don (Polygalaceae). Meded. Landbouwhogesch. Wageningen, 77: 1-45.
18. Borges LA, Sobrinho MS, Lopes AV (2009). Phenology, pollination, and breeding system of the threatened tree Caesalpinia echinata Lam. (Fabaceae), and a review of studies on the reproductive biology in the genus. Flora: Morphology, Distribution, Functional Ecology of Plants, 204(2): 111–130. https://doi.org/10.1016/j.flora.2008.01.003
19. Brantjes NBM (1982). Pollen placement and reproductive isolation between two brazilian Polygala species (Polygalaceae). Plant Systematics and Evolution, 141(1): 41–52. https://doi.org/10.1007/BF01006478
20. Bruneau A, Anderson GJ (1988). Reproductive biology of diploid and triploid Apios americana (Leguminosae). American Journal of Botany, 75(12): 1876-1883.
21. Bruneau A, Anderson GJ (1994). To bee or not to bee?: The pollination biology of Apios americana (Leguminosae). Plant Systematics and Evolution, 192(1–2): 147–149. https://doi.org/10.1007/BF00985913
22. Cane JH (2006). An Evaluation of Pollination Mechanisms for Purple Prairie-clover, Dalea purpurea (Fabaceae: Amorpheae). The American Midland Naturalist, 156(1): 193–197. https://doi.org/10.1674/0003-0031(2006)156[193:aeopmf]2.0.co;2
23. Cardel Y (2004). Linking herbivory and pollination: costs and selection implications in Centrosema virginianum Bentham (Fabaceae: Papilionoideae). https://doi.org/10.25148/etd.FI14052571
24. Carleial S, Delgado-Salinas A, Domínguez CA, Terrazas T (2015). Reflexed flowers in Aeschynomene amorphoides (Fabaceae: Faboideae): A mechanism promoting pollination specialization? Botanical Journal of the Linnean Society, 177(4): 657–666. https://doi.org/10.1111/boj.12264
25. Castro S, Loureiro J, Ferrero V, Silveira P, Navarro L (2013). So many visitors and so few pollinators: Variation in insect frequency and effectiveness governs the reproductive success of an endemic milkwort. Plant Ecology, 214(10): 1233–1245. https://doi.org/10.1007/s11258-013-0247-1
26. Castro S, Silveira P, Navarro L (2008a). Effect of pollination on floral longevity and costs of delaying fertilization in the out-crossing Polygala vayredae Costa (Polygalaceae). Annals of Botany, 102(6): 1043–1048. https://doi.org/10.1093/aob/mcn184
27. Castro S, Silveira P, Navarro L (2008b). How flower biology and breeding system affect the reproductive success of the narrow endemic Polygala vayredae Costa (Polygalaceae). Botanical Journal of the Linnean Society, 157(1): 67-81.
28. Cercis orbiculata. Retrieved April, 2016 from https://www.fs.fed.us/database/feis/plants/shrub/cerorb/all.html. Chittka L, Thomson JD, Waser NM (1999). Flower constancy, insect psychology, and plant evolution. Naturwissenschaften, 86: 361-377.
29. Conner JK, Rush S (1996). Effects of flower size and number on pollinator visitation to wild radish, Raphanus raphanistrum. Oecologia, 105(4): 509–516. https://doi.org/10.1007/BF00330014
30. Córdoba SA, Cocucci AA (2011). Flower power: Its association with bee power and floral functional morphology in papilionate legumes. Annals of Botany, 108(5): 919–931. https://doi.org/10.1093/aob/mcr196
31. Cristofolini G, Galloni M, Podda L, Vivarelli D (2012). Pollination ecology provides some new insight into evolution and systematics of Mediterranean Legumes. Bocconea, 24: 22–26.
32. Dafni A, Lehrer M, Keyan PG (1997). Spatial flower parameters and insect spatial vision. Biological Reviews, 72(2): 239–282. https://doi.org/10.1111/j.1469-185X.1997.tb00014.x
33. de Souza JMT, Snak C, Varassin IG (2017). Floral divergence and temporal pollinator partitioning in two synchronopatric species of Vigna (Leguminosae-Papilionoideae). Arthropod-Plant Interactions, 11(3): 285–297. https://doi.org/10.1007/s11829-017-9498-4
34. Dulberger R, Smith MB, Bawa KS (1994). The stigmatic orifice in Cassia, Senna, and Chamaecrista (Caesalpiniaceae): morphological variation, function during pollination, and possible adaptive significance. American Journal of Botany, 81(11): 1390-1396.
35. Elle E, Carney R (2003). Reproductive assurance varies with flower size in Collinsia parviflora (Scrophulariaceae). American Journal of Botany, 90(6): 888-896.
36. Endress PK (1994). Floral structure and evolution of primitive angiosperms: Recent advances. Plant Systematics and Evolution, 192(1–2): 79–97. https://doi.org/10.1007/BF00985910
37. Etcheverry AV, Protomastro JJ, Westerkamp C (2003). Delayed autonomous self-pollination in the colonizer Crotalaria micans (Fabaceae: Papilionoideae): Structural and functional aspects. Plant Systematics and Evolution, 239(1–2): 15–28. https://doi.org/10.1007/s00606-002-0244-7
38. Etcheverry AV, Alemán MM, Fleming TF (2008). Flower morphology, pollination biology and mating system of the complex flower of Vigna caracalla (Fabaceae: Papilionoideae). Annals of Botany, 102(3): 305–316. https://doi.org/10.1093/aob/mcn106
39. Etcheverry AV, Vogel S (2018). Interactions between the asymmetrical flower of Cochliasanthus caracalla (Fabaceae: Papilionoideae) with its visitors. Flora: Morphology, Distribution, Functional Ecology of Plants, 239: 141–150. https://doi.org/10.1016/j.flora.2017.10.006
40. Eynard C, Galetto L (2002). Pollination ecology of Geoffroea decorticans (Fabaceae) in central Argentine dry forest. Journal of Arid Environments, 51(1): 79–88. https://doi.org/10.1006/jare.2001.0923
41. Faegri K, van Der Pijl L (1979). The Principles of Pollination Ecology. Pergamon Press, Oxford.
42. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics, 35: 375-403.
43. Galloni M, Cristofolini G (2003). Floral rewards and pollination in Cytiseae (Fabaceae). Plant Systematics and Evolution, 238(1–4): 127–137. https://doi.org/10.1007/s00606-002-0270-5
44. Galloni M, Podda L, Vivarelli D, Quaranta M, Cristofolini G (2008). Visitor diversity and pollinator specialization in Mediterranean legumes. Flora: Morphology, Distribution, Functional Ecology of Plants, 203(1): 94–102. https://doi.org/10.1016/j.flora.2006.12.006
45. Gegear RJ (2005). Multicomponent floral signals elicit selective foraging in bumblebees. Naturwissenschaften, 92(6): 269-271.
46. Gegear RJ, Laverty TM (2005). Flower constancy in bumblebees: A test of the trait variability hypothesis. Animal Behaviour, 69(4): 939–949. https://doi.org/10.1016/j.anbehav.2004.06.029
47. Gélvez-Zúñiga I, Neves AC, Teixido AL, Fernandes GW (2018). Reproductive biology and floral visitors of Collaea cipoensis (Fabaceae), an endemic shrub of the rupestrian grasslands. Flora: Morphology, Distribution, Functional Ecology of Plants, 238: 129–137. https://doi.org/10.1016/j.flora.2017.03.012
48. Giovanetti M, Aronne G( 2012). Honey bee handling behaviour on the papilionate flower of Robinia pseudoacacia L. Arthropod-Plant Interactions, 7(1): 119–124. https://doi.org/10.1007/s11829-012-9227-y Gomes da Silva AL, Chaves SR, Brito JM (2011). Reproductive biology of Bowdichia virgilioides Kunth (Fabaceae). Acta Scientiarum. Biological Sciences, 33(4): 463-470. https://doi.org/10.4025/actascibiolsci.v33i4.9003
49. Gottsberger G, Silberbauer-Gottsberger I (1988). Evolution of flower structures and pollination in neotropical Cassiinae (Caesalpiniaceae) species. Phyton, 28:293–320.
50. Goulson D (1999). Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspectives in Plant Ecology, Evolution and Systematics, 2(2): 185-209.
51. Gross CL (2001). The effect of introduced honeybees on native bee visitation and fruit-set in Dillwynia juniperina (Fabaceae) in a fragmented ecosystem. Biological Conservation, 102(1): 89–95. https://doi.org/10.1016/S0006-3207(01)00088-X
52. Gumbert A, Kunze J (1999). Inflorescence height affects visitation behavior of bees - A case study of an aquatic plant community in Bolivia. Biotropica, 31(3): 466–477. https://doi.org/10.1111/j.1744-7429.1999.tb00389.x
53. Hall HG, Avila L (2016). Megachile sculpturalis, the giant resin bee, overcomes the blossom structure of sunn hemp (Crotalaria juncea) that impedes pollination. Journal of Melittology, (65): 1-11.
54. Harder LD (1983). Functional differences of the proboscides of short-and long-tongued bees (Hymenoptera, Apoidea). Canadian Journal of Zoology, 61(7): 1580-1586.
55. Hargreaves AL, Harder LD, Johnson SD (2009). Consumptive emasculation: The ecological and evolutionary consequences of pollen theft. Biological Reviews, 84(2): 259–276. https://doi.org/10.1111/j.1469-185X.2008.00074.x
56. Hattori M, Nagano Y, Itino T (2015). Geographic variation in flower size and flower-visitor composition of two bumblebee-pollinated, spring-flowering herbs, Lamium album L. var. barbatum (Lamiaceae) and Meehania urticifolia (Lamiaceae). American Journal of Plant Sciences, 6(05): 737.
57. Heering JH (1995). Botanical and Agronomic Evaluation of a Collection of Sesbania sesban and Related Perennial Species. Landbouw Universiteit Wageningen, Netherlands.
58. Henning JA, Peng YS, Montague MA, Teuber LR (1992). Honey bee (Hymenoptera: Apidae) behavioral response to primary alfalfa (Rosales: Fabaceae) floral volatiles. Journal of Economic Entomology, 85(1): 233-239.
59. Herrera J (2001). The variability of organs differentially involved in pollination, and correlations of traits in Genisteae (Leguminosae: Papilionoideae). Annals of Botany, 88(6): 1027–1037. https://doi.org/10.1006/anbo.2001.1541
60. Hingston AB (1999). Affinities between southern Tasmanian plants in native bee visitor profiles. Australian Journal of Zoology, 47(4): 361-384.
61. Hingston AB, McQuillan PB (2000). Are pollination syndromes useful predictors of floral visitors in Tasmania? Austral Ecology, 25(6): 600-609.
62. Howell GJ, Slater AT, Knox RB (1993). Secondary pollen presentation in angiosperms and its biological significance. Australian Journal of Botany, 41(5): 417-438.
63. Jacobi CM, Ramalho M, Silva M (2005). Pollination biology of the exotic rattleweed Crotalaria retusa L. (Fabaceae) in NE Brazil. Biotropica, 37(3): 357–363. https://doi.org/10.1111/j.1744-7429.2005.00047.x
64. Johnson SD, Alexandersson R, Linder HP (2003). Experimental and phylogenetic evidence for floral mimicry in a guild of fly-pollinated plants. Biological Journal of the Linnean Society, 80(2): 289–304. https://doi.org/10.1046/j.1095-8312.2003.00236.x
65. Johnson SD, Jürgens A (2010). Convergent evolution of carrion and faecal scent mimicry in fly-pollinated angiosperm flowers and a stinkhorn fungus. South African Journal of Botany, 76(4): 796–807. https://doi.org/10.1016/j.sajb.2010.07.012
66. Kampny CM (1995). Pollination and flower diversity in Scrophulariaceae. The Botanical Review, 61(4): 350-366. Kožuharova E, Firmage D (2009). Notes on the reproductive biology of Astragalus dasyanthus Pall. (Fabaceae) a rare plant for Bulgaria. Comptes rendus de l’Académie bulgare des Sciences, 62(9): 1079-1088.
67. Leppik EE (1966). Floral evolution and pollination in the Leguminosae. Annales Botanici Fennici 3: 299 -308.
68. Lewis G (2005). Caesalpinieae. In Legumes of the world, G Lewis, B Schrire, B Mackinder and M Lock (eds.). Royal Botanic Gardens, Kew, Richmond, U.K. p. 127-161
69. Lihoreau M, Ings TC, Chittka L, Reynolds AM (2016). Signatures of a globally optimal searching strategy in the three-dimensional foraging flights of bumblebees. Scientific Reports, 6(1):1-13.
70. Lloyd DG, Schoen DJ (1992). Self-and cross-fertilization in plants. I. Functional Dimensions. International Journal of Plant Sciences, 153(3, Part 1), 358-369.
71. LPWG (2017). A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon, 66 (1): 44-77.
72. Malo JE, Baonza J (2002). Are there predictable clines in plant–pollinator interactions along altitudinal gradients? The example of Cytisus scoparius (L.) Link in the Sierra de Guadarrama (Central Spain). Diversity and Distributions, 8(6): 365-371.
73. Maloof JE, Inouye DW (2000). Are nectar robbers cheaters or mutualists? Ecology, 81(10): 2651-2661.
74. Mayer C, Dehon C, Gauthier AL, Naveau O, Rigo C, Jacquemart AL (2014). Nectar robbing improves male reproductive success of the endangered Aconitum napellus ssp. lusitanicum. Evolutionary Ecology, 28(4): 669–685. https://doi.org/10.1007/s10682-014-9696-9
75. McMahon M, Hufford L (2005). Evolution and development in the amorphoid clade (Amorpheae: Papilionoideae: Leguminosae): petal loss and dedifferentiation. International Journal of Plant Sciences, 166: 383-396.
76. Meireles AC, Queiroz JA, Quirino ZGM (2015). Mecanismo explosivo de polinização em Periandra mediterranea (Vell.) Taub. (Fabaceae) na Reserva Biológica Guaribas, Paraíba, Brasil. Biotemas, 28(4): 71-81.
77. Muir J (2013). Scotch Broom (Cytisus scoparius, Fabaceae) and the Pollination and Reproductive Success of Three Garry Oak-Associated Plant Species. University of Calgary, Canada.
78. Myczko Ł, Banaszak-Cibicka W, Sparks TH, Tryjanowski P (2015). Do queens of bumblebee species differ in their choice of flower colour morphs of Corydalis cava (Fumariaceae)? Apidologie, 46(3): 337–345. https://doi.org/10.1007/s13592-014-0326-x
79. Navarro L (2000). Pollination ecology of Anthyllis vulneraria subsp. vulgaris (Fabaceae): nectar robbers as pollinators. American Journal of Botany, 87(7): 980-985.
80. Ne'eman G, Nesher R (1995). Pollination ecology and the significance of floral color change in Lupinus pilosos L. (Fabaceae). Israel Journal of Plant Sciences, 43(2): 135-145.
81. Ogilvie JE, Zalucki JM, Boulter SL (2009). Pollination biology of the sclerophyllous shrub Pultenaea villosa willd. (Fabaceae) in southeast Queensland, Australia. Plant Species Biology, 24(1): 11–19. https://doi.org/10.1111/j.1442-1984.2009.00235.x
82. Olesen JM (1996). From naivete to experience: bumblebee queens (Bombus terrestris) foraging on Corydalis cava (Fumariaceae). Journal of the Kansas Entomological Society, 274-286.
83. Ollerton J, Watts S (2000). Phenotype space and floral typology: towards an objective assessment of pollination syndromes. Det Norske Videnskaps-Akademi. I. Matematisk-Naturvidenskapelige Klasse, Skrifter, Ny Serie, 39: 149-159.
84. Pando JB, Fohouo FNT, Tamesse JL (2011). Foraging and pollination behaviour of Xylocopa calens Lepeletier (Hymenoptera: Apidae) on Phaseolus coccineus L. (Fabaceae) flowers at Yaounde (Cameroon). Entomological Research, 41(5): 185–193. https://doi.org/10.1111/j.1748-5967.2011.00334.x
85. Parker IM (1997). Pollinator limitation of Cytisus scoparius (Scotch broom), an invasive exotic shrub. Ecology, 78(5): 1457-1470.
86. Parker IM, Engel A, Haubensak KA, Goodell K (2002). Pollination of Cytisus scoparius (Fabaceae) and Genista monspessulana (Fabaceae), two invasive shrubs in California. Madroño, 25-32.
87. Pennington RT, Klitgaard BB, Ireland H, Lavin M (2000). New insights into floral evolution and basal Papilionoideae from molecular phylogenies. In: Herendeen PS and Bruneau A. eds. Advances in Legume Systematics: Part, 9, Royal Botanic Gardens, Kew, 233-248.
88. Persson C (2001). Phylogenetic relationships in Polygalaceae based on plastid DNA sequences from the trnL-F region. Taxon, 763-779.
89. Peter CI, Johnson SD (2008). Mimics and magnets: The importance of color and ecological facilitation in floral deception. Ecology, 89(6): 1583–1595. https://doi.org/10.1890/07-1098.1
90. Polhill RM, Raven PH (1981). Advances in Legume Systematics. Parts 1 and 2, Royal Botanic Gardens, Kew.
91. Polhill RM, Raven PH, Stirton C (1981). Evolution and systematics of the Leguminosae. In: Polhill RM and Raven PH. eds. Advances in Legume Systematics, Part 1, Royal Botanical Gardens, Kew, 1-26.
92. Primack RB, Inouye DW (1993). Factors affecting pollinator visitation rates: a biogeographic comparison. Current Science, (65): 257-262.
93. Proctor M, Yeo P, Lack A (1996). The Natural History of Pollination. Harper Collins Publishers, London, UK.
94. Queiroz LDE (1996). Pollination ecology studies in Cratylia Mart. ex Benth.(Leguminosae: Papilionoideae) and its taxonomic and evolutionary implications. Sitientibus (UEFS), (15): 119–131.
95. Rafferty NE, Ives AR (2013). Phylogenetic trait-based analyses of ecological networks. Ecology, 94(10): 2321–2333. https://doi.org/10.1890/12-1948.1
96. Raine NE, Chittka L (2007). The adaptive significance of sensory bias in a foraging context: floral colour preferences in the bumblebee Bombus terrestris. PLoS ONE, 2(6): 1–8. https://doi.org/10.1371/journal.pone.0000556
97. Raju AJS, Rao CP (2016). Pollination mechanism and pollinators of the endemic plant Rhynchosia beddomei Baker. International Journal of Botany Studies, 1(7): 1–3.
98. Ramalho M, Silva M, Carvalho G (2014). Pollinator sharing in specialized bee pollination systems: A test with the synchronopatric lip flowers of Centrosema Benth. (Fabaceae). Sociobiology, 61(2): 189–197. https://doi.org/10.13102/sociobiology.v61i2.189-197
99. Robertson C (1928). Flowers and insects. Lists of visitors of 453 flowers. The Science Press Printing Company, Lancaster, PA.
100. Rodríguez-Riaño T (2004). Reproductive biology in Cytisus multiflorus (Fabaceae). Annales Botanici Fennici, 41: 179–188.
101. Rossi M, Fisogni A, Nepi M, Quaranta M, Galloni M (2014). Bouncy versus idles: On the different role of pollinators in the generalist Gentiana lutea L. Flora: Morphology, Distribution, Functional Ecology of Plants, 209(3–4): 164–171. https://doi.org/10.1016/j.flora.2014.02.002
102. Rust RW, Clement SL (1977). Entomophilous pollination of the self-compatible species Collinsia sparsiflora Fisher and Meyer. Journal of the Kansas Entomological Society, 37-48.
103. Sahai K (2009). Reproductive biology of two species of Canavalia DC. (Fabaceae)-A non-conventional wild legume. Flora: Morphology, Distribution, Functional Ecology of Plants, 204(10): 762–768. https://doi.org/10.1016/j.flora.2008.11.005
104. Schiestl FP, Johnson SD (2013). Pollinator-mediated evolution of floral signals. Trends in Ecology and Evolution, 28(5): 307–315. https://doi.org/10.1016/j.tree.2013.01.019
105. Schrire BD (1989). A multidisciplinary approach to pollination biology in the Leguminosae. Advances in Legume Biology. Monographs in Systematic Botany from the Missouri Botanical Garden, 29, 183-242.
106. Shambhu B (2013). Studies on flower visitors of field bean Lablab purpureus (L.) Sweet and their role in pollination and pod set. University of Agricultural Sciences, GKVK, India.
107. Shi X, Wang JC, Zhang DY, Gaskin JF, Pan BR (2010). Pollination ecology of the rare desert species Eremosparton songoricum (Fabaceae). Australian Journal of Botany, 58(1): 35–41. https://doi.org/10.1071/BT09172
108. Shivanna KR (2014). Biotic pollination: how plants achieve conflicting demands of attraction and restriction of potential pollinators. Reproductive Biology of Plants, 218-267.
109. Skorupski P, Spaethe J, Chittka L (2006). Visual search and decision making in bees: time, speed, and accuracy. International Journal of Comparative Psychology, 19: 342-347.
110. Slagle MW, Hendrix SD (2009). Reproduction of Amorpha canescens (Fabaceae) and diversity of its bee community in a fragmented landscape. Oecologia, 161(4): 813–823. https://doi.org/10.1007/s00442-009-1429-3
111. Spaethe J, Tautz J, Chittka L (2001). Visual constraints in foraging bumblebees: flower size and color affect search time and flight behavior. Proceedings of the National Academy of Sciences, 98(7): 3898-3903.
112. Stanley D, Otieno M, Syeijven K, Berlin ES, Piironen T, Willmer P, Nuttman C (2016). Pollination ecology of Desmodium setigerum (Fabaceae) in Uganda; do big bees do it better? Journal of Pollination Ecology, 19 (7): 43-49.
113. Stirton CH (1977). The pollination of Canavalia virosa by Xylocopid and Magachilid bees. Bothalia, 12(2): 225-227.
114. Stout JC (2000). Does size matter? Bumblebee behaviour and the pollination of Cytisus scoparius L. (Fabaceae). Apidologie, 31(1): 129-139.
115. Stout JC, Kells AR, Goulson D (2002). Pollination of the invasive exotic shrub Lupinus arboreus (Fabaceae) by introduced bees in Tasmania. Biological Conservation, 106(3): 425–434. https://doi.org/10.1016/S0006-3207(02)00046-0
116. Streinzer M, Paulus HF, Spaethe (2009). Floral colour signal increases short-range detectability of a sexually deceptive orchid to its bee pollinator. Journal of Experimental Biology, 212(9): 1365–1370. https://doi.org/10.1242/jeb.027482
117. Suzuki N (2000). Pollinator limitation and resource limitation of seed production in the Scotch broom Cytisus scoparius (Leguminosae). Plant Species Biology, 187–193.
118. Tucker SC (2002). Floral ontogeny of Cercis (Leguminosae: Caesalpinioideae: Cercideae): does it show convergence with papilionoids? International Journal of Plant Sciences, 163(1): 75-87.
119. Tucker SC (2003). Update on floral development floral development in legumes. Plant Physiology, 131: 911–926. https://doi.org/10.1104/102.017459.center
120. Valido A, Dupont YL, Hansen DM (2002). Native birds and insects, and introduced honey bees visiting Echium wildpretii (Boraginaceae) in the Canary Islands. Acta Oecologica, 23(6): 413–419. https://doi.org/10.1016/S1146-609X(02)01167-0
121. van der Pijl L (1961). Ecological aspects of flower evolution. II. Zoophilous flower classes. Evolution, 15(1): 44-59.
122. Vivarelli D, Petanidou T, Nielsen A, Cristofolini G (2011). Small-size bees reduce male fitness of the flowers of Ononis masquillierii (Fabaceae), a rare endemic plant in the northern Apennines. Botanical Journal of the Linnean Society, 165(3): 267–277. https://doi.org/10.1111/j.1095-8339.2010.01105.x
123. Waddington KD (1979). Divergence in inflorescence height: an evolutionary response to pollinator fidelity. Oecologia, 40(1): 43-50.
124. Westerkamp C (1989). Von Pollenhaufen, Nudelspritzen und Pseudo-staubblättern. Blütenstaub aus zweiter Hand. Palmengarten, (53) 146-149.
125. Westerkamp C (1991). Honeybees are poor pollinators—why? Plant Systematics and Evolution, 177(1): 71-75.
126. Westerkamp C (1993). The co-operation between the asymmetric flower of Lathyrus latifolius (Fabaceae-Vicieae) and its flowers. Phyton, 33(1): 121–137.
127. Westerkamp C, Paul H (1993). Apios americana, a fly-pollinated papilionaceous flower? Plant Systematics and Evolution, 187(1-4): 135-144.
128. Westerkamp C (1996). Pollen in bee-flower relations some considerations on melittophily. Botanica Acta, 109: 325-332.
129. Westerkamp C (1997). Keel blossoms: bee flowers with adaptations against bees. Flora: Morphologie, Geobotanik, Oekophysiologie, 192:125-32.
130. Westerkamp C, Weber A (1997). Secondary and tertiary pollen presentation in Polygala myrtifolia and allies (Polygalaceae, South Africa). South African Journal of Botany, 63(5): 254–258. https://doi.org/10.1016/S0254-6299(15)30762-6
131. Westerkamp C, Weber A (1999). Keel flowers of the Polygalaceae and Fabaceae: a functional comparison. Botanical Journal of the Linnean Society, 129: 207-221.
132. Westerkamp C, Claßen-Bockhoff R (2007). Bilabiate flowers: The ultimate response to bees? Annals of Botany, 100(2): 361–374. https://doi.org/10.1093/aob/mcm123.
133. Zhang D, Xiang SHI, JianCheng Wang, Gaskin HLJF (2011). Breeding system and its consequence on fruit set of a rare sand dune shrub Eremosparton songoricum (Fabaceae: Papilionoideae). Implications for Conservation. 干旱区科学, 3(4): 231-239.