Abstract
Differences in floral morphology are often hypothesized to stem from selection by different pollinators. Thus, the presence of multiple floral color morphs within a species might indicate visitation by different pollinator species. To test this prediction, we examined Ipomoea aquatica Forssk., a morning glory species with a “white” morph (all-white flowers) and a “purple” morph (white corolla lobes with purple corolla tubes). We studied this species in Nong Khai, Thailand, where some populations are monomorphic for a single color and others are polymorphic. We compared (a) animal visitation rates to each morph; (b) visitor and pollinator community composition at each morph; and (c) the female reproduction of each morph. Visitation rates were obtained from camcorder footage and used to analyze community composition. Female reproduction was assessed from a pollination experiment with five treatments (open, open emasculation, hand-cross, hand-self, and closed). We found that the main pollinators (bees and butterflies) visited both morphs, and that overall insect community composition to the two floral colors did not differ significantly. Moreover, we found that I. aquatica is capable of spontaneous autogamy but still benefits from pollinators, as flowers in the closed treatment set significantly fewer seeds than flowers in the open and hand cross-pollinated treatments. When comparing female reproduction between morphs, we did not find significant differences for either fruit set or seed set. These findings suggest that floral visitors interact with the two morphs similarly, and that the high-reproductive success experienced by both colors may help maintain the polymorphism in nature.
Similar content being viewed by others
Availability of data
Data was uploaded to a public repository (Mendeley Data): https://dx.doi.org/10.17632/vrb7wsm69z.1.
References
Araujo LS, Medina AM, Gimenes M (2018) Pollination efficiency on Ipomoea bahiensis (Convolvulaceae): morphological and behavioural aspects of floral visitors. Iheringia Sér Zool 108:e2018012. https://doi.org/10.1590/1678-4766e2018012
Austin DF (2007) Water spinach (Ipomoea aquatica, Convolvulaceae): a food gone wild. Ethnobot Res Applic 5:123–146. https://doi.org/10.17348/era.5.0.123-146
Brown BA, Clegg MT (1984) Influence of flower color polymorphism on genetic transmission in a natural population of the common morning glory, Ipomoea purpurea. Evolution 38:796–803. https://doi.org/10.1111/j.1558-5646.1984.tb00352.x
Bullock SH, Ayala R, Baker I, Herbert GB (1987) Reproductive biology of the tree Ipomoea wolcottiana (Convolvulaceae). Madroño 34:304–314
Cant ET, Smith AD, Reynolds DR, Osborne JL (2005) Tracking butterfly flight paths across the landscape with harmonic radar. Proc Roy Soc London, Ser B, Biol Sci 272:785–790. https://doi.org/10.1098/rspb.2004.3002
Carlson JE, Holsinger KE (2010) Natural selection on inflorescence color polymorphisms in wild Protea populations: the role of pollinators, seed predators, and intertrait correlations. Amer J Bot 97:934–944. https://doi.org/10.3732/ajb.0900348
Chitchak N, Traiperm P, Staples G, Rattanakrajang P, Sumanon P (2018) Species delimitation of some Argyreia (Convolvulaceae) using phenetic analyses: insights from leaf anatomical data reveal a new species. Botany 96:217–233. https://doi.org/10.1139/cjb-2017-0108
de Santiago-Hernández MH, Martén-Rodríguez S, Lopezaraiza-Mikel M, Oyama K, González-Rodríguez A, Quesada M (2019) The role of pollination effectiveness on the attributes of interaction networks: from floral visitation to plant fitness. Ecology 100:e02803. https://doi.org/10.1002/ecy.2803
de Souza Pacheco Filho AJ, Westerkamp C, Freitas BM (2011) Ipomoea bahiensis pollinators: bees or butterflies? Flora 206:662–667. https://doi.org/10.1016/j.flora.2011.02.002
Devoto M, Medan D, Roig-Alsina A, Norberto HM (2009) Patterns of species turnover in plant-pollinator communities along a precipitation gradient in Patagonia (Argentina). Austral Ecol 34:848–857. https://doi.org/10.1111/j.1442-9993.2009.01987.x
Dyer AG, Boyd-Gerny S, Shrestha M, Lunau K, Garcia JE, Koethe S, Wong BB (2016) Innate colour preferences of the australian native stingless bee Tetragonula carbonaria Sm. J Comp Physiol A 202:603–613. https://doi.org/10.1007/s00359-016-1101-4
Dyer FC, Seeley TD (1991) Dance dialects and foraging range in three Asian honey bee species. Behav Ecol Sociobiol 28:227–233. https://doi.org/10.1007/BF00175094
Eckhart VM, Rushing NS, Hart GM, Hansen JD (2006) Frequency-dependent pollinator foraging in polymorphic Clarkia xantiana ssp. xantiana populations: implications for flower colour evolution and pollinator interactions. Oikos 112:412–421. https://doi.org/10.1111/j.0030-1299.2006.14289.x
Elam DR, Linhart YB (1988) Pollination and seed production in Ipomopsis aggregata: differences among and within flower color morphs. Amer J Bot 75:1262–1274. https://doi.org/10.1002/j.1537-2197.1988.tb14186.x
Ellis AG, Johnson SD (2009) The evolution of floral variation without pollinator shifts in Gorteria diffusa (Asteraceae). Amer J Bot 96:793–801. https://doi.org/10.3732/ajb.0800222
Epperson BK, Clegg MT (1987) Frequency-dependent variation for outcrossing rate among flower-color morphs of Ipomoea purpurea. Evolution 41:1302–1311. https://doi.org/10.1111/j.1558-5646.1987.tb02468.x
Eriksson O, Bremer B (1992) Pollination systems, dispersal modes, life forms, and diversification rates in angiosperm families. Evolution 46:258–266. https://doi.org/10.1111/j.1558-5646.1992.tb02000.x
Frey FM, Dunton J, Garland K (2011) Floral color variation and associations with fitness-related traits in Malva moschata (Malvaceae). Pl Spec Biol 26:235–243. https://doi.org/10.1111/j.1442-1984.2011.00325.x
Galetto L, Bernardello G (2004) Floral nectaries, nectar production dynamics and chemical composition in six Ipomoea species (Convolvulaceae) in relation to pollinators. Ann Bot (Oxford) 94:269–280. https://doi.org/10.1093/aob/mch137
Giurfa M, Vorobyev M, Kevan P, Menzel R (1996) Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts. J Comp Physiol A 178:699–709. https://doi.org/10.1007/BF00227381
Goulson D, Cory JS (1993) Flower constancy and learning in foraging preferences of the green-veined white butterfly Pleris napi. Ecol Entomol 18:315–320. https://doi.org/10.1111/j.1365-2311.1993.tb01107.x
Grant V (1949) Pollination systems as isolating mechanisms in angiosperms. Evolution 3:82–97. https://doi.org/10.2307/2405454
Grubben G, Denton O (2004) Plant resources of tropical Africa 2: vegetables. PROTA Foundation, Wageningen, Netherlands. Available at: http://edepot.wur.nl/417517. Accessed 16 Nov 2018
Gumbert A (2000) Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behav Ecol Sociobiol 48:36–43. https://doi.org/10.1007/s002650000213
Harwood E, Sytsma M (2003) Risk assessment for Chinese water spinach (Ipomoea aquatica) in Oregon. Center for Lakes and Reservoirs, Portland State University, Portland
Herrera CM (1988) Variation in mutualisms: the spatiotemporal mosaic of a pollinator assemblage. Biol J Linn Soc 35:95–125. https://doi.org/10.1111/j.1095-8312.1988.tb00461.x
Heystek A, Geerts S, Barnard P, Pauw A (2014) Pink flower preference in sunbirds does not translate into plant fitness differences in a polymorphic Erica species. Evol Ecol 28:457–470. https://doi.org/10.1007/s10682-014-9693-z
Janzen DH, Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season. Ecology 49:96–110. https://doi.org/10.2307/1933565
Keasar T, Bilu Y, Motro U, Shmida A (1997) Foraging choices of bumblebees on equally rewarding artificial flowers of different colors. Israel J Pl Sci 45:223–233. https://doi.org/10.1080/07929978.1997.10676686
Irwin RE, Strauss SY, Storz S, Emerson A, Guibert G (2003) The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84:1733–1743. https://doi.org/10.1890/0012-9658(2003)084%5b1733:TROHIT%5d2.0.CO;2
Ketjarun K, Staples GW, Swangpol SC, Traiperm P (2016) Micro-morphological study of Evolvulus spp. (Convolvulaceae): the old world medicinal plants. Bot Stud 57:25. https://doi.org/10.1186/s40529-016-0141-y
Klein A-M, Vaissiere BE, Cane JH, Steffan-Dewenter I (2006) Importance of pollinators in changing landscapes for world crops. Proc Roy Soc London, Ser B, Biol Sci 274:303–313. https://doi.org/10.1098/rspb.2006.3721
Leonard SA, Dornhaus A, Papaj RD (2011) Flowers help bees cope with uncertainty: signal detection and the function of floral complexity. J Exp Biol 214:113–121. https://doi.org/10.1242/jeb.047407
Maimoni-Rodella RCS, Yanagizawa YANP (2007) Floral biology and breeding system of three Ipomoea weeds. Pl Danin 25:35–42. https://doi.org/10.1590/S0100-83582007000100004
Malerba R, Nattero J (2012) Pollinator response to flower color polymorphism and floral display in a plant with a single-locus floral color polymorphism: consequences for plant reproduction. Ecol Res 27:377–385. https://doi.org/10.1007/s11284-011-0908-2
Meira M, Silva EPd, David JM, David JP (2012) Review of the genus Ipomoea: traditional uses, chemistry and biological activities. Rev Bras Farmacogn 22:682–713. https://doi.org/10.1590/S0102-695X2012005000025
Narbona E, Wang H, Ortiz P, Arista M, Imbert E (2018) Flower colour polymorphism in the Mediterranean Basin: occurrence, maintenance and implications for speciation. Pl Biol 1:8–20. https://doi.org/10.1111/plb.12575
Niovi Jones K, Reithel JS (2001) Pollinator-mediated selection on a flower color polymorphism in experimental populations of Antirrhinum (Scrophulariaceae). Amer J Bot 88:447–454. https://doi.org/10.2307/2657109
Ogunwenmo KO, Oyelana OA (2009) Biotypes of Ipomoea aquatica Forssk. (Convolvulaceae) exhibit ecogeographic and cytomorphological variations in Nigeria. Pl Biosystems 143:71–80. https://doi.org/10.1080/11263500802633618
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
Ortiz PL, Berjano R, Talavera M, Rodríguez-Zayas L, Arista M (2015) Flower colour polymorphism in Lysimachia arvensis: how is the red morph maintained in mediterranean environments? Perspect Pl Ecol Evol Syst 17:142–150. https://doi.org/10.1016/j.ppees.2015.01.004
Ovaskainen O, Smith AD, Osborne JL, Reynold DR, Carreck NL, Martin AP, Niitepõld K, Hanski I (2008) Tracking butterfly movements with harmonic radar reveals an effect of population age on movement distance. Proc Natl Acad Sci USA 105:19090–19095. https://doi.org/10.1073/pnas.0802066105
Papiorek S, Junker RR, Alves-dos-Santos I, Melo GA, Amaral-Neto LP, Sazima M, Wolowski M, Freitas L, Lunau K (2016) Bees, birds and yellow flowers: pollinator-dependent convergent evolution of UV patterns. Pl Biol 18:46–55. https://doi.org/10.1111/plb.12322
Patiño S, Jeffree C, Grace J (2002) The ecological role of orientation in tropical Convolvulaceous flowers. Oecologia 130:373–379. https://doi.org/10.1007/s00442-001-0824-1
Prasad KN, Divakar S, Shivamurthy GR, Aradhya SM (2005) Isolation of a free radical-scavenging antioxidant from water spinach (Ipomoea aquatica Forssk). J Sci Food Agric 85:1461–1468. https://doi.org/10.1002/jsfa.2125
Raimúndez-Urrutia E, Avendano L, Velázquez D (2008) Reproductive biology of the morning glory Merremia macrocalyx (Ruiz & Pavon) O’donnell (Convolvulaceae). J Torrey Bot Soc 135:299–308. https://doi.org/10.3159/08-RA-027.1
Rausher MD (2008) Evolutionary transitions in floral color. Int J Pl Sci 169:7–21. https://doi.org/10.1086/523358
Rosas-Guerrero V, Aguilar R, Martén-Rodríguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida J, Quesada M (2014) A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecol Lett 17:388–400. https://doi.org/10.1111/ele.12224
Sanderson CE, Orozco BS, Hill PS, Wells H (2006) Honeybee (Apis mellifera ligustica) response to differences in handling time, rewards and flower colours. Ethology 112:937–946. https://doi.org/10.1111/j.1439-0310.2006.01245.x
Schemske D, Bierzychudek P (2007) Spatial differentiation for flower color in the desert annual Linanthus parryae: was wright right? Evolution 61:2528–2543. https://doi.org/10.1111/j.1558-5646.2007.00219.x
Smith JP, Heard TA, Beekman M, Gloag R (2017) Flight range of the australian stingless bee Tetragonula carbonaria (Hymenoptera: Apidae). Austral Entomol 56:50–53. https://doi.org/10.1111/aen.12206
Stanton ML, Snow AA, Handel SN, Bereczky J (1989) The impact of a flower-color polymorphism on mating patterns in experimental populations of wild radish (Raphanus raphanistrum L.). Evolution 43:335–346. https://doi.org/10.1111/j.1558-5646.1989.tb04231.x
Staples G, Traiperm P (2010) Convolvulaceae. In: Flora of Thailand, 1st edn. Royal Forest Department, Bangkok
Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms. I: pollination mechanisms. Annual Rev Ecol Syst 1:307–326. https://doi.org/10.1146/annurev.es.01.110170.001515
Streisfeld MA, Kohn JR (2007) Environment and pollinator-mediated selection on parapatric floral races of Mimulus aurantiacus. J Evol Biol 20:122–132. https://doi.org/10.1111/j.1420-9101.2006.01216.x
Suwanphak K (2013) Thailand butterfly guide, 1st edn. Sarakadee, Nonthaburi
Suwanphak K (2016) Thailand insect guide, 1st edn. Sarakadee, Nonthaburi
Takahashi Y, Koh-Ichi T, Masakado K (2015) Flower color polymorphism maintained by overdominant selection in Sisyrinchium sp. J Pl Res 128:933–939. https://doi.org/10.1007/s10265-015-0750-7
Thai Meteorological Department (2019) Thai Meteorological Department. Available at: https://www.tmd.go.th/en/. Accessed 4 Oct 2019
Vaidya P, McDurmon A, Mattoon E, Keefe M, Carley L, Lee CR, Bingham R, Anderson JT (2018) Ecological causes and consequences of flower color polymorphism in a self-pollinating plant (Boechera stricta). New Phytol 218:380–392. https://doi.org/10.1111/nph.14998
Van Nieuwstadt MGL, Ruana Iraheta CE (1996) Relation between size and foraging range in stingless bees (Apidae, Meliponinae). Apidologie 27:219–228. https://doi.org/10.1051/apido:19960404
Warren J, Mackenzie S (2001) Why are all colour combinations not equally represented as flower-colour polymorphisms? New Phytol 151:237–241. https://doi.org/10.1046/j.1469-8137.2001.00159.x
Wolfe LM (1993) Reproductive consequences of a flower color polymorphism in Hydrophyllum appendiculatum. Amer Midl Naturalist 129:405–408. https://doi.org/10.2307/2426522
Wolfe LM, Sowell DR (2006) Do pollination syndromes partition the pollinator community? A test using four sympatric morning glory species. Int J Pl Sci 167:1169–1175. https://doi.org/10.1086/507651
Acknowledgements
We are thankful to Nong Khai locals for their assistance with field work, and to Wipawee Nilapaka, Natthaphong Chitchak, and Pantamith Ratanakrajang for helpful comments and suggestions during discussions about this project. We also thank Nico Blüthgen and four anonymous reviewers for comments on an earlier draft of the manuscript.
Funding
This study was supported by Mahidol University (Mentorship Grant awarded to ABS and PT; Young Scientist Scholarship awarded to PH).
Author information
Authors and Affiliations
Contributions
This study was conceived and designed by ABS, PH, and PT; data were collected by PH; data were analyzed by ABS and PH; figures and tables were prepared by ABS and PH; the first draft was written by ABS and PH; the manuscript was revised by ABS, PH, and PT; and the final version was approved by ABS, PH, and PT.
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that they have no conflict of interest.
Ethics approval
Permission to work with animals was granted by MUSC-IACUC (Faculty of Science, Mahidol University-Institutional Animal Care and Use Committee) (license number MUSC60-037-387).
Additional information
Handling Editor: Thais N. C. Vasconcelos.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Information on Electronic Supplementary Materials
Below is the link to the electronic supplementary material.
Online Resource 1.
Visitation rates of all animal species visiting Ipomoea aquatica flowers in Nong Khai, Thailand. Visitation rates to both floral color morphs, purple flowers only, and white flowers only are listed, as well as the results from zero-inflated regression models determining whether or not floral color significantly influenced visitation rates
Rights and permissions
About this article
Cite this article
Hassa, P., Traiperm, P. & Stewart, A.B. Pollinator visitation and female reproductive success in two floral color morphs of Ipomoea aquatica (Convolvulaceae). Plant Syst Evol 306, 88 (2020). https://doi.org/10.1007/s00606-020-01716-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-020-01716-1