Differences in pollination syndromes and the frequency of autonomous delayed selfing between co-flowering Hibiscus aponeurus (Sprague and Hutch) and H. flavifolius (Ulbr) from Kenya
DOI:
https://doi.org/10.26786/1920-7603(2018)threeAbstract
Delayed autonomous selfing offers a mechanism for seed production when pollination levels are low or unpredictable. At Mpala Research Centre (MRC) in Kenya, we examined the relationships between floral attraction, insect visitation, and delayed autonomous selfing through backwards stylar curvature in the co-flowering Hibiscus aponeurus and H. flavifolius. Despite producing similar pollen and nectar rewards, visitation rates and the composition of floral visitor guilds varied significantly between these species. Across four years of observations, floral visitation in H. flavifolius was dominated by bees, and in H. aponeurus by a mixture of bees, butterflies and beetles. Visitation rates to H. flavifolius flowers (range 0.17 - 2.1 visits flr-1hr-1) were two times greater than to H. aponeurus flowers (range 0 - 2.7 visits flr-1hr-1), which resulted in significantly higher pollen deposition and removal rates in H. flavifolius than in H. aponeurus. Field crosses demonstrated little pollen limitation in either species. In open-pollinated flowers, H. aponeurus displayed significantly greater stylar curvature and apparent self-pollination than did H. flavifolius. Floral attributes in H. aponeurus, such as a smaller corolla size and a downwards orientation of the stylar column, also suggest that delayed selfing is a more important mechanism of reproductive assurance in this species than in H. flavifolius. Determining whether these differences in insect visitation and stylar curvature are characteristic for these species or are unique to MRC will require comparison with populations located in other parts of the ranges, genetic tests of selfing rates, and chemical analyses of nectar, pollen, and floral volatiles.
References
African Plant Database (version 3.0.4). Conservatoire et Jardin Botaniques de la Ville de Genève and South African National Biodiversity Institute, Pretoria, South Africa. [online] URL:http://www.ville-ge.ch/musinfo/bd/cjb/africa/details.php?id=81504 (accessed March 2017).
Agnew ADQ, Agnew S (1994) Upland Kenya wildflowers: a flora of the ferns and herbaceous flowering plants of upland Kenya, 2nd ed. East Africa Natural History Society, Nairobi, Kenya.
Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecology Letters 9:968–980. DOI: https://doi.org/10.1111/j.1461-0248.2006.00927.x
Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271-281. DOI: https://doi.org/10.1890/06-1017
Alonso C, Vamosi JC, Knight TM, Steets JA, Ashman TL (2010) Is reproduction of endemic plant species particularly pollen limited in biodiversity hotspots? Oikos 119:1192–1200. DOI: https://doi.org/10.1111/j.1600-0706.2009.18026.x
Azuma, H, Toyota M, Asakawa Y (2001) Intraspecific variation of floral scent chemistry in Magnolia kobus DC. (Magnoliaceae). Journal of Plant Research 114:411–422. DOI: https://doi.org/10.1007/PL00014006
Baker HG, Baker I (1982) Chemical constituents of nectar in relation to pollination mechanisms and phylogeny. In: Nitecki M. (ed.) Biochemical aspects of evolutionary biology. University of Chicago Press, Chicago, pp.1311-1371.
Baldock KCR, Memmott J, Ruiz-Guajardo JC, Roze D, Stone GN (2011) Daily temporal structure in African savanna flower visitation networks and consequences for network sampling. Ecology 92:687–698. DOI: https://doi.org/10.1890/10-1110.1
Barkhadle AMI, Ongaro L, Pignatti S (1994) Pastoralism and plant cover in the lower Shabelle region, Southern Somalia. Landscape Ecology 9:79-88. DOI: https://doi.org/10.1007/BF00124375
Brown JH (1984) On the relationship between abundance and distribution of species. The American Naturalist 124:255-279. DOI: https://doi.org/10.1086/284267
Brys R, Jacquemyn J (2011) Variation in the functioning of autonomous self-pollination, pollinator services and floral traits in three Centaurium species. Annals of Botany 107:917-925. DOI: https://doi.org/10.1093/aob/mcr032
Brys R, Jacquemyn J (2012) Effects of human-mediated pollinator impoverishment on floral traits and mating patterns in a short-lived herb: an experimental approach. Functional Ecology 26:189-197. DOI: https://doi.org/10.1111/j.1365-2435.2011.01923.x
Burd M (1994) Bateman's principle and plant reproduction: the role of pollen limitation in fruit and seed set. The Botanical Review 60:83-139. DOI: https://doi.org/10.1007/BF02856594
Buttrose MS, Grant WJR, Lott JNA (1977) Reversible curvature of style branches of Hibiscus trionum L., a pollination mechanism. Australian Journal of Botany 25:567-570. DOI: https://doi.org/10.1071/BT9770567
Byers KJRP, Bradshaw Jr HD, Riffell JA (2014) Three floral volatiles contribute to differential pollinator attraction in monkey flowers (Mimulus). Journal of Experimental Biology 217:614-623. DOI: https://doi.org/10.1242/jeb.092213
Chittka L, Wasser N (1997) Why red flowers are not invisible to bees. Israel Journal of Plant Sciences 45:169-183. DOI: https://doi.org/10.1080/07929978.1997.10676682
Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou PO, Goodwillie C, Johntson MO, Kelly JK, Moeller DA, Porcher E, Ree RH, Vallejo-Marín M, Winn AA (2010) Plant mating systems in a changing world. Trends in Ecology and Evolution 25:35-43. DOI: https://doi.org/10.1016/j.tree.2009.06.013
Elliot SE, Irwin RE (2009) Effects of flowering plant density on pollinator visitation, pollen receipt, and seed production in Delphinium barbeyi (Ranunculaceae). American Journal of Botany 96:912–919. DOI: https://doi.org/10.3732/ajb.0800260
Exell AW (1961) Malvaceae In: Exell AW, Wild H (eds) Flora Zambesiaca: Mozambique, Federation of Rhodesia and Nyasaland, Bechuanal and Protectorate, vol. 1, part 2, p. 420. [online] http://apps.kew.org/efloras/search.do. (Accessed 3 November 2016). Information used with permission of the Trustees of the Royal Botanic Gardens, Kew.
Friis I, Vollensen K (1998) Flora of the Sudan-Uganda border area east of the Nile. Catalogue of vascular plants, ser. I, part 1. The Royal Danish Academy of Sciences and Letters, Munksgaard, Copenhagen.
González-Teuber M, Heil M (2009) Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signaling & Behavior 9:809-813. DOI: https://doi.org/10.4161/psb.4.9.9393
Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution, and Systematics 36:47-79. DOI: https://doi.org/10.1146/annurev.ecolsys.36.091704.175539
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 2:185-209. DOI: https://doi.org/10.1078/1433-8319-00070
Herlihy CR, Eckert CG (2005) Evolution of self-fertilization at geographical range margins? A comparison of demographic, floral, and mating system variables in central vs. peripheral populations of Aquilegia canadensis (Ranunculaceae). American Journal of Botany 92:744-751. DOI: https://doi.org/10.3732/ajb.92.4.744
Jain SK (1976) The evolution of inbreeding in plants. Annual Review of Ecology and Systematics 7:469–495. DOI: https://doi.org/10.1146/annurev.es.07.110176.002345
Jorgensen R, Arathi HS (2013) Floral longevity and autonomous selfing are altered by pollination and water availability in Collinsia heterophylla. Annals of Botany 112:821-828. DOI: https://doi.org/10.1093/aob/mct146
Kalisz S, Vogler DW, Hanley KM (2004) Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430:884-887. DOI: https://doi.org/10.1038/nature02776
Kalisz S, Vogler D, Fails B, Finer M, Shepard E, Herman T, Gonzales R (1999) The mechanism of delayed selfing in Collinsia verna (Scrophulariaceae). America Journal of Botany 86:1239-1247. DOI: https://doi.org/10.2307/2656771
Klips RA, Snow AA (1997) Delayed autonomous self-pollination in Hibiscus laevis (Malvaceae). American Journal of Botany 84:48-53. DOI: https://doi.org/10.2307/2445882
Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman TL (2005) Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution, and Systematics 36:467-497. DOI: https://doi.org/10.1146/annurev.ecolsys.36.102403.115320
Kumar G, Kadam GB, Saha TN, Girish KS, Tiwari AK, Kumar R (2014) Studies on floral biology of Malva sylvestris L. Indian Journal of Horticulture 71:295-297.
Larson BMH, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biological Journal of the Linnean Society 69:503-520. DOI: https://doi.org/10.1111/j.1095-8312.2000.tb01221.x
Lloyd DG, Schoen DJ (1992) Self- and cross-fertilization in plants. I. Functional dimensions. International Journal of Plant Sciences 153:358-369. DOI: https://doi.org/10.1086/297040
Morgan MT, Wilson WG (2005) Self-fertilization and the escape from pollen limitation in variable pollination environments. Evolution 59:1143-1148. DOI: https://doi.org/10.1111/j.0014-3820.2005.tb01050.x
Morgan MT, Wilson WG, Knight TM (2005) Plant population dynamics, pollinator foraging, and the selection of self-fertilization. The American Naturalist 166:169-183. DOI: https://doi.org/10.1086/431317
Pannell JR, Barrett SCH (1998) Baker’s law revisited: reproductive assurance in a metapopulation. Evolution 52:657-668. DOI: https://doi.org/10.1111/j.1558-5646.1998.tb03691.x
Pfeil BE, Brubaker CL, Craven LA, Crisp MD (2002) Phylogeny of Hibiscus and the tribe Hibisceae (Malvaceae) using chloroplast DNA sequences of ndhF and the rpl16 intron. Systematic Botany 27:333-350.
Qu R, Li X, Luo Y, Dong M, Xu H, Chen X, Dafni A (2007) Wind-dragged corolla enhances self-pollination: a new mechanism of delayed self-pollination. Annals of Botany 100:1155-1164. DOI: https://doi.org/10.1093/aob/mcm209
Raine NE, Pierson AS, Stone GN (2007) Plant-pollinator interactions in a Mexican Acacia community. Arthropod-Plant Interactions 1:101-117. DOI: https://doi.org/10.1007/s11829-007-9010-7
Rambuda TN, Johnson SD (2004) Breeding systems of invasive alien plants in South Africa: does Baker’s rule apply? Diversity and Distributions 10:409-416. DOI: https://doi.org/10.1111/j.1366-9516.2004.00100.x
Ramsey ML, Seed L, Vaughton G (2003) Delayed selfing and low levels of inbreeding depression in Hibiscus trionum (Malvaceae). Australian Journal of Botany 51:275-281. DOI: https://doi.org/10.1071/BT02128
Rodríguez-Gironés MA, Santamaría L (2004) Why are so many bird flowers red? Public Library of Science Biology 2:1515-1519. DOI: https://doi.org/10.1371/journal.pbio.0020350
Ruan CJ, Chen SC, Qun L, Texeira Da Silva JA (2011) Adaptive evolution of context-dependent style curvature in some species of the Malvaceae: a molecular phylogenetic approach. Plant Systematics and Evolution 297:57-74. DOI: https://doi.org/10.1007/s00606-011-0499-y
Ruan CJ, Li H, Mopper S (2008a) The impact of pollen tube growth on stigma lobe curvature in Kosteletzkya virginica: the best of both worlds. South African Journal of Botany 74:65-70. DOI: https://doi.org/10.1016/j.sajb.2007.08.012
Ruan CJ, Mopper S, Texeira Da Silva JA, Qin P, Zhang QX, Shan Y (2009) Context-dependent style curvature in Kosteletzkya virginica (Malvaceae) offers reproductive assurance under unpredictable pollinator environments. Plant Systematics and Evolution 277:207-215. DOI: https://doi.org/10.1007/s00606-008-0127-7
Ruan CJ, Qin P, Xi Y (2005) Floral traits and pollination modes in Kosteletzkya virginica (Malvaceae). Belgian Journal of Botany 138:39-46.
Ruan CJ, Mopper S, Texeira Da Silva JA, Qin P (2010) Style curvature and its adaptive significance in the Malvaceae. Plant Systematics and Evolution 288:13-23. DOI: https://doi.org/10.1007/s00606-010-0305-2
Ruan CJ, Zhou L, Zeng F, Han R, Qin Q, Luttis S, Saad L, Mahy G. (2008b) Contribution of delayed autonomous selfing to reproductive success in Kosteletzkya virginica. Belgian Journal of Botany 141:3-13.
Ruiz-Guajardo JC (2008) Community plant-pollinator interactions in a Kenyan savannah. Ph.D. dissertation, University of Edinburgh, Edinburgh, UK.
Sampson BJ, Pounders CT, Werle CT, Mallette TR, Larsen D, Chetelain L, Lee KC (2016) Aggression between floral specialist bees enhances pollination of Hibiscus (section Trionum: Malvaceae). Journal of Pollination Ecology 18:7-12. DOI: https://doi.org/10.26786/1920-7603(2016)11
Scriven LA, Sweet MJ, Port GR (2013) Flower density is more important than habitat type for increasing flower visiting insect diversity. International Journal of Ecology 2013, Article ID 237457, 12 pages. DOI: https://doi.org/10.1155/2013/237457
Seed L, Vaughton G, Ramsey M (2006) Delayed autonomous selfing and inbreeding depression in the Australian annual Hibiscus trionum var. vesicarius (Malvaceae). Australian Journal of Botany 54:27-34. DOI: https://doi.org/10.1071/BT05017
Somme L, Mayer C, Jacquemart AL (2014). Multilevel spatial structure impacts on the pollination services of Comarum palustre (Rosaceae). PLoS One 9:1-10. DOI: https://doi.org/10.1371/journal.pone.0099295
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 USA. 98:3898-3903. DOI: https://doi.org/10.1073/pnas.071053098
Stebbins GL (1957) Self-fertilization and population variability in higher plants. The American Naturalist 91:337-354. DOI: https://doi.org/10.1086/281999
Stone G, Willmer P, Nee S (1996) Daily partitioning of pollinators in an African Acacia community. Proceedings of the Royal Society of London Series B-Biological Sciences 263:1389-1393. DOI: https://doi.org/10.1098/rspb.1996.0203
Stone GN, Willmer P, Rowe JA (1998) Partitioning of pollinators during flowering in an African Acacia community. Ecology 79:2808-2827. DOI: https://doi.org/10.1890/0012-9658(1998)079[2808:POPDFI]2.0.CO;2
Thomann ME, Imbert E, Devaux C, Cheptou PO (2013) Flowering plants under global pollinator decline. Trends in Plant Science 18:353-359. DOI: https://doi.org/10.1016/j.tplants.2013.04.002
Thomson JD (2001) Using pollination deficits to infer pollinator declines: can theory guide us? Conservation Ecology 5:6. [online] URL: http://www.consecol.org/vol5/iss1/art6/. DOI: https://doi.org/10.5751/ES-00270-050106
Vamosi JC, Knight TM, Steets JA, Mazer SJ, Burd M, Ashman TL (2006) Pollination decays in biodiversity hotspots. Proceedings of the National Academy of Sciences USA 103:956-961. DOI: https://doi.org/10.1073/pnas.0507165103
Vamosi JC, Steets JC, Ashman TL (2013) Drivers of pollen limitation: macroecological interactions between breeding system, rarity, and diversity. Plant Ecology & Diversity 6:171-180. DOI: https://doi.org/10.1080/17550874.2013.769130
Vanbergen, AJ (2013) Threats to an ecosystem service: pressures on pollinators. Frontiers in Ecology & the Environment 11: 251–259. DOI: https://doi.org/10.1890/120126
Vaughton G, Ramsey M (2010) Pollinator-mediated selfing erodes the flexibility of the best-of-both-worlds mating stragey in Bulbine vagans. Functional Ecology 24:374-382. DOI: https://doi.org/10.1111/j.1365-2435.2009.01648.x
Waser NM (1986) Flower constancy: definition, cause, and measurement. The American Naturalist 127:593-603. DOI: https://doi.org/10.1086/284507
Watanabe ME (2014) Pollinators at risk: human activities threaten key species. BioScience 64:5-10. DOI: https://doi.org/10.1093/biosci/bit012
Whitehead MR, Peakall R (2009) Integrating floral scent, pollination ecology and population genetics. Functional Ecology 23:863-874. DOI: https://doi.org/10.1111/j.1365-2435.2009.01620.x
Willmer PG, Stone GN (2004) Behavioral, ecological and physiological determinants of the activity patterns of bees. Advances in the Study of Behavior 34:347-466. DOI: https://doi.org/10.1016/S0065-3454(04)34009-X
Wright SI, Kalisz S, Slotte T (2013) Evolutionary consequences of self-fertilization in plants. Proceedings of the Royal Society B 280:20130133. DOI: https://doi.org/10.1098/rspb.2013.0133
Zhang C, Zhou GY, Yang YP, Duan YW (2014) Better than nothing: evolution of autonomous selfing under strong inbreeding depression in an alpine annual from Qinghai-Tibet Plateau. Journal of Systematics and Evolution 52:363-367 DOI: https://doi.org/10.1111/jse.12082
Published
How to Cite
Issue
Section
License
Copyright (c) 2018 Juan Carlos Ruiz Guajardo, Andrew Schnabel, Britnie McCallum, Adriana Otero Arnaiz, Katherine C. R. Baldock, Graham N Stone
This work is licensed under a Creative Commons Attribution 4.0 International License.
