Pollen limitation failing reproductive success in selected animal pollinated trees of tropical moist deciduous forest of north-eastern hill region, India
Keywords:
Pollination, Pollen limitation, Pollen quantity, Bird pollination, Pollination successAbstract
The aim of this study was to estimate reproductive effort and success in tropical trees and to examine the effect of pollen limitation of reproductive success. Pollen limitation was assessed through pollen supplementation experiment in response to open pollination treament. The taxa selected were Bombax ceiba, Erythrina stricta (ornithophilous trees), Lagerstroemia speciosa, Mesua ferrea and Schima wallichii (entomophilous trees). Index of pollen limitation was maximum in Bombax ceiba and Erythrina stricta (both self - incompatible species). The remaining three species were partially self-incompatible with favouring selfing by Lagerstroemia speciosa and Mesua ferrea and supporting outcrossing by Schima wallichii. Therefore, the high index of pollen limitation in Bombax ceiba and Erythrina stricta might be due to the effect of either being lack of quality pollen or lack of bird pollinators. All five species produce a large amount of pollen at individual tree level in the order of 108 (Erythrina stricta) to 1010 (Mesua ferrea). Fruit and seed set following pollen supplementation were higher than the open pollination (as control) in all the study species. Pollen limitation was the result of limited pollen quantity and quality. Pollen limitation in this study is likely associated with the effectiveness of pollinator and their frequency, as all the studied species had produced ample pollen at tree crown level which ultimately leading to pollinator resource limitation in tropical trees.
Downloads
References
Ahlinder, J., Giles, B. E., & García-Gil, M. R. (2021). Life stage-specific inbreeding depression in long-lived Pinaceae species depends on population connectivity. Scientific Reports, 11(1), 1-15.
Aizen, M. A., & Harder, L. D. (2007). Expanding the limits of the pollen‐limitation concept: effects of pollen quantity and quality. Ecology, 88(2), 271-281.
Allison, T. D. (1990). Pollen production and plant density affect pollination and seed production in Taxus canadensis. Ecology, 71(2), 516-522.
Ashman, T. L., Knight, T. M., Steets, J. A., Amarasekare, P., Burd, M., Campbell, D. R., Dudash, M.R., Johnston, M.O., Mazer, S.J., Mitchell, R.J., Morgan, M.T., & Wilson, W. G. (2004). Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology, 85(9), 2408-2421.
Bartoš, M., Janeček, Š., Janečková, P., Chmelová, E., Tropek, R., Götzenberger, L., Klomberg, Y., & Jersáková, J. (2020). Are reproductive traits related to pollen limitation in plants? A case study from a central European meadow. Plants, 9(5), 640.
Baskin, J. M., & Baskin, C. C. (2018). Pollen limitation and its effect on seed germination. Seed Science Research, 28(4), 253-260.
Bawa, K. S. (1990). Plant-pollinator interactions in tropical rain forests. Annual Review of Ecology and Systematics, 21, 399-422.
Bierzychudek, P. (1981). Pollinator limitation of plant reproductive effort. The American Naturalist, 117(5), 838-840.
Bona, A., Kłosowski, S., Jadwiszczak, K. A., & Petrova, G. (2022). Flowering and quality of seeds and pollen in endangered populations of Betula humilis. Trees, 36(1), 313-324.
Burd, M. (1994). Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. The Botanical Review, 60(1), 83-139.
Campbell, D. R., & Halama, K. J. (1993). Resource and pollen limitations to lifetime seed production in a natural plant population. Ecology, 74(4), 1043-1051.
Charalampopoulos, A., Damialis, A., Tsiripidis, I., Mavrommatis, T., Halley, J. M., & Vokou, D. (2013). Pollen production and circulation patterns along an elevation gradient in Mt Olympos (Greece) National Park. Aerobiologia, 29(4), 455-472.
Charlesworth, D., & Charlesworth, B. (1987). Inbreeding depression and its evolutionary consequences. Annual Review of Ecology, Evolution and Systematics, 18, 237-268.
Chen, M., & Zhao, X. Y. (2017). Effect of pollen and resource limitation on reproduction of Zygophyllum xanthoxylum in fragmented habitats. Ecology and Evolution, 7(21), 9076-9084.
Chen, M., & Zuo, X. A. (2018). Pollen limitation and resource limitation affect the reproductive success of Medicago sativa L. BMC ecology, 18(1), 1-10.
Chen, M., & Zuo, X. A. (2019). Effect of pollen limitation and pollinator visitation on pollination success of Haloxylon ammodendron (CA Mey.) bunge in fragmented habitats. Frontiers in plant science, 10, 327.
Colling, G., Reckinger, C., & Matthies, D. (2004). Effects of pollen quantity and quality on reproduction and offspring vigor in the rare plant Scorzonera humilis (Asteraceae). American Journal of Botany, 91(11), 1774-1782.
Cosacov, A., Nattero, J., & Cocucci, A. A. (2008). Variation of pollinator assemblages and pollen limitation in a locally specialized system: the oil-producing Nierembergia linariifolia (Solanaceae). Annals of Botany, 102(5), 723-734.
Cristóbal-Pérez, E. J., Fuchs, E. J., Olivares-Pinto, U., & Quesada, M. (2020). Janzen-Connell effects shape gene flow patterns and realized fitness in the tropical dioecious tree Spondias purpurea (Anacardiaceae). Scientific Reports, 10(1), 1-12.
Csépe, Z., Leelőssy, Á., Mányoki, G., Kajtor-Apatini, D., Udvardy, O., Péter, B., Páldy, A., Gelybó, G., Szigeti, T., Pándics, T., Kofol-Seliger, A., Simčič, A., Leru, P.M., Eftimie, A.M., Šikoparija, B., Radišić, P., Stjepanović, B., Hrga, I., Večenaj, A., Vucić, A., Peroš-Pucar, D., Škorić, T., Ščevková, J., Bastl, M., Berger, U., & Magyar, D. 2020: The application of a neural network-based ragweed pollen forecast by the Ragweed Pollen Alarm System in the Pannonian biogeographical region. Aerobiologia, 36(2), 131–140.
Damialis, A., Fotiou, C., Halley, J. M., & Vokou, D. (2011). Effects of environmental factors on pollen production in anemophilous woody species. Trees, 25(2), 253-264.
Dawson, D.G., & Bull, P.C. (1975). Counting birds in New Zealand forests. Notornis, 22(2), 101-109.
Devaux, C., Porcher, E., & Lande, R. (2019). Mating systems and avoidance of inbreeding depression as evolutionary drivers of pollen limitation in animal-pollinated self-compatible plants. Annals of botany, 123(2), 327-336.
Devy, M. S., & Davidar, P. (2003). Pollination systems of trees in Kakachi, a mid‐elevation wet evergreen forest in Western Ghats, India. American Journal of Botany, 90(4), 650-657.
Dufaÿ, M., Vaudey, V., De Cauwer, I., Touzet, P., Cuguen, J., & Arnaud, J. F. (2008). Variation in pollen production and pollen viability in natural populations of gynodioecious Beta vulgaris ssp. maritima: evidence for a cost of restoration of male function?. Journal of Evolutionary Biology, 21(1), 202-212.
Duminil, J., Fineschi, S., Hampe, A., Jordano, P., Salvini, D., Vendramin, G. G., & Petit, R. J. (2007). Can population genetic structure be predicted from life-history traits?. The American Naturalist, 169(5), 662-672.
Duminil, J., Hardy, O. J., & Petit, R. J. (2009). Plant traits correlated with generation time directly affect inbreeding depression and mating system and indirectly genetic structure. BMC Evolutionary Biology, 9(1), 1-14.
Etcheverry, A. V., & Alemán, C. E. T. (2005). Reproductive Biology of Erythrina falcata (Fabaceae: Papilionoideae) 1. Biotropica, 37(1), 54-63.
Etcheverry, A. V., Alemán, M. M., & Fleming, T. F. (2008). Flower morphology, pollination biology and mating system of the complex flower of Vigna caracalla (Fabaceae: Papilionoideae). Annals of Botany, 102(3), 305-316.
Faegri, K., Kaland, P. E., & Krzywinski, K. (1989). Textbook of pollen analysis (No. Ed. 4). John Wiley & Sons Ltd..
Ferriol, M., Pichot, C., & Lefèvre, F. (2011). Variation of selfing rate and inbreeding depression among individuals and across generations within an admixed Cedrus population. Heredity, 106(1), 146-157.
Filon, F. L., Bosco, A., Barbina, P., Sauli, M. L., & Longo, L. R. (2000). Betulaceae and Corylaceae in Trieste (NE-Italy): Aerobiological and clinical data. Aerobiologia, 16(1), 87-91.
Fleming, T. H., & Muchhala, N. (2008). Nectar‐feeding bird and bat niches in two worlds: pantropical comparisons of vertebrate pollination systems. Journal of Biogeography, 35(5), 764-780.
Gioulekas, D., Papakosta, D., Damialis, A., Spieksma, F., Giouleka, P., & Patakas, D. (2004). Allergenic pollen records (15 years) and sensitization in patients with respiratory allergy in Thessaloniki, Greece. Allergy, 59(2), 174-184.
Glémin, S., Bazin, E., & Charlesworth, D. (2006). Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proceedings of the Royal Society B: Biological Sciences, 273(1604), 3011-3019.
Gómez, J. M., Abdelaziz, M., Lorite, J., Jesús Muñoz‐Pajares, A., & Perfectti, F. (2010). Changes in pollinator fauna cause spatial variation in pollen limitation. Journal of Ecology, 98(5), 1243-1252.
González-Varo, J. P., Arroyo, J., & Aparicio, A. (2009). Effects of fragmentation on pollinator assemblage, pollen limitation and seed production of Mediterranean myrtle (Myrtus communis). Biological Conservation, 142(5), 1058-1065.
Hilje, B., Calvo-Alvarado, J., Jiménez-Rodríguez, C., & Sánchez-Azofeifa, A. (2015). Tree species composition, breeding systems, and pollination and dispersal syndromes in three forest successional stages in a tropical dry forest in Mesoamerica. Tropical Conservation Science, 8(1), 76-94.
Hirayama, K., Ishida, K., Tomaru, N. (2005). Effects of pollen shortage and self-pollination on seed production of an endangered tree, Magnolia stellata. Annals of Botany, 95, 1009–1015.
Holsinger, K. E. (2000). Reproductive systems and evolution in vascular plants. Proceedings of the National Academy of Sciences, 97(13), 7037-7042.
Hufford, K. M., & Hamrick, J. L. (2003). Viability selection at three early life stages of the tropical tree, Platypodium elegans (Fabaceae, Papilionoideae). Evolution, 57(3), 518-526.
Iwaizumi, M. G., & Takahashi, M. (2012). Effects of pollen supply and quality on seed formation and maturation in Pinus densiflora. Journal of Plant Research, 125(4), 517-525.
Jadwiszczak, K. A., Kłosowski, S., Zalewska, I., Banaszek, A., & Chrzanowska, A. (2017). Genetic diversity and sexual reproduction in relict populations of Betula nana. Silva Fennica, 51(2), 5643.
Kearns, C.A., Inouye, D.W., & Waser, N.M. (1998). Endangered mutualisms: the conservation of plant–pollinator interactions. Annual Review of Ecology, Evolution and Systematics, 29, 83–112.
Khanduri, V. P., & Kumar, K. S. (2017b). Pollen production and release in Mesua ferrea Linn.(Guttiferae): a spatio-temporal pattern. Aerobiologia, 33(1), 13-21.
Khanduri, V. P., Kumar, K. S., Sharma, C. M., Riyal, M. K., & Kar, K. (2019). Pollen limitation and seed set associated with year-to-year variation in flowering of Gmelina arborea in a natural tropical forest. Grana, 58(2), 133-143.
Khanduri, V. P., Kumar, K. S., Sharma, C. M., Riyal, M. K., Kar, K., Singh, B., & Sukumaran, A. (2021). Passerine birds supporting cross pollination in Erythrina stricta Roxb. Dendrobiology, 85, 117-126.
Khanduri, V. P., Sharma C. M., Riyal, M. K., & Sukumaran, A. (2022). Racial hybridization and inbreeding depression in Cedrus deodara (Roxb.) G. Don. Kastamonu University Journal of Forestry Faculty, 22(1), 47-55.
Khanduri, V. P., Sharma, C. M., Kumar, K. S., & Ghildiyal, S. K. (2013). Annual variation in flowering phenology, pollination, mating system, and pollen yield in two natural populations of Schima wallichii (DC.) Korth. The Scientific World Journal, 2013, 350157.
Khanduri, V.P. (2014). Annual variation in floral phenology and pollen production in Lagerstroemia speciosa: an entomophilous tropical tree. Songlanakarin Journal of Science and Technology, 36(4), 389-396.
Khanduri, V.P. (2016). Mating system and seedling growth of five tropical tree species. Scientia Forestalis, 44(110), 509–517.
Khanduri, V.P., & Kumar, K.S. (2017a). Reproductive effort and success in Bombax ceiba L. in a tropical forest of Mizoram, Indo-Burma region of North-East India. Brazilian Journal of Botany, 40(1),157–166
Khanduri, V.P., & Sukumaran, A. (2019). Pollen dispersion in Myrica esculenta (Myricaceae): a dioecious anemophilous tree species of Himalaya. Aerobiologia, 35(4), 583–591.
Khanduri, V.P., Kumar, K.S., & Sharma, C.M. (2015). Role of pollen production in mating success in some tropical tree species. Brazilian Journal of Botany, 38(1), 107–112.
Klein, A. M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the royal society B: biological sciences, 274(1608), 303-313.
Knight, T. M., Steets, J. A., & Ashman, T. L. (2006). A quantitative synthesis of pollen supplementation experiments highlights the contribution of resource reallocation to estimates of pollen limitation. American Journal of Botany, 93(2), 271-277.
Knight, T.M., Steets, J.A., Vamosi, J.C., Mazer, S.J., Burd, M., Campbell, D.R., Dudash, M.R., Johnston, M.O., Mitchell, R.J., & Ashman, T.L. (2005). Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution and Systematics, 36, 467–497.
Lande, R., & Schemske, D.W. (1985). The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution, 39(1), 24–40.
Larson, B. M., & Barrett, S. C. (2000). A comparative analysis of pollen limitation in flowering plants. Biological journal of the Linnean Society, 69(4), 503-520.
Lázaro, A., & Traveset, A. (2006). Reproductive success of the endangered shrub Buxus balearica Lam. (Buxaceae): pollen limitation, and inbreeding and outbreeding depression. Plant Systematics and Evolution, 261(1), 117-128.
Lever, J. J., van Nes, E. H., Scheffer, M., & Bascompte, J. (2014). The sudden collapse of pollinator communities. Ecology letters, 17(3), 350-359.
Liu, M., Compton, S. G., Peng, F. E., Zhang, J., & Chen, X. Y. (2015). Movements of genes between populations: are pollinators more effective at transferring their own or plant genetic markers?. Proceedings of the Royal Society B: Biological Sciences, 282(1808), 20150290.
McKone, M. J. (1990). Characteristics of pollen production in a population of New Zealand snow‐tussock grass (Chionochloa pallens Zotov). New Phytologist, 116(3), 555-562.
Moles, A. T., & Ollerton, J. (2016). Is the notion that species interactions are stronger and more specialized in the tropics a zombie idea?. Biotropica, 48(2), 141-145.
Moore, P. D., Webb, J. A., & Collinson, M. E. (1991). Pollen Analysis, 2nd edn Blackwell.
Mu, J., Yang, Y., Luo, Y., Su, R., & Niklas, K. J. (2017). Pollinator preference and pollen viability mediated by flower color synergistically determine seed set in an Alpine annual herb. Ecology and Evolution, 7(9), 2947-2955.
Nakanishi, A., Yoshimaru, H., Tomaru, N., Miura, M., Manabe, T., & Yamamoto, S. I. (2015). Inbreeding depression at the sapling stage and its genetic consequences in a population of the outcrossing dominant tree species, Castanopsis sieboldii. Tree Genetics & Genomes, 11(3), 1-10.
Obigba, S. O. (2021). Understanding Past and Present Vegetation Dynamics using the Palynological Approach: An Introductory Discourse. In Vegetation Index and Dynamics. Eds. Carmina, E. C., Ortiz, A. C. Canas, R. Q. & Musarella, C. M., PP 1-21,IntechOpen.
Oldroyd, H. (1958). Collecting, Preserving and Studying Insects. Hutchinson & Co. Publishers Ltd.
Ollerton, J. (2017). Pollinator diversity: distribution, ecological function, and conservation. Annual Review of Ecology, Evolution and Systematics, 48, 353–76.
Ollerton, J., Winfree, R., & Tarrant, S. (2011). How many flowering plants are pollinated by animals?. Oikos, 120(3), 321-326.
Pauw, A., & Stanway, R. (2015). Unrivalled specialization in a pollination network from South Africa reveals that specialization increases with latitude only in the Southern Hemisphere. Journal of Biogeography, 42(4), 652-661.
Portillo Lemus, L. O., Harang, M., Bozec, M., Haury, J., Stoeckel, S., & Barloy, D. (2022). Late-acting self-incompatible system, preferential allogamy and delayed selfing in the heteromorphic invasive populations of Ludwigia grandiflora subsp. hexapetala. Peer Community Journal, 2.
Ramos, S. L. F., Dequigiovanni, G., Sebbenn, A. M., Lopes, M. T. G., Kageyama, P. Y., de Macêdo, J. L. V., Matias, K., & Veasey, E. A. (2016). Spatial genetic structure, genetic diversity and pollen dispersal in a harvested population of Astrocaryum aculeatum in the Brazilian Amazon. BMC Genetics, 17(1), 1-10.
Rao, V. R., & Hodgkin, T. (2002). Genetic diversity and conservation and utilization of plant genetic resources. Plant Cell, Tissue and Organ Culture, 68(1), 1-19.
Rodger, J. G., & Ellis, A. G. (2016). Distinct effects of pollinator dependence and self-incompatibility on pollen limitation in South African biodiversity hotspots. Biology Letters, 12(6), 20160253.
Rodger, J. G., & Johnson, S. D. (2013). Self-pollination and inbreeding depression in Acacia dealbata: Can selfing promote invasion in trees?. South African Journal of Botany, 88, 252-259.
Rodríguez-Rodríguez, M. C., Jordano, P., & Valido, A. (2013). Quantity and quality components of effectiveness in insular pollinator assemblages. Oecologia, 173(1), 179-190.
Rogers, C. A. (1993). Application of aeropalynological principles in palaeoecology. Review of Palaeobotany and Palynology, 79(1-2), 133-140.
Schoen, D. J., & Lloyd, D. G. (1992). Self-and cross-fertilization in plants. III. Methods for studying modes and functional aspects of self-fertilization. International Journal of Plant Sciences, 153(3, Part 1), 381-393.
Sousa-Silva, R., Smargiassi, A., Kneeshaw, D., Dupras, J., Zinszer, K., & Paquette, A. (2021). Strong variations in urban allergenicity riskscapes due to poor knowledge of tree pollen allergenic potential. Scientific Reports, 11(1), 1-13.
Sukumaran, A., Khanduri, V. P., & Sharma, C. M. (2020). Pollinator-mediated self-pollination and reproductive assurance in an isolated tree of Magnolia grandiflora L. Ecological Processes, 9(1), 1-9.
Tamura, S., & Kudo, G. (2000). Wind pollination and insect pollination of two temperate willow species, Salix miyabeana and Salix sachalinensis. Plant Ecology, 147(2), 185-192.
Van der Niet, T., Peakall, R., & Johnson, S. D. (2014). Pollinator-driven ecological speciation in plants: new evidence and future perspectives. Annals of Botany, 113(2), 199-212.
Van Etten, M. L., Tate, J. A., Anderson, S. H., Kelly, D., Ladley, J. J., Merrett, M. F., Peterson, P.G., & Robertson, A. W. (2015). The compounding effects of high pollen limitation, selfing rates and inbreeding depression leave a New Zealand tree with few viable offspring. Annals of Botany, 116(5), 833-843.
Voukantsis, D., Niska, H., Karatzas, K., Riga, M., Damialis, A., & Vokou, D. (2010). Forecasting daily pollen concentrations using data-driven modeling methods in Thessaloniki, Greece. Atmospheric Environment, 44(39), 5101-5111.
Wesselingh, R. A. (2007). Pollen limitation meets resource allocation: towards a comprehensive methodology. New Phytologist, 174(1), 26-37.
Westgate, M. E., Lizaso, J., & Batchelor, W. (2003). Quantitative relationships between pollen shed density and grain yield in maize. Crop Science, 43(3), 934-942.
Wilcock, C., & Neiland, R. (2002). Pollination failure in plants: why it happens and when it matters. Trends in Plant Science, 7(6), 270-277.
Wolowski, M., Ashman, T. L., & Freitas, L. (2013). Community-wide assessment of pollen limitation in hummingbird-pollinated plants of a tropical montane rain forest. Annals of botany, 112(5), 903-910.
Wright, S. I., Ness, R. W., Foxe, J. P., & Barrett, S. C. (2008). Genomic consequences of outcrossing and selfing in plants. International Journal of Plant Sciences, 169(1), 105-118.
Yang, C. F., Sun, S. G., & Guo, Y. H. (2005). Resource limitation and pollen source (self and outcross) affecting seed production in two louseworts, Pedicularis siphonantha and P. longiflora (Orobanchaceae). Botanical Journal of the Linnean Society, 147(1), 83-89.
Zheljazkov, V. D., Semerdjieva, I. B., Stevens, J. F., Wu, W., Cantrell, C. L., Yankova-Tsvetkova, E., & Astatkie, T. (2021). Phytochemical investigation and reproductive capacity of the bulgarian endemic plant ppecies Marrubium friwaldskyanum Boiss. (Lamiaceae). Plants, 11(1), 114.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 ZRC-SAZU
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Authors guarantee that the work is their own original creation and does not infringe any statutory or common-law copyright or any proprietary right of any third party. In case of claims by third parties, authors commit their self to defend the interests of the publisher, and shall cover any potential costs.
More in: Submission chapter
