Insects facilitate wind pollination in pollen-limited Crateva adansonii (Capparaceae)
Yash Mangla A and Rajesh Tandon A BA Department of Botany, University of Delhi, Delhi – 110007, India.
B Corresponding author. Email: rjtnd@rediffmail.com
Australian Journal of Botany 59(1) 61-69 https://doi.org/10.1071/BT10174
Submitted: 9 July 2010 Accepted: 22 December 2010 Published: 10 February 2011
Abstract
Low fruit-set in obligately outbreeding plant species is attributed to a variety of reasons that can be ascertained from reproductive studies. In the present work, the causes of poor natural fruit-set in Crateva adansonii DC. were investigated. Floral biology, the role of wind and insects in pollination and the breeding system of the species were studied in two natural populations for three consecutive seasons (2006–08). The flowers exhibited traits conducive to a mixture of wind and insect pollination (ambophily). Although a variety of insects visited the flowers, they were ineffective in pollinating. Nevertheless, active foraging by the honeybees (Apis dorsata, A. mellifera and A. cerana indica) facilitated enhanced pollen dispersal in the air and resulted in indirect pollination by wind. Airborne pollen grains pollinated the plants only up to 10 m. Fruit-set from open pollination was comparable to wind-pollinated flowers. Supplemental pollination treatments established the occurrence of strong self-incompatibility (SI) (index of SI = 0.14). Spontaneous autogamy was prevented by pronounced herkogamy. Low natural fecundity in C. adansonii is due to pollination failure, pollen limitation (pollen limitation index = 0.98) and the sparse distribution of the conspecifics; partial SI may partly ensure reproductive assurance through geitonogamy. In the absence of a pollinator wind appears to act as a secondary mode of pollination.
References
Ågren J (1996) Population size, pollinator limitation, seed set in the self incompatible herb Lythrum salicaria. Ecology 77, 1779–1790.| Population size, pollinator limitation, seed set in the self incompatible herb Lythrum salicaria.Crossref | GoogleScholarGoogle Scholar |
Aizen MA, Feinsinger P (1994) Forest fragmentation, pollination, and plant reproduction in a Chaco dry forest, Argentina. Ecology 75, 330–351.
| Forest fragmentation, pollination, and plant reproduction in a Chaco dry forest, Argentina.Crossref | GoogleScholarGoogle Scholar |
Allison TD (1990) Pollen production and plant density affect pollination and seed production in Taxus canadensis. Ecology 71, 516–552.
| Pollen production and plant density affect pollination and seed production in Taxus canadensis.Crossref | GoogleScholarGoogle Scholar |
Anderson GJ, Bernardello G, Stuessy TF, Crawford DJ (2001) Breeding system and pollination of selected plants endemic to Juan Fernandez Islands. American Journal of Botany 88, 220–233.
| Breeding system and pollination of selected plants endemic to Juan Fernandez Islands.Crossref | GoogleScholarGoogle Scholar | 11222245PubMed |
Antonovics J, Levin DA (1980) The ecological and genetic consequences of density-dependent regulation in plants. Annual Review of Ecology and Systematics 11, 411–452.
| The ecological and genetic consequences of density-dependent regulation in plants.Crossref | GoogleScholarGoogle Scholar |
Bawa KS (1974) Breeding systems of tree species of a lowland tropical community. Evolution 28, 85–92.
| Breeding systems of tree species of a lowland tropical community.Crossref | GoogleScholarGoogle Scholar |
Bawa KS (1990) Plant-pollinator interactions in tropical rain forests. Annual Review of Ecology and Systematics 21, 399–422.
| Plant-pollinator interactions in tropical rain forests.Crossref | GoogleScholarGoogle Scholar |
Bullock SH (1994) Wind pollination of neotropical dioecious trees. Biotropica 26, 172–179.
| Wind pollination of neotropical dioecious trees.Crossref | GoogleScholarGoogle Scholar |
Bullock SH (1995) Plant reproduction in neotropical dry forest. In ‘Seasonally dry tropical forests’. (Eds SH Bullock, HA Mooney, E Medina) pp. 277–302. (Cambridge University Press: Cambridge, UK)
Burd M (1994) Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Botanical Review 60, 83–139.
| Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set.Crossref | GoogleScholarGoogle Scholar |
Cruden RW (1977) Pollen-ovule ratio: a conservative indicator of breeding system in flowering plants. Evolution 31, 32–46.
| Pollen-ovule ratio: a conservative indicator of breeding system in flowering plants.Crossref | GoogleScholarGoogle Scholar |
Culley TM, Weller SG, Sakai AK (2002) The evolution of wind pollination in angiosperms. Trends in Ecology & Evolution 17, 361–369.
| The evolution of wind pollination in angiosperms.Crossref | GoogleScholarGoogle Scholar |
Cunningham SA (2000) Depressed pollination in habitat fragments causes low fruit set. Proceedings of the Royal Society London B: Biological Science 267, 1149–1152.
Dafni A, Calder DM (1987) Pollination by deceit and floral mimesis in Thelymitran antennifera (Orchidaceae). Plant Systematics and Evolution 158, 11–22.
| Pollination by deceit and floral mimesis in Thelymitran antennifera (Orchidaceae).Crossref | GoogleScholarGoogle Scholar |
Dafni A, Dukas R (1986) Insect and wind pollination in Urginea maritima (Liliaceae). Plant Systematics and Evolution 154, 1–10.
| Insect and wind pollination in Urginea maritima (Liliaceae).Crossref | GoogleScholarGoogle Scholar |
de Jong TJ, Waser NM, Klinkhamer PGL (1993) Geitonogamy: the neglected side of selfing. Trends in Ecology & Evolution 8, 321–325.
| Geitonogamy: the neglected side of selfing.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itV2isw%3D%3D&md5=285cee5359dbb53d45d0732bf95060a2CAS |
de la Bandera MC, Traveset A (2006) Breeding system and spatial variation in the pollination biology of the heterocarpic Thymelaea velutina (Thymelaeaceae). Plant Systematics and Evolution 257, 9–23.
| Breeding system and spatial variation in the pollination biology of the heterocarpic Thymelaea velutina (Thymelaeaceae).Crossref | GoogleScholarGoogle Scholar |
Eckert CG, Samis KE, Dart S (2006) Reproductive assurance and the evolution of uniparental reproduction in flowering plants. In ‘Ecology and evolution of flowers’. (Eds LD Harder, SCH Barrett) pp. 183–203. (Oxford University Press: Oxford)
Faegri K, van der Pijl L (1979) ‘The principles of pollination ecology.’ (Pergamon Press: Oxford)
Fenster CB, Armbruster WS, Wilson P, Thomson JD, Dudash MR (2004) Pollination syndromes and floral specialization. Annual Review of Ecology Evolution and Systematics 35, 375–403.
| Pollination syndromes and floral specialization.Crossref | GoogleScholarGoogle Scholar |
Friedman J, Barrett SCH (2009) Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Annals of Botany 103, 1515–1527.
| Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants.Crossref | GoogleScholarGoogle Scholar | 19218583PubMed |
Galen C, Gregory T, Galloway LF (1989) Cost of self-pollination in a self-incompatible plant, Plemonium viscosum. American Journal of Botany 76, 1675–1680.
| Cost of self-pollination in a self-incompatible plant, Plemonium viscosum.Crossref | GoogleScholarGoogle Scholar |
Harder L, Routley M (2006) Pollen and ovule fates and reproductive performance by flowering plants. In ‘Ecology and evolution of flowers’. (Eds LD Harder, SCH Barrett) pp. 61–80. (Oxford University Press: Oxford)
Heslop-Harrison J, Heslop-Harrison Y (1970) Evaluation of pollen viability by enzymatically induced fluorescence; intracellular hydrolysis of fluorescein diacetate. Stain Technology 45, 115–120.
Heslop-Harrison Y, Shivanna KR (1977) The receptive surface of the angiosperm stigma. Annals of Botany 41, 1233–1258.
Hu S, Dilcher DL, Jarzen DM, Taylor DW (2008) Early steps of angiosperm-pollinator coevolution. Proceedings of the National Academy of Sciences of the United States of America 105, 240–245.
| Early steps of angiosperm-pollinator coevolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVajtLc%3D&md5=89649e8f61cf65c5b52b823cc39b2758CAS | 18172206PubMed |
Jacobs M (1964) The genus Crateva (Capparaceae). Blumea 12, 177–207.
Johnson SD, Steiner KE (2000) Generalization versus specialization in plant pollination systems. Trends in Ecology & Evolution 15, 140–143.
| Generalization versus specialization in plant pollination systems.Crossref | GoogleScholarGoogle Scholar |
Kearns CA, Inouye DW (1993) ‘Techniques for pollination biologists.’ (University Press of Colorado: Boulder, CO)
Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualism: the conservation of plant–pollinator interaction. Annual Review of Ecology and Systematics 29, 83–112.
| Endangered mutualism: the conservation of plant–pollinator interaction.Crossref | GoogleScholarGoogle Scholar |
Kress WJ, Beach JH (1994) Flowering plant reproductive systems. In ‘La Selva: ecology and natural history of a neotropical rain forest’. (Eds LA McDade, KS Bawa, A Hespenheide, GS Hartshorn) pp. 161–182. (The University of Chicago Press: Chicago, IL)
Kunin WE (1997) Population size and density effects in pollination: pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber. Journal of Ecology 85, 225–234.
| Population size and density effects in pollination: pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber.Crossref | GoogleScholarGoogle Scholar |
Larson BMH, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biological Journal of Linnaean Society 69, 503–520.
| A comparative analysis of pollen limitation in flowering plants.Crossref | GoogleScholarGoogle Scholar |
Larson KC, Fowler SP, Walker JC (2002) Lack of pollinators limits fruit set in exotic Lonicera japonica. American Midland Naturalist 148, 54–60.
| Lack of pollinators limits fruit set in exotic Lonicera japonica.Crossref | GoogleScholarGoogle Scholar |
Lázaro A, Traveset A (2005) Spatio-temporal variation in the pollination mode of Buxus balearica (Buxaceae), an ambophilous and selfing species: mainland-island comparison. Ecography 28, 640–652.
| Spatio-temporal variation in the pollination mode of Buxus balearica (Buxaceae), an ambophilous and selfing species: mainland-island comparison.Crossref | GoogleScholarGoogle Scholar |
Leereveld H, Meeuse ADJ, Stelleman P (1991) Some cases of visiting of anemophiles by syrphid flies in Madagascar. Israel Journal of Botany 40, 219–223.
Lemen C (1980) Allocation of reproductive effort to the male and female strategies in wind pollinated plants. Oecologia 45, 156–159.
| Allocation of reproductive effort to the male and female strategies in wind pollinated plants.Crossref | GoogleScholarGoogle Scholar |
Linskens HF, Esser K (1957) Über eine specifische Anfärbung der Pollenschläuche im Griffel und die Zahl der Kallosepfropfen nach selbstung und fremdung. Naturweiss 44, 16
| Über eine specifische Anfärbung der Pollenschläuche im Griffel und die Zahl der Kallosepfropfen nach selbstung und fremdung.Crossref | GoogleScholarGoogle Scholar |
Mattson O, Knox RB, Heslop-Harrison J, Heslop-Harrison Y (1974) Protein pellicle as a probable recognition site in incompatibility reactions. Nature 213, 703–704.
Mulcahy DL, Mulcahy GB (1987) The effects of pollen competition. American Scientist 75, 44–50.
Nelson G (1994) ‘The trees of Florida.’ (Pineapple Press Inc.: Sarasota, FL)
Peeters L, Totland O (1999) Wind to insect pollination ratios and floral traits in five alpine Salix species. Canadian Journal of Botany 77, 556–563.
| Wind to insect pollination ratios and floral traits in five alpine Salix species.Crossref | GoogleScholarGoogle Scholar |
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.
| Wind dragged corolla enhances self-pollination: a new mechanism of delayed self-pollination.Crossref | GoogleScholarGoogle Scholar | 17881336PubMed |
Richards AJ (1986) ‘Plant breeding system.’ (George Allen and Unwin: London, UK)
Sacchi CF, Price PW (1988) Pollination of Arroyo willow, Salix lasiolepis: role of insects and wind. American Journal of Botany 75, 1387–1393.
| Pollination of Arroyo willow, Salix lasiolepis: role of insects and wind.Crossref | GoogleScholarGoogle Scholar |
Sarma K, Tandon R, Shivanna KR, Mohan Ram HY (2007) Snail-pollination in Volvulopsis nummularium. Current Science 93, 826–831.
Scandalios JG (1969) Genetic control of multiple molecular forms of enzymes in plants: a review. Biochemical Genetics 3, 37–79.
| Genetic control of multiple molecular forms of enzymes in plants: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXksVKlt70%3D&md5=4409aad126ef9f6f3bbf9e646100dfb6CAS |
Sokal RR, Rohlf FJ (1995) ‘Biometery: the principles and practice of statistics in biological research.’ 3rd edn. (WH Freeman and Company: New York)
Stelleman P (1984) Reflections on the transition from wind pollination to ambophily. Acta Botanica Neerlandica 33, 497–508.
Tamura S, Kudo G (2000) Wind pollination and insect pollination of two temperate willow species, Salix miyabeana and Salix sachalinensis. Plant Ecology 147, 185–192.
| Wind pollination and insect pollination of two temperate willow species, Salix miyabeana and Salix sachalinensis.Crossref | GoogleScholarGoogle Scholar |
Tandon R, Manohara TN, Nijalingappa BHM, Shivanna KR (2001a) Pollination and pollen-pistil interaction in Oil Palm, Elaeis guineensis. Annals of Botany 87, 831–838.
| Pollination and pollen-pistil interaction in Oil Palm, Elaeis guineensis.Crossref | GoogleScholarGoogle Scholar |
Tandon R, Shivanna KR, Mohan Ram HY (2001b) Pollination biology and breeding system of Acacia senegal. Botanical Journal of the Linnean Society 135, 251–262.
| Pollination biology and breeding system of Acacia senegal.Crossref | GoogleScholarGoogle Scholar |
Tandon R, Shivanna KR, Mohan Ram HY (2003) Reproductive biology of Butea monosperma (Fabaceae). Annals of Botany 92, 715–723.
| Reproductive biology of Butea monosperma (Fabaceae).Crossref | GoogleScholarGoogle Scholar | 14500327PubMed |
Waser NM, Chittka L, Price MV (1996) Generalization in pollination systems, and why it matters. Ecology 77, 1043–1060.
| Generalization in pollination systems, and why it matters.Crossref | GoogleScholarGoogle Scholar |
Wilcock C, Neiland R (2002) Pollination failure in plants: why it happens and when it matters. Trends in Plant Science 7, 270–277.
| Pollination failure in plants: why it happens and when it matters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFyns7g%3D&md5=568c402f4cfcd49b91d5b9a5bc9e344dCAS | 12049924PubMed |
Yadav RK, Yadav AS (2008) Phenology of selected woody species in a tropical dry deciduous forest in Rajasthan, India. Tropical Ecology 49, 25–34.
Zapata TR, Arroyo MTK (1978) Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela. Biotropica 10, 221–230.
| Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela.Crossref | GoogleScholarGoogle Scholar |