Pollinator-Mediated Self-Pollination and Reproductive Assurance in an Isolated Tree of Magnolia Grandiflora L
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Sukumaran et al. Ecological Processes (2020) 9:45 https://doi.org/10.1186/s13717-020-00254-5 RESEARCH Open Access Pollinator-mediated self-pollination and reproductive assurance in an isolated tree of Magnolia grandiflora L. Arun Sukumaran, Vinod Prasad Khanduri* and Chandra Mohan Sharma Abstract Background: The ability to produce seeds when pollinators or potential mates are scarce is one of the principal advantages of self-pollination in flowering plants. However, the role of pollinators mediating self-pollination to ensure seed set when pollen or potential mates are limited has received less attention. This study examined the reproductive consequences and involvement of pollinators in assuring seed set in an isolated tree of Magnolia grandiflora, a predominantly outcrossing species. Methods: We tested various aspects of reproduction such as flower density, floral rewards, stigma receptivity, pollinator abundance and behaviour, fruit set and seed set, in two successive reproductive years (2015–2016). Results: Flowers of M. grandiflora possess a suite of traits facilitating pollinator-mediated self-pollination (PMS), although the chances of autonomous self-pollination are reduced due to herkogamy, spatial separation of anther and stigma. The mean pollen production/flower was 5,152,289 ± 285,094 with a pollen-to-ovule ratio of 39430 ± 164. We found a significant positive correlation between number of visits and seed production for bees (r = 0.5099, p = 0.0007) and beetles (r = 0.7159, p = 0.00001), indicating these are effective at PMS. There was a significant negative correlation for thrips (r = – 0.3206, p = 0.044) and no correlation for flies or spiders. The percent fruit set was 100% and the seed set per ovule ranged between 19 and 20%. Conclusions: PMS will guarantee reproductive assurance and mitigate the effect of reduced mates or pollen limitation which is expected to increase the fecundity and establishment of individual trees in geographically isolated locations. Keywords: Pollinator-mediated self-pollination, Magnolia grandiflora, Autonomous self-pollination, Pollinator behaviour, Reproductive assurance Background species is found are supposed to determine whether it is Since the time of Darwin (1876), researchers have been predominantly self-fertilized or predominantly out- interested in why there are plants that are primarily self- crossed. A high proportion of self-compatible species (or fertilizing even though the progeny produced by self- populations) are found in isolated locations (e.g. oceanic fertilization (whether of normally outcrossing or islands, isolated ponds; Baker 1955; Longhurst 1955). normally selfing plants) are often less vigorous than pro- Self-pollinating morphs would be favoured by natural se- geny produced by cross-fertilization. Stebbins (1950) lection when population size or potential mates are stated that the ecological conditions in which a given limited. Hermaphrodite and monoecious species have the poten- tial for self-pollination leading to self-fertilization unless * Correspondence: [email protected] there is a mechanism to avoid it. This self-pollination con- College of Forestry, VCSG Uttarakhand University of Horticulture and Forestry, Ranichauri, Tehri Garhwal, Uttarakhand 249199, India sists of pollen transfer within one flower (autogamy) as well as © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Sukumaran et al. Ecological Processes (2020) 9:45 Page 2 of 9 pollen transfer between different flowers on the same tree However, controlled cross-pollination resulted to com- (geitonogamy). Selfing plants benefit from two distinct advan- paratively high seed set, which varied between 31.77 and tages over their outcrossing competitors (Charlesworth 2006; 43.3% (Chen et al. 2016; Allain et al. 1999;Hirayamaetal. Barrett 2002). First, because selfers are 100% related to their 2005). Here, our specific objectives were to explore (1) progeny and can also act as outcross pollen donors for seed floral characteristics and pollinator rewards in M. grandi- produced by other individuals, they have an inherent trans- flora, (2) how isolation (absence of potential mates) affects mission advantage over outcrossers (Fisher 1941). A second pollinator availability and reproductive success and (3) the major advantage conferred by selfing, first discussed by Dar- effect of pollinator-mediated self-pollination (PMS) on re- win (1876), is the ability to reproduce when pollinators or po- productive assurance. Our approach will provide a de- tential mates are limited (reproductive assurance). One tailed examination of the reproductive aspects associated important aspect of reproductive assurance is the ability of with pollinator-mediated self-pollination (PMS) or facili- selfing lineages to colonize new habitats from a very small tated self-pollination in an isolated tree. founding population. In general, selfing should provide repro- ductive benefits whenever the pollination environment (avail- Methods ability of mates and/or pollinators) is poor (Lloyd 1979). Study site Pollinators can mediate self-pollination by foraging The investigation was carried out in an isolated tree of within flowers (facilitated selfing) or between flowers on M. grandiflora, which was located at the College of For- the same plant (geitonogamy). Reproductive assurance estry, V.C.S.G. Uttarakhand University Horticulture and may result from both autonomous selfing and, to a lesser Forestry, Ranichauri, Tehri Garhwal (Latitude 30° 18″ extent, facilitated selfing (Lloyd and Schoen 1992;Vaugh- N, Longitude 78° 24″ E, altitude 1800–2000 m amsl), ton and Ramsey 2010). However, when pollinators are Uttarakhand, India. The isolated tree was planted in the missing, only autonomous self-pollination may provide re- year 2001 and the seedling was brought from Dehradun; productive assurance (Lloyd 1992). Facilitated selfing, on a survey has been carried at a distance of more than 15 the other hand, only provides reproductive assurance km in the surrounding zone of the local tree and en- when mates are scarce, but generally not when pollinators sured that no other trees are growing or planted. The are limiting. Moreover, because facilitated and geitonog- study was conducted in the month of June to October in amous selfing occurs at the same time as outcrossing, dis- 2 successive years 2015 and 2016. During the study counting costs can be incurred, particularly following period, the mean monthly rainfall was 10.47 mm; the geitonogamy. Accordingly, these selfing modes are average relative humidity was in between 76 and 91.6%. regarded as non-adaptive consequences of attracting ani- Maximum monthly means of daily temperature ranged mals that cross pollinate flowers (Lloyd 1992; de Jong from 22.38 (July 2015) to 23.42 °C (August 2016) and et al. 1993; Harder and Barrett 1995;Eckert2000). the corresponding minimum was from 17.75 (July 2016) Magnolia grandiflora (Magnoliaceae) occurs within to 17.26 °C (August 2016). The July and August are the the relatively ancient order Magnoliales. Until the end of peak rainy season in the study area. the last century, biologists considered Magnoliales to be among the oldest flowering plants with the estimated date Floral phenology of emergence of the order around 95.5 million years ago, Floral characteristics and development were observed in and they are now considered ancient but distinctly special- two consecutive reproductive episodes (2015–2016) on ized flowering plants (Losada 2014). Being a primitive selected flowers of M. grandiflora. Flower buds were plant among angiosperms, the flowers of Magnolia are tagged from the bud initiation. Development of the measured as a theoretical starting point for understanding flower was observed daily and each stage was recorded the evolution of angiosperms (Cronquist 1981). M. grandi- systematically. Floral traits such as colour, shape, size, flora is a medium-sized evergreen tree, mostly distributed phyllotaxy, symmetry and numbers were examined and over East Asia, Central America and North America. Mag- tabulated by close observation. To determine the peak nolia encourages cross-pollination and is specifically time of anthesis, flowers were observed frequently at adapted to beetle pollination (Allain et al. 1999; Baker and regular intervals of the day and correlated with time, Hurd 1968; Gibbs et al. 1977;Ishida1996; Dieringer et al. temperature and humidity of the day. The opening and 1999). The seed set following natural pollination in vari- closing of each flower during the study period were re- ous species of Magnolia is reported to be low, i.e. 8.7% for corded separately. M. stellata (Hirayama et al. 2005), 13–25% for M. hypo- leuca (Kikuzawa