Pollen Aggregation by Viscin Threads in Rhododendron Varies with Pollinator
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Research Pollen aggregation by viscin threads in Rhododendron varies with pollinator Yun-Peng Song1*, Zhi-Huan Huang2* and Shuang-Quan Huang1 1Institute of Evolution and Ecology, School of Life Sciences, Central China Normal University, Wuhan 430079, China; 2Guangxi Institute of Botany, Guangxi Zhuang Autonomous Region and Chinese Academy of Sciences, Guilin 541006, China Summary Author for correspondence: Pollen grains can be dispersed singly or variously aggregated in groups. Whether the evolu- Shuang-Quan Huang tion of pollen aggregation is driven by the pollinator remains unexplored. We hypothesize that Tel: +86 27 67867221 an extensive pollen aggregation is favored under a scarcity of pollinators. Email: [email protected] Variation in pollen aggregation by viscin threads in 13 Rhododendron species was mea- Received: 13 May 2018 sured as it is related to pollen removal in a visit. Visitation rates of functional pollinator groups Accepted: 13 July 2018 that vary in their grooming behavior were investigated in each species. Pollen deposited on stigmas in the field was also sampled. New Phytologist (2019) 221: 1150–1159 Seven Rhododendron species were infrequently pollinated by low-intensity grooming ani- doi: 10.1111/nph.15391 mals, including birds, butterflies and moths. The other six species were more frequently polli- nated by bees with a high intensity of pollen grooming. Bird- and Lepidoptera-pollinated Key words: floral traits, pollen aggregation, species produced longer pollen-connecting threads that connected more pollen grains. Phylo- pollen dosing strategy, pollen grooming genetically independent contrast analysis of the 13 species showed that pollinator visitation behavior, pollen-thread tangles, pollinator frequency was negatively related to amounts of pollen removal per visit but not to stigmatic functional groups, Rhododendron. pollen loads. The finding of interspecific patterns in pollen removal related to pollinator visitation fre- quency suggests pollinator-mediated selection on pollen packaging strategies, supporting the hypothesis of floral evolution via pollen export. of their bodies while moving between flowers (in-flight groom- Introduction ing; Harder, 1998; Tong & Huang, 2018). By contrast, birds Pollinators and plants often confront a conflict of interest con- and Lepidoptera usually visit flowers to forage for nectar and do cerning the fate of pollen. From the perspective of pollinators, not groom pollen so regularly, lacking comb-like structures such selection for enhancing foraging efficiency would be favored, as bees have evolved (Harder, 1998). Pollen grains on beaks or whereas for plants, selection for reducing pollen loss would be feathers are likely to be available for deposition during subse- favored. Models show that animal-pollinated plants benefit from quent visits to receptive flowers, with little pollen loss during presenting pollen in small doses to a large number of pollinators transfer (Muchhala & Thomson, 2010). The optimal pollen pre- as a means of alleviating diminishing returns on male investment sentation strategy is expected to be governed by the frequency of (Harder & Thomson, 1989). The amount of pollen placed on a pollinator visits (Harder & Thomson, 1989), and the capacities pollinator does not generally correlate linearly with the number of those pollinators to remove and transfer pollen (Harder & of grains deposited on stigmas. Compared with small pollen Wilson, 1994; Thomson et al., 2000; Castellanos et al., 2006; doses placed on pollinators, large pollen doses export proportion- Muchhala & Thomson, 2010). ately smaller quantities of pollen to stigmas, i.e. diminishing The modes of anther dehiscence and pollen packaging among returns on dose size investment (Harder & Thomson, 1989). anthers greatly influence patterns of pollen presentation (Harder Castellanos et al. (2003) compared pollen transfer efficiency & Thomson, 1989; Thomson et al., 2000). Pollen grains of most between bee- and bird-pollinated Penstemon species, and argued species are monads, i.e. single mature pollen grains, but different that different modes of pollen presentation between these groups forms of pollen aggregation, involving tetrads, polyads, pollen were favored by very different intensities of grooming behavior threads and pollinia, have independently evolved among flower- between the two functional pollinator groups, leading to diver- ing plants (Harder & Johnson, 2008). Pollen grains in orchids gent pollen presenting strategies (Castellanos et al., 2006). Bees are grouped into cohesive masses. Such a pollen presentation frequently groom pollen grains off the stigma-contacting surfaces strategy has been considered to rescue the last chance for pollen to be dispersed given that orchids often experience pollinator *Y-P.S. and Z-H.H. contributed equally to this work. scarcity, facilitating the removal of large numbers of pollen grains 1150 New Phytologist (2019) 221: 1150–1159 Ó 2018 The Authors www.newphytologist.com New Phytologist Ó 2018 New Phytologist Trust New Phytologist Research 1151 in a single pollinator visit. Pollen grains are united by viscin variable size from an individual anther. Based on floral traits, it threads in only two families, Ericaceae and Onagraceae (Cruden has been proposed that diverse Rhododendron species may be & Jensen, 1979; Kress, 1981; Knox & McConchie, 1986; Hesse pollinated by bats (in the tropics), birds, Lepidoptera or et al., 2000). These sporopollenin-containing threads that are bees (Stevens, 1976). Early observations of pollinators long, thin, flexible ropes on pollen surface, connecting single pol- indicated that bees (particularly bumblebees) were effective len grains or pollen tetrads (Hesse, 1984) allow aggregation of pollinators of Rhododendron aureum (Kudo et al., 2011), clusters of pollen grains of varying sizes. However, pollen removal Rhododendron cyanocarpum and Rhododendron delavayi (Ma et al., or receipt has not been measured in species with pollen grains 2010), Rhododendron eriocarpum and Rhododendron indicum united by viscin threads (Harder & Johnson, 2008), in which (Tagane et al., 2008), and Rhododendron ponticum (Stout et al., reproductive strategies remain unexplored empirically. 2006; Stout, 2007), but recent investigations involving pollinator Large masses of pollen attached to pollinator bodies are benefi- exclusion experiments showed that birds and butterflies con- cial for plants only if the pollinators do not collect pollen as a tributed more to pollination in larger-flowered species (Epps reward; otherwise, passive loss of pollen increases with large pol- et al., 2015; Huang et al., 2017). len loads on pollinators. For example, the most evolutionarily We sampled 13 Rhododendron species (Table 1) at Cangshan derived forms of pollen aggregation, i.e. pollinia in Orchidaceae Mountain in the East Himalayas, Yunnan Province, southwestern and Apocynaceae (Harder & Johnson, 2008), are rarely groomed China (25°400N, 100°060E) during the flowering period from off during a pollinator visit, but remain on the body to contact late March to early June 2012, 2013, 2016 and 2017. stigmas. If pollen grains are intensively groomed by pollinators, small pollen loads would be favored, limiting removal loss Pollinator species and visitation frequency (Harder & Wilson, 1994). However, if pollinator visitation rates are low, small loads involve a high risk of removal failure (Harder To compare pollinator species and visitation frequency in the 13 & Routley, 2006). In Rhododendron (Ericaceae), anecdotal obser- species, we observed floral visitors to at least three flowering indi- vations show that large-flowered species usually have long viscin viduals for > 10 h in each species. We made at least 20 9 30-min threads and are pollinated by birds and Lepidoptera, which rarely surveys, all between 08:00 h and 18:00 h local time during 2–3d initiate active grooming during foraging bouts, while small- of fine weather. Different kinds of visitors to tagged inflores- flowered species have short viscin threads and are pollinated by cences and numbers of flowers on these inflorescences were bees (Huang et al., 2017). recorded (Huang et al., 2017). Visitors that contacted stigmas To test the hypothesis of pollinator-mediated selection on flo- and anthers and had pollen attached to their bodies were ral evolution, empirical study of pollen removal as a measure of regarded as potential pollinators. Diurnal visitation rates were plant reproductive success is needed. Although a shift of func- recorded as visits per flower per 0.5 h (Fang et al., 2012). Noctur- tional pollinator groups has been considered as an important nal visitation was difficult to observe, so we used an indirect driver for evolution of floral traits among related species method to assess moth visitation to estimate nocturnal visitation (Schemske & Bradshaw, 1999; Fenster et al., 2004; Whittall & by observing moth scale deposition on stigmas under a micro- Hodges, 2007; Harder & Johnson, 2009), very few comparative scope (Singer & Cocucci, 1997; Alonso-Pedano & Ortega-Baes, studies have attempted to estimate pollen removal, leaving the 2012). At least 30 flowers approaching senescence from 10 plants hypothesis poorly tested empirically. To explore whether degrees per species were randomly collected during two fine days. We of pollen aggregation are driven by pollinator selection, we com- pared pollinator functional groups (with different intensities of Æ pollen grooming) and their visitation rates among 13 Table 1 Comparisons