Geographic isolation, pollination syndromes, and pollinator generalization in HimalayanRoscoeaspp. (Zingiberaceae)

Abstract

The pollination syndromes have been widely used to predict effective pollinators of plant species and provide the mechanistic explanation of floral diversity. However, in recent years, the predictive applicability of pollination syndromes has been frequently questioned. The accuracy of the syndromes among the closely related plant species may vary temporally and spatially. This suggests the need for the standardized, comprehensive evaluation of factors influencing the matching of a pollination syndrome of a plant species to the predominant pollinator community. We studied the pollination biology of three geographically/phenologically isolated alpine gingers (Roscoea auriculata, Roscoea capitata, and Roscoea tumjensis) exhibiting the correlated suites of floral traits that suggest long‐tongued insects as major pollinators, to test for the predictive power of the respective pollination syndrome. We also tested if geographical and temporal isolation affects interspecies breeding system and extent of pollinator generalization. We demonstrate that the three Roscoea species are self‐compatible but lack autonomous selfing, and thus completely rely on pollinators for pollination success. Five years of observations demonstrate that only diurnal insect visitors foraged on the flowers of the three Roscoea species. Estimates of the pollinator importance (pollen deposition) of the observed floral visitors indicate that morphologically mismatched bumblebees contribute more than 90% of pollination service in all the three Roscoea species, while long‐tongued butterflies and moths function as nectar robbers. We found that geographical isolation and temporal variation in flowering period does not affect the breeding system and pollinator generalization in the three Roscoea species. The three geographically and phenologically isolated Himalayan Roscoea spp., with long‐tongued insect pollination syndrome, exhibit generalized pollination system and primarily rely on the morphologically mismatched Bombus species for pollination success. While, for three Roscoea spp., our result suggests that pollination syndromes are a weak predictor of efficient contemporary pollinator community, it also substantiates the role of non‐pollinator agents for the evolution of floral traits. The evolution of Bombus pollination in these alpine gingers suggests how the mismatch between plant and pollinator phenology can lead to the emergence of novel reproductive strategies among the congeners, which ultimately seems to play a key role for the speciation and diversification of the genus Roscoea in the Himalayas.

Functional implications of the specialized staminal appendages in alpine ginger (Roscoeaspp.: Zingiberaceae)

“…The flowers were then left open to visitation by the potential floral visitors. Previous findings (Paudel et al., 2015, 2017, 2019) based on both observational data and bagging experiments suggest the absence of nocturnal pollinators to the study species. Thus, we focused our observation for diurnal visitors only.…”

“…Previous studies (Paudel et al., 2017, 2019) reveal that moths ( Macroglossum nycteris ) visit the flowers of R. alpina , R. capitata and R. tumjensis for nectar robbing, but do not facilitate their pollination. Bumblebees ( Bombus tanguticus ) and butterflies ( Pachliopta aristolochiae ) act as nectar robbers of R. auriculata .…”

“…These Roscoea spp. are self‐compatible, but their natural breeding does not occur through autonomous selfing (Paudel et al., 2015, 2019). Flowers of all six Roscoea spp.…”

“…The typical flowers of the genus Roscoea comprise a pair of staminal appendages that are derived from the joint between anther and filament and protrude as flangelike outgrowths in the opposite direction of anther lobes (Cowley, 1982, 2007; Ngamriabsakul, 2005). In the recent years, there have been several studies on the pollination biology of Roscoea species both in the Himalayan clade (Paudel, Burd, Shrestha, Dyer, & Li, 2018; Paudel, Kessler, Shrestha, Zhao, & Li, 2019; Paudel et al., 2016; Paudel, Shrestha, Dyer, & Li, 2017) and North‐Indo Chinese clade (Fan & Li, 2012; Zhang et al., 2010; Zhang & Li, 2008), but none of these studies addresses how the presence of staminal appendages benefits the pollination process. Meanwhile, previous studies on other plant groups, such as Incarvillea (Bignoniaceae), Salvia (Lamiaceae), Torenia fournieri (Scrophulariaceae), and Zingiber densissimum (Zingiberaceae), suggest that staminal appendages play a key role in pollen dispensing (Armstrong, 1992; Fan & Li, 2016; Han et al., 2008; Reith et al., 2007; Zhang et al., 2011).…”

Spatiotemporal shifts in the role of floral traits in shaping tropical plant-pollinator interactions

“…Fenster, Reynolds, Williams, Makowsky, & Dudash, 2015;Hargreaves, Johnson, & Nol, 2004;Rosas-Guerrero et al, 2014;Vandelook et al, 2019) and contradicting (e.g. Blüthgen, Menzel, Hovestadt, Fiala, & Blüthgen, 2007;Ollerton et al, 2009;Paudel, Kessler, Shrestha, Zhao, & Li, 2019;Rocha, Domingos-Melo, Zappi, & Machado, 2020;Wang, Wen, Qian, Pei, & Zhang, 2020) the validity of the pollination syndrome hypothesis. Researchers also demonstrated that pollination systems can show parallel adaptations to multiple pollinator groups (Dellinger, Scheer, et al, 2019), and thus suggested reclassification of some pollination syndromes (Dellinger, Chartier, et al, 2019), or proposed that pollination syndrome theory can be improved by other concepts, like optimal foraging theory or evolution stable strategy (Pyke, 2016).…”