Plant Biology ISSN 1435-8603 RESEARCH PAPER Reproductive biology of two Himalayan alpine gingers (Roscoea spp., Zingiberaceae) in China: pollination syndrome and compensatory floral mechanisms Z.-Q. Zhang1,2, W. J. Kress1,3, W.-J. Xie4, P.-Y. Ren1, J.-Y. Gao1 & Q.-J. Li1 1 Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Yunnan, China 2 Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Yunnan, China 3 Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA 4 Flower Research Institute, Yunnan Academy of Agricultural Sciences, Yunnan, China Keywords ABSTRACT Biodiversity hotspot; compensatory floral mechanism; conservation; Hengduan According to the concept of pollination syndromes, floral traits reflect specialisation Mountains; long-proboscid pollinator; to a particular pollinator or set of pollinators. However, the reproductive biology of pollination syndrome. endemic, and often specialised, plants may require increased attention as climate change accelerates worldwide. Species of Roscoea endemic to the Himalayan region Correspondence have striking orchid-like flowers with long corolla tubes, suggesting pollination by Q.-J. Li, Key Laboratory of Tropical Forest long-tongued insects. Until now, the reproductive biology of species of Roscoea has Ecology, Xishuangbanna Tropical Botanical been poorly documented. We investigated the floral biology, breeding system and Garden, Chinese Academy of Sciences, pollination ecology of R. cautleoides and R. humeana, from Hengduan Mountains, a Yunnan 666303, China. global biodiversity hotspot in southwest China. We also tested whether floral lon- E-mail: [email protected] gevity increases pollination success. Pollination experiments showed that the two species were self-compatible and depended on insects for fruit production. Over Editor several flowering seasons we did not observe any potential pollinators with long A. Dafni tongues that matched the corolla tube visiting flowers in centres of distribution. The principal pollinators observed were pollen-collecting generalist bees, with low Received: 7 April 2010; Accepted: 26 visitation frequencies. In general, members of the ginger family are characterised by October 2010 short-lived (usually 1 day) flowers, but flowers of R. cautleoides and R. humeana last 8 and 6 days, respectively. Removing stigmas decreased fruit set in both study doi:10.1111/j.1438-8677.2010.00423.x populations. Our results suggest that the original pollinators may have been long- tongued insects that are now absent from the Chinese Himalayas because habitats have responded to climate change. However, long-lived and self-compatible flowers, coupled with the presence of generalist pollinators, are traits that have allowed these gingers to reproduce and continue to persist in the alpine habitats. A number of specialised pollination systems have been INTRODUCTION described in global hotspots, where exceptional concentrations The relationship between plants and their animal pollinators of endemic species are found, such as the Cape Floral Region of has been widely used since the time of Darwin as a model sys- South Africa (Goldblatt & Manning 2000; Pauw 2006). Increas- tem for the study of adaptation (Barrett 2010). Observations ing evidence suggests that global change will have a significant of pollination systems by Darwin (1862), Vogel (1954) and impact on plant–pollinator interactions, and may result in bio- others suggested that different pollinators promoted selection diversity loss (reviewed in Alonso et al. 2010). Recent investiga- for diverse floral forms, which produced an array of ‘pollina- tions indicate that pollinator populations across the globe are tion syndromes’ – suites of convergent floral traits that are declining, especially in biodiversity hotspots (Mitchell & adapted to their particular pollinators (reviewed in Fenster Ashman 2008). In addition, the exceptional concentration of et al. 2004). The concept of pollination syndromes has been a endemic species present in such biodiversity hotspots suggests fundamental subject in plant reproductive ecology because of that these local species are facing a higher risk of extinction its capacity to predict the pollinator type of a given species than more widespread taxa (Johnson 2004; Vamosi et al. based on the basis of its floral traits (Vogel 1954; Faegri & 2006). Therefore, understanding specialised plant–pollinator van der Pijl 1979; Fenster et al. 2004). The most famous interactions and floral adaptation is critical in a rapidly chang- example is Darwin’s prediction of the long-proboscid pollina- ing world from a conservation perspective (Kearns et al. 1998; tor of a Malagasy orchid with an extremely long nectar spur Johnson 2004). In fact, little is known about the reproductive (Darwin 1862). Many works that have followed these original biology of the majority of plants in species-rich tropical studies have also strongly supported and crystallised this con- countries where many such hotspots are located. cept. However, whether pollination syndromes exist continues The genus Roscoea is a small genus of 18 species in the to be debated (e.g. Ollerton et al. 2007). ginger (Zingiberaceae) family (Cowley 2007). The striking Plant Biology ª 2010 German Botanical Society and The Royal Botanical Society of the Netherlands 1 Reproductive biology of two Himalayan alpine gingers Zhang, Kress, Xie, Ren, Gao & Li orchid-like flowers generally have long corolla tubes and pro- Roscoea humeana and R. cautleoides are perennial hermaph- vide nectar as a reward, suggesting a long-tongued insect flo- roditic herbs, reaching a height of 9–40 cm. At our study site, ral syndrome. In addition, similar to the genus Salvia they are sympatric and usually co-flower from May to June. (Lamiaceae; Troll 1929; Classen-Bockhoff et al. 2003), the The two species of Roscoea are distinguished through both veg- versatile anther is reversibly movable. However, in contrast to etative features and floral characteristics (Fig. 1A and B). Ros- Salvia with elongated connectives, the thecae in the Zingiber- coea humeana has ovate, sessile leaves while R. cautleoides has aceae are elongated, pivoting around a thin joint. This anther narrowly lanceolate, petiolate leaves. In this research site, flow- structure was first described in Roscoea by Lynch (1882), who ers of R. humeana are purple while flowers of R. cautleoides are predicted that it is a mechanism for cross-fertilisation. bright yellow with a longer flora tube than R. cautleoides (Fig. 1 The Zingiberaceae is a large, predominantly tropical family C). In addition, R. humeana generally flowers before the leaves of animal-pollinated pantropical monocotyledons, comprising emerge, while flowers of R. cautleoides are located at the apex about 1300 species in 52 genera (Kress et al. 2002). Floral mor- of a leafy shoot. In spite of their floral and vegetative differ- phologies are correlated with corresponding pollinator groups ences, a phylogenetic analyses of the ITS region suggested that in many ginger species (reviewed in Sakai et al. 1999; Kress & R. humeana and R. cautleoides are closely related in a small Specht 2005). Despite our increasing knowledge of the repro- unresolved clade of four species in the genus (Ngamriabsakul et ductive biology of the ginger family (Li et al. 2001; Wang et al. al. 2000). Our research site is in the core of the distributional 2004), only one detailed study has been conducted on the pol- range of both species, which is restricted to the southeast part lination system of the only true alpine genus, Roscoea (Zhang of Hengduan Mountains, i.e., Northern Yunnan Province and & Li 2008). Furthermore, most species of Roscoea are concen- neighbouring Sichuan Province. trated in the eastern Himalayas (Nepal to north India) and the Hengduan Mountains of southwest China (Cowley 2007). This Flower biology area is widely regarded as a global biodiversity hotspot because of its high species diversity and endemism (Wilson 1992; We conducted our phenological observations in Ganhaizi in Myers et al. 2000), but little information is available on repro- 2004. We randomly selected 63 individuals of each species on ductive biology of the endemic plant species in this area. which we counted inflorescences per plant and flowers per Here, we describe the floral biology, breeding system and inflorescence; one unopened bud was selected in each individ- pollination ecology of two sympatric species of Roscoea, R. ual for recording flower longevity. The length of the corolla cautleoides and R. humeana. We explore the possible adaptive tube was measured on 30 flowers per species using a vernier significance of floral traits in relation to pollinator type and caliper. To measure the nectar concentration and volume, we environmental conditions. According to the concept of polli- haphazardly selected approximately 60 flowers of each species nation syndromes, floral trait combinations reflect the polli- (one flower from each plant) and bagged them in nylon net nator type. Thus, we predicted that long-proboscid insects bags before the flowers opened. After anthesis, six flowers of should be the pollinators of long-tubed Roscoea, which was each species were chosen and removed from plants at 09:00, supported by preliminary observations in the eastern Himala- 12:00 and 15:00 h on three consecutive days to measure nectar yas (Fletcher & Son 1931; Dierl 1968). Through