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Scrophulariaceae) in Northwestern Yunnan, China1

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Scrophulariaceae) in Northwestern Yunnan, China1 POLLINATION BIOLOGY OF Hong Wang2 and De-Zhu Li2* FOUR PEDICULARIS SPECIES (SCROPHULARIACEAE) IN NORTHWESTERN YUNNAN, CHINA1 ABSTRACT Pedicularis L. (Scrophulariaceae) represents a classic example of ¯oral morphological diversity for pollination biol- ogists. In the species-rich areas of the Himalayas there have been few studies on the pollination syndromes of Pedi- cularis, especially of the long-tubed species. In the summer and fall of 2000, the pollination biology of four species of Pedicularis was studied in Zhongdian of northwestern Yunnan, China. The four species, foraged by three bumblebee species, possess two different corolla types: Pedicularis lutescens Franch. ex Maxim. subsp. lutescens and P. densispica Franch. ex Maxim. have a short-tubed, erostrate, and nectariferous corolla type and are pollinated exclusively by Bombus friseanus Skorikov and B. lucorum Latr. workers foraging ¯ower nectar and pollinating nototribically; P. integrifolia Hook. f. and P. tricolor Hand.-Mazz. have long-tubed, rostrate, and nectarless corollas and are pollinated sternotribically by Bombus festivus Smith and B. friseanus workers hanging on the S-shaped beak or supported by the bowl-shaped lower lips. Cross-pollination by bumblebee workers is the most important reproductive mechanism observed for these Pedicularis in Yunnan. Nectar-foraging bumblebee queens and lepidopteran moths or butter¯ies were not found to pollinate any of these Pedicularis species. Otherwise, the interactions between Pedicularis and Bombus and pollination mechanisms in northwestern Yunnan are similar to those in Japan and North America. The present study provides new evidence that the Japanese species had evolved from Himalayan migrants in a pattern parallel to that of North American species. Key words: Bombus, northwestern Yunnan, Pedicularis, pollen/ovule ratio, pollination mechanism, Scrophulariaceae. Pedicularis (Scrophulariaceae) comprises some rolla form appears in species endemic to the Him- 600 to 800 species (Wang et al., 2003) and is one alayas (Macior, 1984). Because of its diverse co- of the largest angiosperm genera in the Northern rolla forms and large number of species, the origin Hemisphere (Mabberley, 1987; Yang et al., 1998). and evolution of Pedicularis have long intrigued The species of Pedicularis are generally perennial botanists. Limpricht (1924) considered the Hima- or annual (rarely biennial) herbs hemiparasitic on layan region as a center of origin, although Prain grasses. Floral morphology displays striking differ- (1890) earlier suggested that Pedicularis originated ences in the corolla shape and the length of the in the Holarctic and dispersed from a common bo- corolla tube. The corolla is strongly zygomorphic, real center. Hong (1983) identi®ed a small area in consisting of an upper lip (galea) enclosing four the Himalayas, in western Sichuan and northwest- introrse anthers and a style running the length of ern Yunnan, as containing ca. 300 species of Ped- the galea, with the stigma exserted beyond its tip. icularis. Pointing out the morphological diversity The galea can be variously beaked, toothed, and and high degree of endemism in this region, Macior crested, while the lower lip is variously trilobed, (1982, 1988) also favored the Himalayan origin hy- usually spreading, and external to the upper lip in pothesis. bud. Of four general corolla forms in the genus de- Pedicularis displays enormous diversity of ¯oral scribed by Maximowicz (1888) and Li (1951)Ði.e., form (Pennell, 1948) and is a classic example of beakless, toothless; beakless, toothed; beaked, pollination syndrome diversi®cation within a genus. short-tubed; beaked, long-tubedÐonly the last is Beginning in the late 19th century, pollination absent from Japan and North America, and this co- mechanisms of Pedicularis have been studied in 1 Project supported by the National Natural Science Foundation of China (No. 39970060) and the national program for R & D Infrastructure and Facility Development (2004DKA30430). We thank Cao-Chang Hu and Hui-Fen Zhu (KUN) for valuable help during ®eldwork. We also thank Jie Cai (Yunnan University, now KUN) for carrying out partial pollen analysis. We are grateful to Gary Hannan (Eastern Michigan University) for critical reading of an earlier version of the manuscript, and to Lazarus Walter Macior (Akron University, Ohio) for kind assistance with the literature. 2 Laboratory for Plant Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650204, China. *Author for correspondence: [email protected]. ANN.MISSOURI BOT.GARD. 92: 127±138. 2005. 128 Annals of the Missouri Botanical Garden North America and Europe. MuÈller (1881), Weed Table 1. Distribution of the four studied Pedicularis (1884), and Kunth (1898±1905) primarily consid- species. ered the ¯oral morphology and the foraging behav- iors of the pollinators. Since then, Macior (see 1982 Taxon Distribution for a summary of earlier studies; Macior, 1984, Pedicularis densispica Northwestern Yunnan, 1986) made a systematic and thorough investiga- western Sichuan, south- tion of the pollination ecology, endemic adaptation, ern and southeastern and evolution of pollination mechanisms in Pedi- Xizang cularis, primarily in the North American species. P. integrifolia Northwestern Yunnan, southwestern and western Meanwhile, Sprague (1962), Faegri and van der Pijl Sichuan, southeastern (1966), MacInnes (1972), and Kwak (1979) dem- Xizang; Bhutan, Nepal, onstrated similar patterns of pollination ecology in Sikkim this genus as well as co-adaptations between Ped- P. lutescens subsp. lutescens Northwestern Yunnan icularis and its pollinators. Earlier studies revealed P. tricolor Northwestern Yunnan that the evolution of Pedicularis has been closely co-adapted to its pollinators, principally bumble- bees (Bombus). Pollination has been noted for a Pedicularis species in northwestern Yunnan (Wang solitary bee (Osmia tristella)inP. semibarbata L. & Li, 1998; Wang, 1998) and provided evidence in (Macior, 1977) and by hummingbirds in P. densi- support of Macior's (1991) explanation of the func- ¯ora Benth. (Macior, 1986), with these seen as tion of the long-tubed species. Meanwhile, through more recent adaptations. Such phenomena have not insect bagging studies in Sichuan, Macior and Tang yet been observed in Chinese Pedicularis, but there (1997, 1999) reported pollinator dependence of are hundreds more taxa to observe. The pollination three Pedicularis species. However, knowledge of ecology of Pedicularis in Asia remained completely the pollination syndromes of Pedicularis in the unknown until Macior (1988) made his ®rst study Himalayas is far from adequate. Only the pollina- in Japan. Interestingly, his Japanese observations tion syndromes of 2 (e.g., P. siphonantha D. Don revealed a close parallel between pollination mech- var. delavayi (Franch. ex Maxim.) Tsoong and P. anisms in Japan and North America. Subsequently, longi¯ora Rudolph var. tubiformis (Klotzsch) some Asian species were observed primarily from Tsoong) of the 16 long-tubed species in Yunnan the western and Chinese Himalayas (Macior, 1991; have been documented. These, plus the other 2 Macior & Sood, 1990, Macior & Tang, 1997, 1999; species (P. megalantha D. Don and P. punctata Wang & Li, 1998; Macior et al., 2001). This study Decne.) observed in the western Himalayas, were was extended to the Himalayan species, especially the only 4 long-tubed species studied by pollination those bearing ¯owers of the unique long-tubed co- biologists. This study aimed mainly to test the con- rolla type, found only in the Himalayas. It was sug- troversial explanations about the function of the gested that the species with long-tubed beaks were long-tubed ¯owers and to compare it with the func- adapted to moth pollination (Pennell, 1943). How- tion of other types of corollas. One interesting ques- ever, Macior's preliminary observations revealed tion is whether the long-tubed species are polli- that the long, nectarless corolla tube was probably nated by lepidopteran insects or by bumblebees a ¯oral adaptation of these plants, which are dwarf- and the evolutionary consequences. It is believed sized at high elevations, for attracting other polli- that more studies on the pollination biology in the nators. Obviously, more case studies are needed to species-richest area will provide more light on the test Pennell's hypothesis and to compare Macior's cause of diversi®cation of Pedicularis. results in Japan and the western Himalayas. There are 352 species of Pedicularis in China, of which MATERIALS AND METHODS some 272 species are endemic (Yang et al., 1998), with some transboreal species of extensive geo- In the summer and fall of 2000, pollination in- graphic disjunctions (Macior, 1988), e.g., P. verti- vestigations were conducted in alpine areas of the cillata L. In southwestern China, the province of county of Zhongdian, northwestern Yunnan, China. Yunnan contains 151 species of Pedicularis, in- We here report the pollination biology of four Ped- cluding all four corolla forms, with about half of the icularis species in northwestern Yunnan, including endemic species in China and 16 long-tubed spe- two long-tubed species, P. integrifolia and P. tri- cies and varieties (Wang & Li, 1999; Li et al., color, and two short-tubed, erostrate, and nectari- 2002). In the summers of 1993 and 1997, we made ferous species, P. lutescens subsp. lutescens and P. a preliminary study of the pollination biology of densispica
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