Ecol Res (2015) 30: 507–515 DOI 10.1007/s11284-015-1248-4 ORIGINAL ARTICLE Gensheng Bao • Kenji Suetsugu • Hongsheng Wang Xiang Yao • Li Liu • Jing Ou • Chunjie Li Effects of the hemiparasitic plant Pedicularis kansuensis on plant community structure in a degraded grassland Received: 4 March 2014 / Accepted: 30 January 2015 / Published online: 12 February 2015 Ó The Ecological Society of Japan 2015 Abstract Species-rich grasslands have high conservation Fabaceae. We also found that aboveground biomass of value because they support diverse floral and faunal grasses and legumes was higher in quadrats from which assemblages. Alpine grassland is an important and the parasite had been removed than in intact controls, characteristic ecosystem of the Qinghai-Tibet Plateau, while the biomass of sedges and forbs was unaffected by but ca. 30 % has been severely degraded by the com- parasite removal. However, removal significantly de- bined effects of climate change, human activity, over- creased plant species richness and Shannon–Wiener di- grazing and rodent damage. One potential method to versity. These results suggest that P. kansuensis modifies restore grassland diversity involves using hemiparasitic the competitive balance in grassland communities of the plants to modify the competitive relationships among Qinghai-Tibet Plateau, allowing for colonization by neighboring species. A possible candidate is Pedicularis subordinate species and thereby enhancing species di- kansuensis, a hemiparasitic plant found in grasslands versity and contributing to restoration of these degraded throughout the Qinghai-Tibet Plateau, but more infor- grasslands. mation on its host associations and its effects on sur- rounding vegetation is required to assess its suitability. Keywords Host selectivity Æ Haustoria Æ Host range Æ Thus, we examined host associations of P. kansuensis by Community structure Æ Orobanchaceae direct root excavation at a selected site on the Qinghai- Tibet Plateau and found that haustoria formation is non-randomly distributed among host species, with Introduction preferential bias for members of Poaceae, Rosaceae and Parasitic plants, which comprise more than 20 families, Electronic supplementary material The online version of this article 270 genera and more than 1 % of all angiosperm species, (doi:10.1007/s11284-015-1248-4) contains supplementary material, are important components of numerous natural and semi- which is available to authorized users. natural communities (Press 1998). They can be classified G. Bao Æ X. Yao Æ L. Liu Æ C. Li (&) as root or shoot parasites depending where connections State Key Laboratory of Grassland Agro-Ecosystems, College of are formed with host plants and as hemiparasites or ho- Pastoral Agriculture Science and Technology, Lanzhou University, loparasites depending on whether they possess or lack P.O. Box 61, Lanzhou 730020, China functional chloroplasts, respectively (Musselman and E-mail: [email protected] Press 1995). Root hemiparasites retain the capacity for G. Bao photosynthesis, but are partially dependent upon hosts E-mail: [email protected] for the acquisition of water, mineral nutrients and carbon, which they obtain through connections made by special- G. Bao Æ H. Wang Grassland Institute, Qinghai Academy of Animal Science and ized organs called haustoria (Irving and Cameron 2009). Veterinary Medicine, 1 Weier Road, Biological Industrial District, It has been suggested that in semi-natural commu- Xining 810003 Qinghai, China nities, root hemiparasites capable of interacting with diverse host species may act as ecosystem engineers, K. Suetsugu Graduate School of Human and Environmental Studies, Kyoto modifying community structure and function (Pywell University, Yoshida-Nihonmatsu-cho, Sakyo, Kyoto 606-8501, et al. 2004; Ameloot et al. 2005; Decleer et al. 2013). Japan Although root hemiparasitic plants generally have a wide host range, they damage some species (preferred J. Ou hosts) more than others (Press and Phoenix 2005). Department of Biology, Qinghai University, 251 Ningda Road, Xining 810016 Qinghai, China Consequently, they may be capable of altering the 508 competitive balance among surrounding plants by de- candidate for use in grassland restoration programs in creasing the competitive advantage of dominant species, this region; yet, as a representative species of degraded allowing subordinate species the opportunity to colonize grasslands (Song 2006; Bao and Wang 2011), it may the habitat (Gibson and Watkinson 1992; Marvier 1998; have host preferences for subordinate species and thus Ameloot et al. 2005; Hedberg et al. 2005; Press and contribute to reductions in grassland diversity. Phoenix 2005; Hellstro¨ m et al. 2011; Decleer et al. 2013). More information on the host range, preferences In doing so, root hemiparasitic plants may alter plant and effects of P. kansuensis on degraded plant com- community structure and increase diversity. munities is essential both for understanding its eco- The ecological role of species in the root-hemi- logical role and for rigorously assessing its potential parasitic genus Rhinanthus has been well characterized use in the restoration of species-rich grasslands. Thus, (Gibson and Watkinson 1991, 1992; Davies et al. 1997). we examined the host selectivity and effects on com- Species of Rhinanthus prefer poaceous hosts and have munity structure and productivity of P. kansuensis at a been shown to reduce host competitive advantage, re- selected grassland site on the Qinghai-Tibet Plateau. leasing forb species from competitive exclusion and Specifically, we examined the host range by directly thereby enhancing grassland diversity (Westbury 2004; observing root systems, quantified host selectivity by Ameloot et al. 2005; Bardgett et al. 2006). The intro- comparing numbers of haustorial connections to each duction of Rhinanthus spp. has been effectively used to host species with root abundance and investigated the restore low-diversity pastures to high-diversity meadows effects of P. kansuensis removal on plant community in Europe (Pywell et al. 2004; Westbury 2004; Bullock structure and productivity. and Pywell 2005). However, little is known about the effects of other hemiparasites on the structure and pro- ductivity of natural plant communities, including whe- Materials and methods ther they increase species diversity by limiting competitive dominants and thereby facilitate coexistence Study species and site (Press and Phoenix 2005). If root hemiparasites prefer subordinate species as hosts, they could reduce the P. kansuensis Maxim. is an annual or biennial herb that abundance of subordinate species, enhancing the com- is endemic to northwestern China and typically grows to petitive advantage of dominant species, and reducing the 20–45 cm in height. The stems are usually straight with a overall diversity of the plant community (Gibson and terminal inflorescence that is typically 25–30 cm long, Watkinson 1989). Thus, rigorous assessment of hemi- with numerous purple–pink to purple–red, or sometimes parasitic species’ host preferences is required to predict white, flowers (Yang et al. 1998). It invades semi-natural their effects on specific ecosystems. or degraded grasslands and has been used as an indi- Species-rich grasslands have high conservation value cator species of degraded pastures (Qiu et al. 2006; Zhe because they support diverse floral and faunal assem- et al. 2010). Like other root or stem parasites, P. kan- blages. The Qinghai-Tibet Plateau, sometimes called the suensis absorbs nutrients and water from its host via Earth’s ‘‘third pole’’, is an important eco-region (Wang haustoria. and Cheng 2001) in which alpine grasslands are a Field studies were carried out at a grassland site in characteristic landscape. Combined effects of climate Haiyan County, Haibei Tibetan Autonomous Prefec- change, human activity, overgrazing and rodent dam- ture, Qinghai Province, China (37°03¢44.82¢¢N, age, however, have severely degraded almost 30 % of 100°42¢34.40¢¢E) between May and September of both alpine grasslands in the plateau (Yang et al. 2004; Shang 2012 and 2013. According to data acquired from the and Long 2007). Consequently, grassland restoration is weather bureau of Qinghai Province, the average annual vital to conserve biodiversity in the Qinghai-Tibet Pla- rainfall from 2000 to 2012 in this region was 286.4 mm, teau. most of which (180.5 mm) fell between June and August. Pedicularis (Orobanchaceae) is one of the largest The mean annual average temperature was À1.9 °C, genera of flowering plants, comprising 800 species with monthly means ranging from À16.4 °C in January mainly distributed in montane and alpine zones of the to 11.8 °C in August. Because of intense grazing, northern hemisphere (Mill 2001; Wang et al. 2003;Ree vegetative cover at the site during the study period was 2005). There are an estimated 364 species of Pedicularis less than 60 %. Therefore, according to the cover scale in China alone (Yang et al. 2010; Yu et al. 2011), most of of Zhou et al. (2005) (non-degraded >85 %, lightly which inhabit degraded or semi-natural grasslands with degraded 70–85 %, moderately degraded 50–70 %, a consistent assemblage of co-occurring plants (Zhou heavily degraded <50 %), the grassland was classified et al. 2003; Qiu et al. 2006; Zhe et al. 2010). Many as moderately degraded. The vegetation of this alpine Pedicularis species can exploit a wide range of hosts grassland was composed primarily of Kobresia capilli- (Piehl 1963; Musselman and Mann