Skip to main content
Log in

Effects of the hemiparasitic plant Pedicularis kansuensis on plant community structure in a degraded grassland

  • Original Article
  • Published:
Ecological Research

Abstract

Species-rich grasslands have high conservation value because they support diverse floral and faunal assemblages. Alpine grassland is an important and characteristic ecosystem of the Qinghai-Tibet Plateau, but ca. 30 % has been severely degraded by the combined effects of climate change, human activity, overgrazing and rodent damage. One potential method to restore grassland diversity involves using hemiparasitic plants to modify the competitive relationships among neighboring species. A possible candidate is Pedicularis kansuensis, a hemiparasitic plant found in grasslands throughout the Qinghai-Tibet Plateau, but more information on its host associations and its effects on surrounding vegetation is required to assess its suitability. Thus, we examined host associations of P. kansuensis by 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 preferential bias for members of Poaceae, Rosaceae and Fabaceae. We also found that aboveground biomass of grasses and legumes was higher in quadrats from which the parasite had been removed than in intact controls, while the biomass of sedges and forbs was unaffected by parasite removal. However, removal significantly decreased plant species richness and Shannon–Wiener diversity. These results suggest that P. kansuensis modifies the competitive balance in grassland communities of the Qinghai-Tibet Plateau, allowing for colonization by subordinate species and thereby enhancing species diversity and contributing to restoration of these degraded grasslands.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ameloot E, Verheyen K, Hermy M (2005) Meta-analysis of standing crop reduction by Rhinanthus spp. and its effect on vegetation structure. Folia Geobotanica 40:289–310

    Article  Google Scholar 

  • Bao G, Wang H (2011) Allelopathic effects of Pedicularis kansuensis Maxim. on several graminaceous grass species on alpine meadow. Chin J Grassl 33:88–94 (in Chinese)

    Google Scholar 

  • Bardgett RD, Smith RS, Shiel RS, Peacock S, Simkin JM, Quirk H, Hobbs PJ (2006) Parasitic plants indirectly regulate below-ground properties in grassland ecosystems. Nature 439:969–972

    Article  CAS  PubMed  Google Scholar 

  • Borowicz VA, Armstrong JE (2012) Resource limitation and the role of a hemiparasite on a restored prairie. Oecologia 169:783–792

    Article  PubMed  Google Scholar 

  • Bullock J, Pywell R (2005) Rhinanthus: a tool for restoring diverse grassland? Folia Geobotanica 40:273–288

    Article  Google Scholar 

  • Cameron DD, Seel WE (2007) Functional anatomy of haustoria formed by Rhinanthus minor: linking evidence from histology and isotope tracing. New Phytol 174:412–419

    Article  CAS  PubMed  Google Scholar 

  • Cameron DD, Hwangbo JK, Keith AM, Geniez JM, Kraushaar D, Rowntree J, Seel WE (2005) Interactions between the hemiparasitic angiosperm Rhinanthus minor and its hosts: from the cell to the ecosystem. Folia Geobotanica 40:217–229

    Article  Google Scholar 

  • Cameron DD, Coats AM, Seel WE (2006) Differential resistance among host and non-host species underlies the variable success of the hemi-parasitic plant Rhinanthus minor. Ann Bot 98:1289–1299

    Article  PubMed Central  PubMed  Google Scholar 

  • Chuang T, Heckard L (1971) Observations on root-parasitism in Cordylanthus (Scrophulariaceae). Am J Bot 58:218–228

    Article  Google Scholar 

  • Davies D, Graves J, Elias C, Williams P (1997) The impact of Rhinanthus spp. on sward productivity and composition: implications for the restoration of species-rich grasslands. Biol Conserv 82:87–93

    Article  Google Scholar 

  • Decleer K, Bonte D, Van Diggelen R (2013) The hemiparasite Pedicularis palustris: ‘Ecosystem engineer’ for fen-meadow restoration. J Nature Conserv 21:65–71

    Article  Google Scholar 

  • Fisher J, Phoenix G, Childs D, Press M, Smith S, Pilkington M, Cameron D (2013) Parasitic plant litter input: a novel indirect mechanism influencing plant community structure. New Phytol 198:222–231

    Article  PubMed  Google Scholar 

  • Gauslaa Y, Odasz AM (1990) Water relations, temperatures, and mineral nutrients in Pedicularis dasyantha (Scrophulariaceae) from Svalbard, Norway. Holarct Ecol 13:112–121

    Google Scholar 

  • Gibson C, Watkinson A (1989) The host range and selectivity of a parasitic plant: Rhinanthus minor L. Oecologia 78:401–406

    Article  Google Scholar 

  • Gibson C, Watkinson A (1991) Host selectivity and the mediation of competition by the root hemiparasite Rhinanthus minor. Oecologia 86:81–87

    Article  Google Scholar 

  • Gibson C, Watkinson A (1992) The role of the hemiparasitic annual Rhinanthus minor in determining grassland community structure. Oecologia 89:62–68

    Article  Google Scholar 

  • Hedberg A, Borowicz V, Armstrong J (2005) Interactions between a hemiparasitic plant, Pedicularis canadensis L. (Orobanchaceae), and members of a tallgrass prairie community. J Torrey Bot Soc 132:401–410

    Article  Google Scholar 

  • Hellström K, Bullock J, Pywell R (2011) Testing the generality of hemiparasitic plant effects on mesotrophic grasslands: a multi-site experiment. Basic Appl Ecol 12:235–243

    Article  Google Scholar 

  • Huang X, Guan K, Li A (2011) Biological traits and their ecological significances of parasitic plants: a review. Chin J Ecol 30:1838–1844 (in Chinese)

    Google Scholar 

  • Irving L, Cameron D (2009) You are what you eat: interactions between root parasitic plants and their hosts. Adv Bot Res 50:87–138

    Article  CAS  Google Scholar 

  • Jiang F, Jeschke W, Hartung W, Cameron D (2008) Does legume nitrogen fixation underpin host quality for the hemiparasitic plant Rhinanthus minor? J Exp Bot 59:917–925

    Article  CAS  PubMed  Google Scholar 

  • Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley

    Google Scholar 

  • Lafferty K, Dobson A, Kuris A (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:11211–11216

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lafferty K, Allesina S, Arim M, Briggs C, De Leo G, Dobson A, Dunne J, Johnson P, Kuris A, Marcogliese D (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546

    Article  PubMed Central  PubMed  Google Scholar 

  • Li X, Gao J, Brierley G, Qiao Y, Zhang J, Yang Y (2011) Rangeland degradation on the Qinghai-Tibet plateau: implications for rehabilitation. Land Degrad Dev 24:72–80

    Article  Google Scholar 

  • Malcolm W (1966) Root parasitism of Castilleja coccinea. Ecology 47:179–186

    Article  Google Scholar 

  • Marvier MA (1998) Parasite impacts on host communities: plant parasitism in a California coastal prairie. Ecology 79:2616–2623

    Google Scholar 

  • Marvier M, Smith D (1997) Conservation implications of host use for rare parasitic plants. Conserv Biol 11:839–848

    Article  Google Scholar 

  • Mill R (2001) Notes relating to the flora of Bhutan: XLIII. Scrophulariaceae (Pedicularis). Edinb J Bot 58:57–98

    Google Scholar 

  • Musselman L, Mann W (1977) Host plants of some Rhinanthoideae (Scrophulariaceae) of eastern North America. Plant Syst Evol 127:45–53

    Article  Google Scholar 

  • Musselman L, Press M (1995) Introduction to parasitic plants. In: Press M, Graves J (eds) parasitic plants. Chapman & Hall, London, pp 1–13

    Google Scholar 

  • Pate J (1995) Mineral relationships of parasites and their hosts. In: Press MC, Graves JD (eds) Parasitic plants. Chapman and Hall, London, pp 80–102

    Google Scholar 

  • Pennings S, Callaway R (1996) Impact of a parasitic plant on the structure and dynamics of salt marsh vegetation. Ecology 77:1410–1419

    Article  Google Scholar 

  • Piehl M (1963) Mode of attachment, haustorium structure, and hosts of Pedicularis canadensis. Am J Bot 50:978–985

    Article  Google Scholar 

  • Press M (1998) Dracula or Robin Hood? A functional role for root hemiparasites in nutrient poor ecosystems. Oikos 82:609–611

    Article  Google Scholar 

  • Press MC, Graves JD (1995) Parasitic plants. Chapman & Hall Ltd, London

    Google Scholar 

  • Press M, Phoenix G (2005) Impacts of parasitic plants on natural communities. New Phytol 166:737–751

    Article  PubMed  Google Scholar 

  • Pywell R, Bullock J, Walker K, Coulson S, Gregory S, Stevenson M (2004) Facilitating grassland diversification using the hemiparasitic plant Rhinanthus minor. J Appl Ecol 41:880–887

    Article  Google Scholar 

  • Qiu Z, Ma Y, Shi J, Pan D, Li R (2006) Influence of Pedicularis kansuensis on Elymus nutans artificial grassland in “Black Soil Type” degenerated alpine grassland. Grassl Turf 5:26–29 (in Chinese)

    Google Scholar 

  • Quested H, Cornelissen J, Press M, Callaghan T, Aerts R, Trosien F, Riemann P, Gwynn-Jones D, Kondratchuk A, Jonasson S (2003a) Decomposition of sub-arctic plants with differing nitrogen economies: a functional role for hemiparasites. Ecology 84:3209–3221

    Article  Google Scholar 

  • Quested H, Press M, Callaghan T (2003b) Litter of the hemiparasite Bartsia alpina enhances plant growth: evidence for a functional role in nutrient cycling. Oecologia 135:606–614

    Article  PubMed  Google Scholar 

  • Ree R (2005) Phylogeny and the evolution of floral diversity in Pedicularis (Orobanchaceae). Int J Plant Sci 166:595–613

    Article  CAS  Google Scholar 

  • Reed J (2012) The effects of hemiparasitism by Castilleja species on community structure in alpine ecosystems. Purs J Undergrad Res Univ Tennessee 3:8

    Google Scholar 

  • Ren Y, Guan K, Li A, Hu X, Zhang L (2010) Host dependence and preference of the root hemiparasite, Pedicularis cephalantha Franch. (Orobanchaceae). Folia Geobotanica 45:443–455

    Article  Google Scholar 

  • Ren G, Shang Z, Long R, Hou Y, Deng B (2013) The relationship of vegetation and soil differentiation during the formation of black-soil-type degraded meadows in the headwater of the Qinghai-Tibetan Plateau, China. Environ Earth Sci 69:235–245

    Article  Google Scholar 

  • Rümer S, Cameron DD, Wacker R, Hartung W, Jiang F (2007) An anatomical study of the haustoria of Rhinanthus minor attached to roots of different hosts. Flora 202:194–200

    Article  Google Scholar 

  • Sato T, Watanabe K, Kanaiwa M, Niizuma Y, Harada Y, Lafferty K (2011) Nematomorph parasites drive energy flow through a riparian ecosystem. Ecology 92:201–207

    Article  PubMed  Google Scholar 

  • Sato T, Egusa T, Fukushima K, Oda T, Ohte N, Tokuchi N, Watanabe K, Kanaiwa M, Murakami I, Lafferty K (2012) Nematomorph parasites indirectly alter the food web and ecosystem function of streams through behavioural manipulation of their cricket hosts. Ecol Lett 15:786–793

    Article  PubMed  Google Scholar 

  • Shang Z, Long R (2007) Formation causes and recovery of the “Black Soil Type” degraded alpine grassland in Qinghai-Tibetan Plateau. Front Agric China 1:197–202

    Article  Google Scholar 

  • Song Z (2006) It is urgent task to recover and comprehensively manage the grassland ecology of Bayingbuluke. Chin J Agric Resour Reg Plan 27:21–25 (in Chinese)

    Google Scholar 

  • Spasojevic M, Suding K (2011) Contrasting effects of hemiparasites on ecosystem processes: can positive litter effects offset the negative effects of parasitism? Oecologia 165:193–200

    Article  PubMed Central  PubMed  Google Scholar 

  • Suetsugu K, Kawakita A, Kato M (2008) Host range and selectivity of the hemiparasitic plant Thesium chinense (Santalaceae). Ann Bot 102:49–55

    Article  PubMed Central  PubMed  Google Scholar 

  • Suetsugu K, Takeuchi Y, Futai K, Kato M (2012) Host selectivity, haustorial anatomy and impact of the invasive parasite Parentucellia viscosa on floodplain vegetative communities in Japan. Bot J Linn Soc 170:69–78

    Article  Google Scholar 

  • Těšitel J, Lepš J, Vráblová M, Cameron DD (2011) The role of heterotrophic carbon acquisition by the hemiparasitic plant Rhinanthus alectorolophus in seedling establishment in natural communities: a physiological perspective. New Phytol 192:188–199

    Article  PubMed  Google Scholar 

  • Těšitel J, Hejcman M, Lepš J, Cameron DD (2013) How does elevated grassland productivity influence populations of root hemiparasites? Commentary on Borowicz and Armstrong (Oecologia 2012). Oecologia 172:933–936

    Article  PubMed  Google Scholar 

  • Van Hoveln MD, Evans BA, Borowicz VA (2011) Hemiparasite—host plant interactions and the impact of herbivory: a field experiment. Botany 89:537–544

    Article  Google Scholar 

  • Wang G, Cheng G (2001) Characteristics of grassland and ecological changes of vegetations in the source regions of Yangtze and Yellow rivers. J Desert Res 21:101–107

    CAS  Google Scholar 

  • Wang H, Mill R, Blackmore S (2003) Pollen morphology and infra-generic evolutionary relationships in some Chinese species of Pedicularis (Scrophulariaceae). Plant Syst Evol 237:1–17

    Article  Google Scholar 

  • Watling J, Press M (2001) Impacts of infection by parasitic angiosperms on host photosynthesis. Plant Biol 3:244–250

    Article  CAS  Google Scholar 

  • Westbury D (2004) Rhinanthus minor L. J Ecol 92:906–927

    Article  Google Scholar 

  • Whittaker R (1972) Evolution and measurement of species diversity. Taxon 21:213–251

    Article  Google Scholar 

  • Yang H, Holmgren N, Mill R (1998) Pedicularis Linn. In: Wu ZY, Raven PH (eds) Flora of China, Scrophulariaceae–Gesneriaceae. Science Press, Beijing, p 156

    Google Scholar 

  • Yang M, Wang S, Yao T, Gou X, Lu A, Guo X (2004) Desertification and its relationship with permafrost degradation in Qinghai-Xizang (Tibet) plateau. Cold Reg Sci Technol 39:47–53

    Article  Google Scholar 

  • Yang Y, Fang J, Ma W, Guo D, Mohammat A (2010) Large-scale pattern of biomass partitioning across China’s grasslands. Glob Ecol Biogeogr 19:268–277

    Article  Google Scholar 

  • Yu W, Huang P, Ree RH, Liu M, Li D, Wang H (2011) DNA barcoding of Pedicularis L. (Orobanchaceae): evaluating four universal barcode loci in a large and hemiparasitic genus. J Syst Evol 49:425–437

    Article  Google Scholar 

  • Zhe C, Zhou H, Zhao X, Wen J, Ye X, Yang Y (2010) The effect of Alpine meadow degradation on Pedicularis kansuensis’s growth and resource allocation in blooming date. Ecol Environ Sci 19:2800–2807

    Google Scholar 

  • Zhou H, Zhou L, Zhao X, Liu W, Yan Z, Shi Y (2003) Degradation process and integrated treatment of “black soil beach” grassland in the source regions of Yangtze and Yellow rivers. Chin J Ecol 22:51–55 (in Chinese)

    Google Scholar 

  • Zhou H, Zhao X, Tang Y, Gu S, Zhou L (2005) Alpine grassland degradation and its control in the source region of the Yangtze and Yellow Rivers, China. Grassl Sci 51:191–203

    Article  Google Scholar 

Download references

Acknowledgments

We wish to thank Dr. Jakub Těšitel and an anonymous reviewer for their constructive comments on an earlier version of the manuscript. Prof. Steve W. Adkins, Chunping Zhang and Chunhui Zhang helped revise the manuscript, Minglong Yuan and Hui Song gave inspiring advice on the manuscript, and Mr. Huiqiang Li assisted with sampling. The research was financially supported by the National Key Basic Research Program (973) of China (2014CB138702), the Natural Science Foundation of China (31372366), the Program for Changjiang Scholars and Innovative Research Team in University (IRT13019) and the Special Fund for Agro-Scientific Research in the Public Interest (201203041).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chunjie Li.

Electronic supplementary material

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bao, G., Suetsugu, K., Wang, H. et al. Effects of the hemiparasitic plant Pedicularis kansuensis on plant community structure in a degraded grassland. Ecol Res 30, 507–515 (2015). https://doi.org/10.1007/s11284-015-1248-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-015-1248-4

Keywords

Navigation