Parasitism modifies the direct effects of warming on a hemiparasite and its host

Autoři: Nicole E. Rafferty aff001;  Lindsey Agnew aff001;  Paul D. Nabity aff003
Působiště autorů: Department of Evolution, Ecology, and Organismal Biology, University of California, Riverside, California, United States of America aff001;  Rocky Mountain Biological Laboratory, Crested Butte, Colorado, United States of America aff002;  Department of Botany and Plant Sciences, University of California, Riverside, California, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224482


Climate change is affecting interactions among species, including host-parasite interactions. The effects of warming are of particular interest for interactions in which parasite and host physiology are intertwined, such as those between parasitic plants and their hosts. However, little is known about how warming will affect plant parasitic interactions, hindering our ability to predict how host and parasite species will respond to climate change. Here, we test how warming affects aboveground and belowground biomass of a hemiparasitic species (Castilleja sulphurea) and its host (Bouteloua gracilis), asking whether the effects of warming depend on the interaction between these species. We also measured how warming affected the number of haustorial connections between parasite and host. We grew each species alone and together under ambient and warmed conditions. Hosts produced more belowground biomass under warming. However, host biomass was reduced when plants were grown with a hemiparasite. Thus, parasitism negated the benefit of warming on belowground growth of the host. Host resource allocation to roots versus shoots also changed in response to both interaction with the parasite and warming, with hosts producing more root biomass relative to shoot biomass when grown with a parasite and when warmed. As expected, hemiparasite biomass was greater when grown with a host. Warmed parasites had lower root:shoot ratios but only when grown with a host. Under elevated temperatures, hemiparasite aboveground biomass was marginally greater, and plants produced significantly more haustoria. These findings indicate that warming can influence biomass production, both by modifying the interaction between host plants and hemiparasites and by affecting the growth of each species directly. To predict how species will be affected, it is important to understand not only the direct effects of warming but also the indirect effects that are mediated by species interactions. Ultimately, understanding how climate change will affect species interactions is key to understanding how it will affect individual species.

Klíčová slova:

Climate change – Grasses – Host-pathogen interactions – Parasitism – Plants – Seeds – Species interactions – Haustoria


1. Scheffers BR, De Meester L, Bridge TCL, Hoffmann AA, Pandolfi JM, Corlett RT, et al. The broad footprint of climate change from genes to biomes to people. Science. 2016;354: aaf7671. doi: 10.1126/science.aaf7671 27846577

2. Parmesan C, Hanley ME. Plants and climate change: complexities and surprises. Ann Bot. 2015;116: 849–864. doi: 10.1093/aob/mcv169 26555281

3. Alexander JM, Diez JM, Levine JM. Novel competitors shape species responses to climate change. Nature. 2015;525: 515–518. doi: 10.1038/nature14952 26374998

4. Urban MC, Bocedi G, Hendry AP, Mihoub JB, Peer G, Singer A, et al. Improving the forecast for biodiversity under climate change. Science. 2016;353: aad8466. doi: 10.1126/science.aad8466 27609898

5. Gilman SE, Urban MC, Tewksbury JJ, Gilchrist GW, Holt RD. A framework for community interactions under climate change. Trends Ecol Evol. 2010;25: 325–331. doi: 10.1016/j.tree.2010.03.002 20392517

6. Gehman A-LM, Hall RJ, Byers JE. Host and parasite thermal ecology jointly determine the effect of climate warming on epidemic dynamics. Proc Natl Acad Sci. 2018;115: 744–749. doi: 10.1073/pnas.1705067115 29311324

7. Paull SH and Johnson PTJ. Can we predict climate-driven changes to disease dynamics? Applications for theory and management in the face of uncertainty. In: Brodie JF, Post E, Doak DF, editors. Wildlife conservation in a changing climate. Chicago: University of Chicago Press; 2013. pp. 109–128.

8. Phoenix GK, Press MC. Effects of climate change on parasitic plants: The root hemiparasitic Orobanchaceae. Folia Geobot. 2005;40: 205–216. doi: 10.1007/BF02803235

9. Forrest JRK, Chisholm SPM. Direct benefits and indirect costs of warm temperatures for high-elevation populations of a solitary bee. Ecology. 2017;98: 359–369. doi: 10.1002/ecy.1655 27861777

10. Press MC, Phoenix GK. Impacts of parasitic plants on natural communities. New Phytologist. 2005; 737–751. doi: 10.1111/j.1469-8137.2005.01358.x 15869638

11. Cameron DD and Phoenix GK. Ecology of hemiparasitic Orobanchaceae with special reference to their interaction with plant communities. In: Joel DM, Gressel J, Musselman LJ, editors. Parasitic Orobanchaceae: Parasitic mechanisms and control strategies. Berlin: Springer-Verlag; 2013. pp. 505–535.

12. Těšitel J, Plavcová L, Cameron DD. Interactions between hemiparasitic plants and their hosts. Plant Signal Behav. 2014;5: 1072–1076. doi: 10.4161/psb.5.9.12563 20729638

13. Marvier MA. Parasitic plant-host interactions: Plant performance and indirect effects on parasite-feeding herbivores. Ecology. 1996;77: 1398–1409. doi: 10.2307/2265537

14. Adler LS. Host effects on herbivory and pollination in a hemiparasitic plant. Ecology. 2002;83: 2700–2710. doi: 10.2307/3072008

15. Adler LS. Host species affects herbivory, pollination, and reproduction in experiments with parasitic Castilleja. Ecology. 2003;84: 2083–2091. doi: 10.1890/02-0542

16. Haan NL, Bakker JD, Bowers MD. Hemiparasites can transmit indirect effects from their host plants to herbivores. Ecology. 2017;99: 399–410. doi: 10.1002/ecy.2087 29131311

17. Bardgett RD, Smith RS, Shiel RS, Peacock S, Simkin JM, Quirk H, et al. Parasitic plants indirectly regulate below-ground properties in grassland ecosystems. Nature. 2006;439: 969–972. doi: 10.1038/nature04197 16495998

18. Spasojevic MJ, Suding KN. Contrasting effects of hemiparasites on ecosystem processes: can positive litter effects offset the negative effects of parasitism? Oecologia. 2010;165: 193–200. doi: 10.1007/s00442-010-1726-x 20658151

19. Hansen DH. Physiology and microclimate in a hemiparasite Castilleja chromosa (Scrophulariaceae). Am J Bot. 1979;66: 477–484. doi: 10.2307/2442496

20. Nyléhn J, Totland Ø. Effects of temperature and natural disturbance on growth, reproduction, and population density in the alpine annual hemiparasite Euphrasia frigida. Arctic, Antarct Alp Res. 1999;31: 259–263. doi: 10.1080/15230430.1999.12003307

21. Ackerfield J. Flora of Colorado. Fort Worth: Botanical Research Institute of Texas Press; 2015.

22. Pyke GH. Local geographic distributions of bumblebees near Crested Butte, Colorado: competition and community structure. Ecology. 1982; 555–573. Available:

23. Luna T. Propagation protocol for Indian paintbrush (Castilleja species). Native Plants Journal. 2005;6: 62–68.

24. Lawrence BA, Kaye TN. Direct and indirect effects of host plants: Implications for reintroduction of an endangered hemiparasitic plant (Castilleja levisecta). Madroño. 2008;55: 151–158. doi: 10.3120/0024-9637(2008)55[151:DAIEOH]2.0.CO;2

25. IPCC (2018). Summary for Policymakers. In: Global Warming of 1.5°C. An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty [Masson Delmotte, V., P. Zhai, H.-O. P. rtner, D. Roberts, J. Skea, P.R. Shukla, A. Pirani, W. Moufouma-Okia, C. P. an, R. Pidcock, S. Connors, J.B.R. Matthews, Y. Chen, X. Zhou, M.I. Gomis, E. Lonnoy, T. Maycock, M. Tignor, and T. Waterfield (eds.)]. In Press.

26. Temperature data obtained from the billy barr weather station. URL

27. R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL

28. Gray SB, Brady SM. Plant developmental responses to climate change. Dev Biol. 2016;419: 64–77. doi: 10.1016/j.ydbio.2016.07.023 27521050

29. Matthies D. Parasite-host interactions in Castilleja and Orthocarpus. Can J Bot. 1997;75: 1252–1260. doi: 10.1139/b97-839

30. Ducharme LA, Ehleringer JR. Gas exchange, delta C-13, and heterotrophy for Castilleja linariifolia and Orthocarpus tolmiei, facultative root hemiparasites on Artemisia tridentata. Gt Basin Nat. 1996;56: 333–340. Available:

31. Ehleringer JR, Schulze ED, Ziegler H, Lange OL, Farquhar GD, Cowar IR. Xylem-tapping mistletoes: Water or nutrient parasites? Science. 1985;227: 1479–1481. doi: 10.1126/science.227.4693.1479 17777782

32. Ren Y-Q, Guan K-Y, Li A-R, Hu X-J, Zhang L. Host dependence and preference of the root hemiparasite, Pedicularis cephalantha Franch. (Orobanchaceae). Folia Geobot. 2010;45: 443–455. doi: 10.1007/s12224-010-9081-6

33. Heide-Jørgensen HS. Introduction: The parasitic syndrome in higher plants. In: Joel DM, Gressel J, Musselman LJ, editors. Parasitic Orobanchaceae: Parasitic mechanisms and control strategies. Berlin: Springer-Verlag; 2013. pp. 25–56.

34. Gibson CC, Watkinson AR. The host range and selectivity of a parasitic plant: Rhinanthus minor L. Oecologia. 1989;78: 401–406. doi: 10.1007/BF00379116 28312588

35. Yang LH, Rudolf VHW. Phenology, ontogeny and the effects of climate change on the timing of species interactions. 2010;13: 1–10. doi: 10.1111/j.1461-0248.2009.01402.x 19930396

36. Paull SH, Johnson PTJ. Experimental warming drives a seasonal shift in the timing of host-parasite dynamics with consequences for disease risk. Ecol Lett. 2014;17: 445–453. doi: 10.1111/ele.12244 24401007

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2019 Číslo 10