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Plant function and evolutionary biology
RESEARCH ARTICLE

A native parasitic plant affects the performance of an introduced host regardless of environmental variation across field sites

Robert M. Cirocco A C , José M. Facelli A and Jennifer R. Watling A B
+ Author Affiliations
- Author Affiliations

A Benham Building DP 312, School of Biological Sciences, The University of Adelaide, SA 5005, Australia.

B All Saints Building, Manchester Metropolitan University, Manchester, M15 6BH, UK.

C Corresponding author. Email: robert.cirocco@adelaide.edu.au

Functional Plant Biology 45(11) 1128-1137 https://doi.org/10.1071/FP17358
Submitted: 20 December 2017  Accepted: 24 May 2018   Published: 27 June 2018

Abstract

Increasing evidence from glasshouse studies shows that native hemiparasitic plants can significantly impact the performance and growth of introduced host plants. We investigated the effect of the native Australian hemiparasite Cassytha pubescens R.Br. on the introduced shrub Ulex europaeus L. at three field sites in South Australia. Parasite infection significantly decreased midday PSII efficiency (ΦPSII) and the maximum electron transport rates (ETRmax) of U. europaeus across sites. The impact of C. pubescens on the photosynthetic performance of U. europaeus may have been caused by infected plants having significantly lower N and K, but higher Fe and Al than uninfected plants at all sites. Significant Al and Fe enrichment in infected plants may be possibly due to the parasite indirectly inducing rhizosphere acidification. At two sites, C. pubescens significantly affected host Fv/Fm, indicating chronic photoinhibition in response to infection. The impact of infection on Fv/Fm was greatest at the wettest site, in line with an experiment where C. pubescens had more impact under high water availability. At this site, infected plants also had the highest foliar Fe and Al. The C isotope (δ13C) of infected plants was significantly lower than that of uninfected plants at only one site. Unusually, the δ13C of the parasite was the same as or significantly higher than that of the hosts. There were no site effects on parasite Fv/Fm or ΦPSII; however, ETRmax and δ13C varied across sites. The results suggest that this native parasite has negative effects on U. europaeus in the field, as was found for glasshouse studies. The abundance of this introduced weed in Australia could be negatively affected by C. pubescens infection.

Additional keywords: carbon isotopes, Cassytha pubescens, nitrogen nutrition, photosynthesis, quantum yield, water potential.


References

Armstrong DM, Croft SJ, Foulkes JN (2003) ‘A biological survey of the Southern Mount Lofty Ranges South Australia.’ (Department for Environment and Heritage: Adelaide)

Bannister P, Strong GL (2001) Carbon and nitrogen isotope ratios, nitrogen content and heterotrophy in New Zealand mistletoes. Oecologia 126, 10–20.
Carbon and nitrogen isotope ratios, nitrogen content and heterotrophy in New Zealand mistletoes.Crossref | GoogleScholarGoogle 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.
Parasitic plants indirectly regulate below-ground properties in grassland ecosystems.Crossref | GoogleScholarGoogle Scholar |

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

Cameron DD, Seel WE (2007) Functional anatomy of haustoria formed by Rhinanthus minor: linking evidence from histology and isotope tracing. New Phytologist 174, 412–419.
Functional anatomy of haustoria formed by Rhinanthus minor: linking evidence from histology and isotope tracing.Crossref | GoogleScholarGoogle 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. Annals of Botany 98, 1289–1299.
Differential resistance among host and non-host species underlies the variable success of the hemi-parasitic plant Rhinanthus minor.Crossref | GoogleScholarGoogle Scholar |

Cechin I, Press MC (1993) Nitrogen relations of the sorghum–Striga hermonthica host–parasite association: growth and photosynthesis. Plant, Cell & Environment 16, 237–247.
Nitrogen relations of the sorghum–Striga hermonthica host–parasite association: growth and photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Cechin I, Press MC (1994) Influence of nitrogen on growth and photosynthesis of a C3 cereal, Oryza sativa, infected with the root hemiparasite Striga hermonthica. Journal of Experimental Botany 45, 925–930.
Influence of nitrogen on growth and photosynthesis of a C3 cereal, Oryza sativa, infected with the root hemiparasite Striga hermonthica.Crossref | GoogleScholarGoogle Scholar |

Cernusak LA, Pate JS, Farquhar GD (2004) Oxygen and carbon isotope composition of parasitic plants and their hosts in southwestern Australia. Oecologia 139, 199–213.
Oxygen and carbon isotope composition of parasitic plants and their hosts in southwestern Australia.Crossref | GoogleScholarGoogle Scholar |

Cirocco RM, Waterman MJ, Robinson SA, Facelli JM, Watling JR (2015) Native hemiparasite and light effects on photoprotection and photodamage in a native host. Functional Plant Biology 42, 1168–1178.

Cirocco RM, Facelli JM, Watling JR (2016a) Does light influence the relationship between a native stem hemiparasite and a native or introduced host? Annals of Botany 117, 521–531.
Does light influence the relationship between a native stem hemiparasite and a native or introduced host?Crossref | GoogleScholarGoogle Scholar |

Cirocco RM, Facelli JM, Watling JR (2016b) High water availability increases the negative impact of a native hemiparasite on its non-native host. Journal of Experimental Botany 67, 1567–1575.
High water availability increases the negative impact of a native hemiparasite on its non-native host.Crossref | GoogleScholarGoogle Scholar |

Cirocco RM, Facelli JM, Watling JR (2017) Does nitrogen affect the interaction between a native hemiparasite and its native or introduced leguminous hosts? New Phytologist 213, 812–821.
Does nitrogen affect the interaction between a native hemiparasite and its native or introduced leguminous hosts?Crossref | GoogleScholarGoogle Scholar |

Clements DR, Peterson DJ, Prasad R (2001) The biology of Canadian weeds. 112. Ulex europaeus L. Canadian Journal of Plant Science 81, 325–337.
The biology of Canadian weeds. 112. Ulex europaeus L.Crossref | GoogleScholarGoogle Scholar |

Delhaize E, Ryan PR (1995) Aluminium toxicity and tolerance in plants. Plant Physiology 107, 315–321.
Aluminium toxicity and tolerance in plants.Crossref | GoogleScholarGoogle Scholar |

Demey A, De Frenne P, Baeten L, Verstraeten G, Hermy M, Boeckx P, Verheyen K (2015) The effects of hemiparasitic plant removal on community structure and seedling establishment in semi‐natural grasslands. Journal of Vegetation Science 26, 409–420.
The effects of hemiparasitic plant removal on community structure and seedling establishment in semi‐natural grasslands.Crossref | GoogleScholarGoogle Scholar |

Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytologist 172, 11–21.
Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation.Crossref | GoogleScholarGoogle Scholar |

Fogarty G, Facelli JM (1999) Growth and competition of Cytisus scoparius, an invasive shrub, and Australian native shrubs. Plant Ecology 144, 27–35.
Growth and competition of Cytisus scoparius, an invasive shrub, and Australian native shrubs.Crossref | GoogleScholarGoogle Scholar |

Gurney AL, Press MC, Ransom JK (1995) The parasitic angiosperm Striga hermonthica can reduce photosynthesis of its sorghum and maize hosts in the field. Journal of Experimental Botany 46, 1817–1823.
The parasitic angiosperm Striga hermonthica can reduce photosynthesis of its sorghum and maize hosts in the field.Crossref | GoogleScholarGoogle Scholar |

Gurney AL, Taylor A, Mbwaga A, Scholes JD, Press MC (2002) Do maize cultivars demonstrate tolerance to the parasitic weed Striga asiatica? Weed Research 42, 299–306.
Do maize cultivars demonstrate tolerance to the parasitic weed Striga asiatica? Crossref | GoogleScholarGoogle Scholar |

Hartley SE, Green JP, Massey FP, Press MCP, Stewart AJA, John EA (2015) Hemiparasitic plant impacts animal and plant communities across four trophic levels. Ecology 96, 2408–2416.
Hemiparasitic plant impacts animal and plant communities across four trophic levels.Crossref | GoogleScholarGoogle Scholar |

Haynes RJ (1990) Active ion uptake and maintenance of cation–anion balance: a critical examination of their role in regulating rhizosphere pH. Plant and Soil 126, 247–264.
Active ion uptake and maintenance of cation–anion balance: a critical examination of their role in regulating rhizosphere pH.Crossref | GoogleScholarGoogle Scholar |

Hibberd JM, Quick WP, Press MC, Scholes JD (1996) The influence of the parasitic angiosperm Striga gesnerioides on the growth and photosynthesis of its host, Vigna unguiculata. Journal of Experimental Botany 47, 507–512.
The influence of the parasitic angiosperm Striga gesnerioides on the growth and photosynthesis of its host, Vigna unguiculata.Crossref | GoogleScholarGoogle Scholar |

Houmani H, Rabhi M, Abdelly C, Debez A (2015) Implication of rhizosphere acidification in nutrient uptake by plants: cases of potassium (K), phosphorus (P), and iron (Fe). In ‘Crop production and global environmental issues’. (Ed. KR Hakeem) pp. 103–122. (Springer: Cham, Switzerland)

Mauromicale G, Lo Monaco A, Longo AMG (2008) Effect of branched broomrape (Orobanche ramosa) infection on the growth and photosynthesis of tomato. Weed Science 56, 574–581.
Effect of branched broomrape (Orobanche ramosa) infection on the growth and photosynthesis of tomato.Crossref | GoogleScholarGoogle Scholar |

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
Chlorophyll fluorescence – a practical guide.Crossref | GoogleScholarGoogle Scholar |

McLuckie J (1924) Studies in Parasitism. I. A contribution to the physiology of the genus Cassytha, Part 1. Proceedings of the Linnean Society of New South Wales 49, 55–78.

Meinzer FC, Woodruff DR, Shaw DC (2004) Integrated responses of hydraulic architecture, water and carbon relations of western hemlock to dwarf mistletoe infection. Plant, Cell & Environment 27, 937–946.
Integrated responses of hydraulic architecture, water and carbon relations of western hemlock to dwarf mistletoe infection.Crossref | GoogleScholarGoogle Scholar |

Miller AC, Watling JR, Overton IC, Sinclair R (2003) Does water status of Eucalyptus largiflorens (Myrtaceae) affect infection by the mistletoe Amyema miquelii (Loranthaceae)? Functional Plant Biology 30, 1239–1247.
Does water status of Eucalyptus largiflorens (Myrtaceae) affect infection by the mistletoe Amyema miquelii (Loranthaceae)?Crossref | GoogleScholarGoogle Scholar |

Pate JS (1995) Mineral relationships of parasites and their hosts. In ‘Parasitic plants’. (Eds MC Press, JD Graves) pp. 80–102. (Chapman & Hall: London, UK)

Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytologist 166, 737–751.
Impacts of parasitic plants on natural communities.Crossref | GoogleScholarGoogle Scholar |

Prider J, Watling J, Facelli JM (2009) Impacts of a native parasitic plant on an introduced and a native host species: implications for the control of an invasive weed. Annals of Botany 103, 107–115.
Impacts of a native parasitic plant on an introduced and a native host species: implications for the control of an invasive weed.Crossref | GoogleScholarGoogle Scholar |

Quested HM (2008) Parasitic plants – impacts on nutrient cycling. Plant and Soil 311, 269–272.
Parasitic plants – impacts on nutrient cycling.Crossref | GoogleScholarGoogle 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.
An anatomical study of the haustoria of Rhinanthus minor attached to roots of different hosts.Crossref | GoogleScholarGoogle Scholar |

Scalon MC, Wright IJ (2015) A global analysis of water and nitrogen relationships between mistletoes and their hosts: broad‐scale tests of old and enduring hypotheses. Functional Ecology 29, 1114–1124.
A global analysis of water and nitrogen relationships between mistletoes and their hosts: broad‐scale tests of old and enduring hypotheses.Crossref | GoogleScholarGoogle Scholar |

Shen H, Prider JN, Facelli JM, Watling JR (2010) The influence of the hemiparasitic angiosperm Cassytha pubescens on photosynthesis of its host Cytisus scoparius. Functional Plant Biology 37, 14–21.
The influence of the hemiparasitic angiosperm Cassytha pubescens on photosynthesis of its host Cytisus scoparius.Crossref | GoogleScholarGoogle Scholar |

Shen H, Xu S-J, Hong L, Wang Z-M, Ye W-H (2013) Growth but not photosynthesis response of a host plant to infection by a holoparasitic plant depends on nitrogen supply. PLoS One 8, e75555
Growth but not photosynthesis response of a host plant to infection by a holoparasitic plant depends on nitrogen supply.Crossref | GoogleScholarGoogle Scholar |

Těšitel J, Těšitelová T, Fisher JP, Lepš J, Cameron DD (2015) Integrating ecology and physiology of root–hemiparasitic interaction: interactive effects of abiotic resources shape the interplay between parasitism and autotrophy. New Phytologist 205, 350–360.
Integrating ecology and physiology of root–hemiparasitic interaction: interactive effects of abiotic resources shape the interplay between parasitism and autotrophy.Crossref | GoogleScholarGoogle Scholar |

Thorp JR, Lynch R (2000) ‘The determination of Weeds of National Significance.’ (National Weeds Strategy Executive Committee: Launceston, Tas.)

Watling JR, Press MC (2000) Infection with the parasitic angiosperm Striga hermonthica influences the response of the C3 cereal Oryza sativa to elevated CO2. Global Change Biology 6, 919–930.
Infection with the parasitic angiosperm Striga hermonthica influences the response of the C3 cereal Oryza sativa to elevated CO2.Crossref | GoogleScholarGoogle Scholar |

Watson DM (2009) Parasitic plants as facilitators: more Dryad than Dracula? Journal of Ecology 97, 1151–1159.
Parasitic plants as facilitators: more Dryad than Dracula?Crossref | GoogleScholarGoogle Scholar |

Westphal MI, Field SA, Tyre AJ, Paton D, Possingham HP (2003) Effects of landscape pattern on bird species distribution in the Mt Lofty Ranges, South Australia. Landscape Ecology 18, 413–426.
Effects of landscape pattern on bird species distribution in the Mt Lofty Ranges, South Australia.Crossref | GoogleScholarGoogle Scholar |