Strong host specificity of a root hemi-parasite (Santalum acuminatum) limits its local distribution: beggars can be choosers
Santalum acuminatum (quandong) is a root hemi-parasite with a very wide distribution across southern Australia. Despite its very wide distribution, along the Jurien Bay chronosequence, it only occurs on the young Quindalup dunes, and it is absent on older dunes. The soils and local vegetation community change across the 10 km chronosequence, with higher species diversity correlated with lower soil phosphorus (P) levels. Here, we aimed to test whether the distribution of quandong on the dune systems can be explained by different neighbours (potential hosts) or different soil P concentrations across the chronosequence.
Quandongs were grown in pots with 18 potential hosts for a year at three P levels, reflecting conditions across the chronosequence. Hemi-parasite growth and neighbour response were measured through the assessment of biomass, root mass ratios, haustorial size and frequency, δ15N and δ13C isotope signatures, as well as amino acid composition of xylem sap.
Effects of neighbour species on the growth of quandongs were stronger when they were paired with Acacia saligna than when grown with other legumes and non-legumes, indicating strong host specificity. Quandong growth with all other species was significantly less than when grown with A. saligna or without a host, indicating strong competition with a conspecific neighbour. Soil P concentration had little effect on quandong growth.
Host specificity and competition from non-hosts comprise main drivers for the distribution of quandong across the Jurien Bay chronosequence, rather than soil P availability. Our results show the importance of host specificity and how it may restrict the distribution of hemi-parasitic plants in different plant communities along a steep ecological gradient.
KeywordsHaustoria Plant hemi-parasite Parasite-host interactions Parasite ecology Quandong Root hemi-parasite Santalum acuminatum Santalaceae
We thank Walter and Adelphe King for providing us with quandong seeds from their property in York, as well as Nancy Scade for plants used in our experiments. We also thank Calum Irvine for assistance in setting up the experiment, and Jia Leng Tee, Yi Ting Lee, Daniel Beeck, and Azrul Azmi for their assistance in the glasshouse. We also acknowledge Craig Liddicoat for providing the continent-wide pH dataset and map. The authors acknowledge use of the Australian Microscopy & Microanalysis Research Facility at the Centre for Microscopy, Characterisation & Analysis, The University of Western Australia, a facility funded by the University, State and Commonwealth Governments. Finally, we thank the anonymous reviewers for their valuable feedback.
F.N, G.C and H. L. conceived the ideas and designed the study, F.N. carried out the experiments and generated the data. K.R. and L.K. undertook the anatomical studies. G.C. undertook the amino acid analyses. F.N. and H.L. analysed the data, and F.N., H.L., K.R., L.K. and G.C. wrote the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflicts of interest.
- Brand J, Jones P, Donovan O (2004) Current growth rates and predicted yields of sandalwood (Santalum spicatum) grown in plantation in South-Western Australia. Sandalwood Research Newsletter 19:4–7Google Scholar
- Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, BerkeleyGoogle Scholar
- Mwangingo P, Teklehaimanot Z, Lulandala L, Mwihomeke S (2005) Host plants of Osyris lanceolata (African sandalwood) and their influence on its early growth performance in Tanzania: research note. South Afr For J 203:55–65Google Scholar
- Nickrent DL, Musselman LJ (2004) Introduction to parasitic flowering plants. Plant Health Instruc 13:300–315Google Scholar
- Pate J (1995) Mineral relationships of parasites and their hosts. In: Press M, Graves J (eds) Parasitic plants. London, Chapman and Hall, pp 80–102Google Scholar
- Pereira CG, Hayes PE, O'Sullivan OS, Weerasinghe LK, Clode PL, Atkin OL, Lambers H (2019) Trait convergence in photosynthetic nutrient-use efficiency along a 2-million year dune chronosequence in a global biodiversity hotspot. J Ecol. (in press)Google Scholar
- Pinheiro J, Bates D, DebRoy S, Sarkar D (2014) R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1–117. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. Accessed June 2018
- R Core Team (2016) R: a language and environment for statistical computing, ViennaGoogle Scholar
- Rossel RV, Chen C, Grundy M, Searle R, Clifford D, Odgers N, Holmes K, Griffin T, Liddicoat C, Kidd D (2014) Soil and landscape grid national soil attribute maps-pH-CaCl2 (3″ resolution)-release 1. v2Google Scholar
- Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray GR, Millar AH, Day DA, Lambers H (2004) Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiol 135:549–560CrossRefGoogle Scholar
- Shinde S, Ghatge R, Mehetre S (1993) Comparative studies on the growth and development of sandalwood tree in association with different hosts. Indian J For 16:165–166Google Scholar