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Strong host specificity of a root hemi-parasite (Santalum acuminatum) limits its local distribution: beggars can be choosers

  • Francis J. NgeEmail author
  • Kosala Ranathunge
  • Lukasz Kotula
  • Gregory R. Cawthray
  • Hans Lambers
Regular Article

Abstract

Aims

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.

Methods

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.

Results

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.

Conclusion

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.

Keywords

Haustoria Plant hemi-parasite Parasite-host interactions Parasite ecology Quandong Root hemi-parasite Santalum acuminatum Santalaceae 

Notes

Acknowledgements

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.

Author contribution

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.

Supplementary material

11104_2019_3966_MOESM1_ESM.docx (92 kb)
ESM 1 Summary statistics of analyses and supplementary figures. (DOCX 91.6 kb)
11104_2019_3966_MOESM2_ESM.docx (22 kb)
ESM 2 Additional details on supplementary methodology and results. (DOCX 22.4 kb)

References

  1. Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot 97:925–931CrossRefGoogle Scholar
  2. Arruda R, Carvalho LN, Del-Claro K (2006) Host specificity of a Brazilian mistletoe, Struthanthus aff. polyanthus (Loranthaceae), in cerrado tropical savanna. Flora 201:127–134CrossRefGoogle Scholar
  3. 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
  4. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77CrossRefGoogle Scholar
  5. Brundrett MC, Abbott L (1991) Roots of jarrah forest plants. I Mycorrhizal associations of shrubs and herbaceous plants. Aust J Bot 39:445–457CrossRefGoogle Scholar
  6. Calladine A, Pate JS, Dixon KW (2000) Haustorial development and growth benefit to seedlings of the root hemiparasitic tree Nuytsia floribunda (Labill.) r.Br. In association with various hosts. Ann Bot 85:733–740CrossRefGoogle Scholar
  7. 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 98:1289–1299CrossRefGoogle Scholar
  8. Chang M, Lynn DG (1986) The haustorium and the chemistry of host recognition in parasitic angiosperms. J Chem Ecol 12:561–579CrossRefGoogle Scholar
  9. Davidson NJ, True KC, Pate JS (1989) Water relations of the parasite: host relationship between the mistletoe Amyema linophyllum (Fenzl) Tieghem and Casuarina obesa Miq. Oecologia 80:321–330CrossRefGoogle Scholar
  10. de Buen LL, Ornelas JF (2002) Host compatibility of the cloud forest mistletoe Psittacanthus schiedeanus (Loranthaceae) in Central Veracruz, Mexico. Am J Bot 89:95–102CrossRefGoogle Scholar
  11. Der JP, Nickrent DL (2008) A molecular phylogeny of Santalaceae (Santalales). Syst Bot 33:107–116CrossRefGoogle Scholar
  12. Ehleringer J, Schulze E-D, Ziegler H, Lange O, Farquhar G, Cowar I (1985) Xylem-tapping mistletoes: water or nutrient parasites? Science 227:1479–1481CrossRefGoogle Scholar
  13. Estabrook EM, Yoder JI (1998) Plant-plant communications: rhizosphere signaling between parasitic angiosperms and their hosts. Plant Physiol 116:1–7CrossRefGoogle Scholar
  14. Fadini RF (2011) Non-overlap of hosts used by three congeneric and sympatric loranthaceous mistletoe species in an Amazonian savanna: host generalization to extreme specialization. Acta Bot Bras 25:337–345CrossRefGoogle Scholar
  15. Hayes P, Turner BL, Lambers H, Laliberté E (2014) Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J Ecol 102:396–410CrossRefGoogle Scholar
  16. Hayes PE, Guilherme Pereira C, Clode PL, Lambers H (2018) Calcium-enhanced phosphorus toxicity in calcifuge and soil-indifferent Proteaceae along the Jurien Bay chronosequence. New Phytol 221:764–777CrossRefGoogle Scholar
  17. Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant Soil 322:49–86CrossRefGoogle Scholar
  18. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefGoogle Scholar
  19. Klaren CH, Van de Dijk SJ (1976) Water relations of the hemiparasite Rhinanthus serotinus before and after attachment. Physiol Plant 38:121–125CrossRefGoogle Scholar
  20. Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, BerkeleyGoogle Scholar
  21. Laliberté E, Turner BL, Costes T, Pearse SJ, Wyrwoll KH, Zemunik G, Lambers H (2012) Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the South-Western Australia biodiversity hotspot. J Ecol 100:631–642CrossRefGoogle Scholar
  22. Laliberté E, Zemunik G, Turner BL (2014) Environmental filtering explains variation in plant diversity along resource gradients. Science 345:1602–1605CrossRefGoogle Scholar
  23. Lamont B, Southall K (1982) Distribution of mineral nutrients between the mistletoe, Amyema preissii and its host, Acacia acuminata. Ann Bot 49:721–725CrossRefGoogle Scholar
  24. Loveys B, Jusaitis M (1994) Stimulation of germination of quandong (Santalum acuminatum) and other Australian native plant seeds. Aust J Bot 42:565–574CrossRefGoogle Scholar
  25. Loveys BR, Tyerman SD, Loveys BR (2002) Effect of different host plants on the growth of the root hemiparasite Santalum acuminatum (quandong). Aust J Exp Agric 42:97–102CrossRefGoogle Scholar
  26. Lu J, Xu D, Kang L, He X (2014) Host-species-dependent physiological characteristics of hemiparasite Santalum album in association with N2-fixing and non-N2-fixing hosts native to southern China. Tree Physiol 34:1006–1017CrossRefGoogle Scholar
  27. Matthies D (1995) Parasitic and competitive interactions between the hemiparasites Rhinanthus serotinus and Odontites rubra and their host Medicago sativa. J Ecol 83:245–251CrossRefGoogle Scholar
  28. Matthies D (1996) Interactions between the root hemiparasite Melampyrum arvense and mixtures of host plants: heterotrophic benefit and parasite-mediated competition. Oikos 75:118–124CrossRefGoogle Scholar
  29. Matthies D (1998) Influence of the host on growth and biomass allocation in the two facultative root hemiparasites Odontites vulgaris and Euphrasia minima. Flora 193:187–193CrossRefGoogle Scholar
  30. Matthies D (2017) Interactions between a root hemiparasite and 27 different hosts: growth, biomass allocation and plant architecture. Perspect Plant Ecol Evol Syst 24:118–137CrossRefGoogle Scholar
  31. Mescher MC, Runyon J, De Moraes CM (2006) Plant host finding by parasitic plants: a new perspective on plant to plant communication. Plant Signal Behav 1:284–286CrossRefGoogle Scholar
  32. 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
  33. Nichols D, Beardsell D (1981) Interactions of calcium, nitrogen and potassium with phosphorus on the symptoms of toxicity in Grevillea cv.‘Poorinda firebird’. Plant Soil 61:437–445CrossRefGoogle Scholar
  34. Nickrent DL, Musselman LJ (2004) Introduction to parasitic flowering plants. Plant Health Instruc 13:300–315Google Scholar
  35. Nickrent DL, Duff RJ, Colwell AE, Wolfe AD, Young ND, Steiner KE (1998) Molecular phylogenetic and evolutionary studies of parasitic plants. In 'Molecular systematics of plants II.' (Eds D Soltis, P Soltis, J Doyle) pp. 211–241. Springer: BostonCrossRefGoogle Scholar
  36. Norton DA, Carpenter MA (1998) Mistletoes as parasites: host specificity and speciation. Trends Ecol Evol 13:101–105CrossRefGoogle Scholar
  37. Norton D, De Lange P (1999) Host specificity in parasitic mistletoes (Loranthaceae) in New Zealand. Funct Ecol 13:552–559CrossRefGoogle Scholar
  38. Okubamichael DY, Griffiths ME, Ward D (2016) Host specificity in parasitic plants—perspectives from mistletoes. AoB Plants 8:plw069CrossRefGoogle Scholar
  39. Ouyang Y, Zhang X, Chen Y, Da Silva JAT, Ma G (2016) Growth, photosynthesis and haustorial development of semiparasitic Santalum album L. penetrating into roots of three hosts: a comparative study. Trees 30:317–328CrossRefGoogle Scholar
  40. 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
  41. Pennings SC, Simpson JC (2008) Like herbivores, parasitic plants are limited by host nitrogen content. Plant Ecol 196:245–250CrossRefGoogle Scholar
  42. 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
  43. Phoenix G, Press M (2005) Linking physiological traits to impacts on community structure and function: the role of root hemiparasitic Orobanchaceae (ex-Scrophulariaceae). J Ecol 93:67–78CrossRefGoogle Scholar
  44. 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
  45. Png GK, Turner BL, Albornoz FE, Hayes PE, Lambers H, Laliberté E (2017) Greater root phosphatase activity in nitrogen-fixing rhizobial but not actinorhizal plants with declining phosphorus availability. J Ecol 105:1246–1255CrossRefGoogle Scholar
  46. R Core Team (2016) R: a language and environment for statistical computing, ViennaGoogle Scholar
  47. Radomiljac AM (1998) The influence of pot host species, seedling age and supplementary nursery nutrition on Santalum album Linn. (Indian sandalwood) plantation establishment within the Ord River irrigation area, Western Australia. For Ecol Manag 102:193–201CrossRefGoogle Scholar
  48. Radomiljac AM, McComb JA, Pate JS, Tennakoon KU (1998) Xylem transfer of organic solutes in Santalum album L. (Indian sandalwood) in association with legume and non-legume hosts. Ann Bot 82:675–682CrossRefGoogle Scholar
  49. Radomiljac AM, McComb JA, McGrath JF (1999) Intermediate host influences on the root hemi-parasite Santalum album L. biomass partitioning. For Ecol Manag 113:143–153CrossRefGoogle Scholar
  50. Rao L (1942) Parasitism in the Santalaceae. Ann Bot 6:131–150CrossRefGoogle Scholar
  51. 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
  52. Rowntree JK, Fisher Barham D, Stewart AJ, Hartley SE (2014) The effect of multiple host species on a keystone parasitic plant and its aphid herbivores. Funct Ecol 28:829–836CrossRefGoogle Scholar
  53. 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 202:194–200CrossRefGoogle Scholar
  54. Schulze E-D, Ehleringer J (1984) The effect of nitrogen supply on growth and water-use efficiency of xylem-tapping mistletoes. Planta 162:268–275CrossRefGoogle Scholar
  55. Seel W, Press M (1993) Influence of the host on three sub-Arctic annual facultative root hemiparasites. New Phytol 125:131–138CrossRefGoogle Scholar
  56. Shah N, Smirnoff N, Stewart G (1987) Photosynthesis and stomatal characteristics of Striga hermonthica in relation to its parasitic habit. Physiol Plant 69:699–703CrossRefGoogle Scholar
  57. 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
  58. Shen H, Ye W, Hong L, Huang H, Wang Z, Deng X, Yang Q, Xu Z (2006) Progress in parasitic plant biology: host selection and nutrient transfer. Plant Biol 8:175–185CrossRefGoogle Scholar
  59. 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
  60. Skrzypek G (2013) Normalization procedures and reference material selection in stable HCNOS isotope analyses: an overview. Anal Bioanal Chem 405:2815–2823CrossRefGoogle Scholar
  61. 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 170:69–78CrossRefGoogle Scholar
  62. Tennakoon K, Pate J, Arthur D (1997a) Ecophysiological aspects of the woody root hemiparasite Santalum acuminatum (R. Br.) a.DC and its common hosts in South Western Australia. Ann Bot 80:245–256CrossRefGoogle Scholar
  63. Tennakoon KU, Pate JS, Stewart GR (1997b) Haustorium-related uptake and metabolism of host xylem solutes by the root hemiparasitic shrub Santalum acuminatum (R. Br.) a. DC.(Santalaceae). Ann Bot 80:257–264CrossRefGoogle Scholar
  64. Turner BL, Hayes PE, Laliberté E (2018) A climosequence of chronosequences in southwestern Australia. Eur J Soil Sci 69:69–85CrossRefGoogle Scholar
  65. Watson DM (2008) Determinants of parasitic plant distribution: the role of host quality. Botany 87:16–21CrossRefGoogle Scholar
  66. Werth CR, Riopel JL (1979) A study of the host range of Aureolaria pedicularia (L.) Raf. (Scrophulariaceae). Am Midl Nat 102:300–306CrossRefGoogle Scholar
  67. Westwood JH, Yoder JI, Timko MP (2010) The evolution of parasitism in plants. Trends Plant Sci 15:227–235CrossRefGoogle Scholar
  68. Yokota T, Sakai H, Okuno K, Yoneyama K, Takeuchi Y (1998) Alectrol and orobanchol, germination stimulants for Orobanche minor, from its host red clover. Phytochemistry 49:1967–1973CrossRefGoogle Scholar
  69. Yoneyama K, Awad AA, Xie X, Yoneyama K, Takeuchi Y (2010) Strigolactones as germination stimulants for root parasitic plants. Plant Cell Physiol 51:1095–1103CrossRefGoogle Scholar
  70. Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nature Plants 1:1–4CrossRefGoogle Scholar
  71. Zemunik G, Turner BL, Lambers H, Laliberté E (2016) Increasing plant species diversity and extreme species turnover accompany declining soil fertility along a long-term chronosequence in a biodiversity hotspot. J Ecol 104:792–805CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of Western AustraliaCrawleyAustralia
  2. 2.School of Biological Sciences, Faculty of ScienceThe University of AdelaideAdelaideAustralia
  3. 3.School of Agriculture and EnvironmentUniversity of Western AustraliaCrawleyAustralia

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