Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot Lambers, H., Ahmedi, I., Berkowitz, O., Dunne, C., Finnegan, P., Hardy, G. E. S. J., ... Teste, F. (2013). Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot. Conservation Physiology, 1(1), 21pp. DOI: 10.1093/conphys/cot010 Published in: Conservation Physiology DOI: 10.1093/conphys/cot010 Document Version Publisher's PDF, also known as Version of record Link to publication in the UWA Research Repository General rights Copyright owners retain the copyright for their material stored in the UWA Research Repository. The University grants no end-user rights beyond those which are provided by the Australian Copyright Act 1968. Users may make use of the material in the Repository providing due attribution is given and the use is in accordance with the Copyright Act 1968. Take down policy If you believe this document infringes copyright, raise a complaint by contacting [email protected]. The document will be immediately withdrawn from public access while the complaint is being investigated. Download date: 25. Jun. 2017 UWA Research Publication Lambers, H., Ahmedi, I., Berkowitz, O., Dunne, C., Finnegan, P., Hardy, G. E. S. J., ... Teste, F. (2013). Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot. Conservation Physiology, 1(1), 21pp. © The Author 2013. Published by Oxford University Press on behalf of The Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted distribution and reproduction in any medium, provided the original work is properly cited. This is the final published version of the article accepted for publication in Conservation Physiology, following peer review. The definitive published version (see citation above) is located on the article abstract page of the publisher, Oxford University Press. This version was made available in the UWA Research Repository on 11th November 2014 in compliance with the publisher’s policies on archiving in institutional repositories. Volume 1 • 2013 10.1093/conphys/cot010 Review Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot Downloaded from Hans Lambers1,*, Idriss Ahmedi1,2, Oliver Berkowitz1,2, Chris Dunne1,3, Patrick M. Finnegan1, Giles E. St J. Hardy2, Ricarda Jost1, Etienne Laliberté1, Stuart J. Pearse1,4 and François P. Teste1 1School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia http://conphys.oxfordjournals.org/ 2Centre for Phytophthora Science and Management, School of Biological Sciences and Biotechnology, Murdoch University, Murdoch, WA 6150, Australia 3Science Division, Department of Environment and Conservation, Locked Bag 104, Bentley Delivery Centre, WA 6983, Australia 4Astron Environmental Services, 129 Royal Street, East Perth, WA 6004, Australia; *Corresponding author: School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia. Tel: + 08 6488 7381. Email: [email protected] South-western Australia harbours a global biodiversity hotspot on the world’s most phosphorus (P)-impoverished soils. The at The University of Western Australia on November 9, 2014 greatest biodiversity occurs on the most severely nutrient-impoverished soils, where non-mycorrhizal species are a prominent component of the flora. Mycorrhizal species dominate where soils contain slightly more phosphorus. In addition to habitat loss and dryland salinity, a major threat to plant biodiversity in this region is eutrophication due to enrichment with P. Many plant species in the south-western Australian biodiversity hotspot are extremely sensitive to P, due to a low capability to down-regulate their phosphate-uptake capacity. Species from the most P-impoverished soils are also very poor competitors at higher P availability, giving way to more competitive species when soil P concentrations are increased. Sources of increased soil P concentrations include increased fire frequency, run-off from agricultural land, and urban activities. Another P source is the P-fertilizing effect of spraying natural environments on a landscape scale with phosphite to reduce the impacts of the introduced plant pathogen Phytophthora cinnamomi, which itself is a serious threat to biodiversity. We argue that alternatives to phosphite for P. cinnamomi management are needed urgently, and propose a strategy to work towards such alternatives, based on a sound understanding of the physiological and molecular mechanisms of the action of phosphite in plants that are susceptible to P. cinnamomi. The threats we describe for the south-western Australian biodiversity hotspot are likely to be very similar for other P-impoverished environments, including the fynbos in South Africa and the cerrado in Brazil. Key words: Cluster roots, eutrophication, non-mycorrhizal plants, phosphite, Phytophthora cinnamomi, Proteaceae Editor: Lawren Sack Received 23 January 2013; Revised 5 April 2013; Accepted 17 April 2013 Conserv. Physiol. (2013) 1: doi: 10.1093/conphys/cot010 Introduction Myers, 2001; Hopper and Gioia, 2004). Due to the old age of the Australian continent, the relative stability of its geol- South-western Australia harbours a global biodiversity ogy, and the fact that most of Australia was last glaciated hotspot, where exceptional numbers of endemic species are over 250 million years ago and has been above sea level for undergoing exceptional loss of habitat (Myers et al., 2000; 145 million years (Miller et al., 2005), many Australian soils © The Author 2013. Published by Oxford University Press on behalf of The Society for Experimental Biology. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted distribution and reproduction in any medium, provided the original work is properly cited. Review Conservation Physiology • Volume 1 2013 are severely nutrient impoverished, and are especially low in Adaptations to extremely phosphorus (P; Beadle, 1953). The most extremely phosphorus-impoverished soils P-impoverished soils occur in the region of the south-western biodiversity hotspot (Lambers et al., 2010, 2012; Laliberté A plant family that is richly represented on severely et al., 2012; Fig. 1). P-impoverished soils in south-western Australia and similar landscapes in South Africa is the Proteaceae (Cowling and In Western Australia’s biodiversity hotspot, the greatest Lamont, 1998). Proteaceae species occur as major ecosystem plant diversity is found on the most severely P-impoverished, components, often as keystone species. They are evergreen sandy soils (Lamont et al., 1977; Lambers et al., 2010; woody plants, ranging in size from prostrate shrubs to trees Fig. 2). A similar pattern of increasing plant diversity with (Cavanagh and Pieroni, 2006; Collins et al., 2008). After lower soil P status has been found for nutrient-poor habitats fires, Proteaceae species regenerate either by sprouting epi- in Royal National Park, in New South Wales, in eastern cormic shoots or by releasing seed from woody follicles Australia, one of the first sites in the world set aside to (Lamont and Markey, 1995). Proteaceae species contribute Downloaded from become a national park in 1879 (Adam et al., 1989; Le prominently to ecosystem functioning, such as fixation of Brocque and Buckney, 2003). This increase in plant diversity carbon, provision of an architectural structure or habitat, with lower soil fertility most probably reflects a global pat- and sharing and recycling of resources to minimize net nutri- tern (Huston, 1994; Grime, 2002; Wardle et al., 2004; ent loss, especially, from the system (Shearer et al., 2009, Laliberté et al., 2013). For example, several long-term soil 2012). Flowers provide food for birds, mammals, and insects chronosequences worldwide show increases in local plant http://conphys.oxfordjournals.org/ (Hopper, 1980; Whelan and Burbidge, 1980; Ladd et al., species richness with soil age, which is associated with lower 1996; Cavanagh and Pieroni, 2006; Collins, 2008). soil [P] (Wardle et al., 2008; Laliberté et al., 2013). These patterns raise the possibility that P limitation per se might Most of the species in the Proteaceae family produce pro- promote the coexistence of plant species (Olde Venterink, teoid roots (Purnell, 1960) and almost all of them are non- 2011). This may be related to the fact that P occurs in soil in mycorrhizal (Shane and Lambers, 2005a). An exception is many chemical forms and that several different P-acquisition the cluster-rooted mycorrhizal species Hakea verrucosa, strategies exist that can target specific forms (Lambers et al., which grows on ultramafic rocks that are rich in nickel 2006, 2008). (Boulet and Lambers, 2005). The release of carboxylic acids from its cluster roots would increase the solubility of nickel One important P-acquisition strategy is the symbiotic and harm the plants; in addition, mycorrhizal associations at The University of Western Australia on November 9, 2014 association with mycorrhizal fungi, which can enhance