High abundance of non-mycorrhizal plant species in severely phosphorus-impoverished Brazilian campos rupestres
Background and aims
We sought to describe the species and functional composition of Brazilian campos rupestres plant communities on severely nutrient-impoverished white sands, to test hypotheses relating plant communities and physiological adaptations to infertile soils. Based on recently-published information on a south-western Australian dune chronosequence, we hypothesised that campos rupestres plant communities would similarly contain a relatively large proportion of non-mycorrhizal species, because of the phosphorus-(P) impoverished nature of the soils. We also sought to test the hypothesis that many of these non-mycorrhizal species have high leaf manganese (Mn) concentrations as a consequence of carboxylate exudation to mobilise soil P.
We conducted flora surveys and quantified mycorrhizal status and foliar Mn concentrations in field sites with strongly-weathered sandy soils. Rhizosphere carboxylates were collected from glasshouse-grown plants to assess a potential correlation of carboxylates and leaf Mn concentrations.
Soils were depleted of all major plant nutrients. Non-mycorrhizal plants were abundant in most field sites (mean relative cover = 48%). Vellozia species were dominant aboveground; belowground, roots were colonised more by dark septate endophytic fungi than by mycorrhizal fungi. From the field sites, foliar Mn concentrations in non-mycorrhizal species increased with decreasing soil P concentrations, but only when soil Mn concentrations were above a minimum threshold (exchangeable [Mn] above detection limit). Across all species, however, there was no relationship of foliar Mn concentrations with soil P concentrations.
Our hypothesis that white-sand campos rupestres communities contain a relatively large proportion of non-mycorrhizal plants was supported. Comparison with similar ecosystems in south-western Australia suggests that plant communities on severely P-impoverished sandy soils, despite differing evolutionary histories and little overlap in plant families, follow convergent evolutionary paths towards increasing abundance of non-mycorrhizal species.
KeywordsCarboxylates Leaf manganese concentrations Mycorrhizas Non-mycorrhizal plants Sandy soils Vellozia
GZ was supported by a scholarship from the Paul Hasluck Bequest administered by the Kwongan Foundation and was the recipient of an Endeavour Research Award provided by Austraining International. GZ also acknowledges the Plant Ecology Program at Unicamp, for financial support for the field work. HL acknowledges support from a CNPq grant, CAPES PVE 88887.108541/2015-00. We thank the Minas Gerais State Park authority for permission to conduct research in the state parks under their administration. UPLC laboratory analyses were done by Alexandra Sarawaya. Sara Adrian, Paulo Mazzafera and Sandra Maria Carmello-Guerreiro, provided laboratory assistance and facilities for the mycorrhizal analysis of roots; Sara Adrian kindly analysed the roots of Vellozia stenocarpa. Livia Echternacht, Graça Wanderley, Juliana dos Santos, Renato de Mello-Silva, Taciana Barbosa Calvacanti, João Martins do Carmo, Edson Dias da Silva, Suzana Costa, Angela Martins and Gustavo Shimizu provided valuable assistance in species identification, and many people from Unicamp assisted with field work. Topographic data for Fig. 1 are based on data services provided by the OpenTopography Facility with support from the National Science Foundation under NSF Award Numbers 1226353 & 1225810.
- Alcantara S, Mello-Silva R, Teodoro GS, Drequeceler K, Ackerly DD, Oliveira RS (2015) Carbon assimilation and habitat segregation in resurrection plants: a comparison between desiccation- and non-desiccation-tolerant species of Neotropical Velloziaceae (Pandanales). Funct Ecol 29:1499–1512CrossRefGoogle Scholar
- Alves RJV, Kolbek J (1994) Plant species endemism in savanna vegetation on table mountains (campo Rupestre) in Brazil. Vegetatio 113:125–139Google Scholar
- de Campos MCR (2012) Phosphorus-acquisition and phosphorus-conservation mechanisms of plants native to south-western Australia or to Brazilian rupestrian fields. PhD Thesis. School of Plant Biology. The University of Western Australia, PerthGoogle Scholar
- Google Inc (2012) Google earth (version 6.2.1). Google Inc., mountain viewGoogle Scholar
- INMET (2015) Historical Data, station 83538 (1961–2015). Instituto Nacional de Meteorologia, Brasília. http://www.inmet.gov.br/portal/index.php?r=bdmep/bdmep
- Lambers H, Shane MW, Laliberté E, Swarts ND, Teste F, Zemunik G (2014) Plant mineral nutrition. In: Lambers H (ed) Plant life on the sandplains in Southwest Australia, a global biodiversity hotspot. UWA Publishing, CrawleyGoogle Scholar
- Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RDC (2015) Nlme: linear and nonlinear mixed effects models. R package version 3.1-120 ednGoogle Scholar
- R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle 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 135:549–560CrossRefPubMedPubMedCentralGoogle Scholar
- Silveira FAO, Negreiros D, Barbosa NP, Buisson E, Carmo FF, Carstensen DW, Conceição AA, Cornelissen TG, Echternacht L, Fernandes GW, Garcia QS, Guerra TJ, Jacobi CM, Lemos-Filho JP, Le Stradic S, Morellato LPC, Neves FS, Oliveira RS, Schaefer CE, Viana PL, Lambers H (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil 403:129–152CrossRefGoogle Scholar
- Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. Elsevier, New YorkGoogle Scholar
- Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae proceedings of the 1st European symposium on mycorrhizae. INRA, ParisGoogle Scholar
- Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nature plants 1: article number: 15050, 15051–15054Google Scholar