Soil types select for plants with matching nutrient‐acquisition and ‐use traits in hyperdiverse and severely nutrient‐impoverished campos rupestres and cerrado in Central Brazil

Abstract

1. Understanding the mechanisms that underlie the generation of beta-diversity remains a challenge in ecology. Underground plant adaptations to environmental gradients have received relatively little attention.2. We studied plant nutrient-acquisition strategies and nutrient-use efficiency at three stages of pedogenesis in infertile soils from campos rupestres and on less infertile soil from cerrado sensu stricto in Brazil. All soils support very high plant diversity with high species turnover between soil types at small spatial scales (metres). We expected that differences in nutrient-acquisition and -use strategies would be associated with this high species turnover. With severely decreasing phosphorus (P) availability, we expected the effectiveness of arbuscular mycorrhizal (AM) symbioses for plant P acquisition to decrease, and reliance on nonmycorrhizal strategies (NM) to increase, while maintaining efficient nutrient use.3. Concentrations of total soil P and nitrogen (N) were greater in soils in cerrado than in those from campos rupestres, and the more weathered soils from campos rupestres were severely P and N impoverished. The proportion of the root length colonized by AM fungi was 71% in the soils from the cerrado and <1% in the most P-impoverished soil type from campos rupestres. Conversely, the proportion of species with nonmycorrhizal P-acquisition strategies such as rhizosheaths was greater in the most P-impoverished soils. Leaf [P] and [N] were very low and decreased with decreasing soil [P] and [N]. Leaf N:P ratios suggest P limitation of plant productivity in the campos rupestres but N-P colimitation in the cerrado.Photosynthetic rates decreased with increasing P impoverishment, but photosynthetic P-use efficiency was very high and photosynthetic N-use efficiency moderately high on all soils. Most species had very high P-remobilization efficiency during leaf senescence (>70%), but only moderate N-remobilization efficiency (~50%).

Vellozioid roots allow for habitat specialization among rock‐ and soil‐dwelling Velloziaceae in campos rupestres

“…When nutrients, especially nitrogen (N), are available in organic forms (Benites et al, ; Benites, Schaefer, Simas, & Santos, ), dark‐septate fungi, poorly known fungal symbionts with strongly melanized hyphae that colonize roots of plants, can have positive effects on plant growth and nutrient uptake (Berthelot, Chalot, Leyval, & Blaudez, ; Newsham, ). Dark‐septate fungi are important root endophytes in campos rupestres plant species (Abrahão, Costa, Lambers, et al, ; Oliveira et al, ; Zemunik et al, ), but we do not know how strong their association is with species growing on different substrates.…”

“…In harsh geodiverse environments as in the rocky mountaintop, seasonally dry grasslands in Brazil, the campos rupestres (Figure a,b) (Silveira et al, ), species with different plant traits occupy different substrates (Alcantara et al, ; Zappi, Moro, Meagher, & Nic Lughadha, ). For example, species with different below‐ground traits for nutrient acquisition such as specialized roots or mycorrhizal associations occur on contrasting substrates (Abrahão, Costa, Lambers, et al, ).…”

“…In severely phosphorus (P)‐impoverished soils of campos rupestres formed from extremely low P parent material such as quartzite (Porder & Ramachandran, ), the costs of P acquisition are very high (Raven, Lambers, Smith, Shaver, & Westoby, ). This might lead to a trade‐off in plant investment among different P‐acquisition strategies (Abrahão, Costa, Lambers, et al, ; Ryan et al, ). At relatively higher soluble inorganic soil P concentrations, mycorrhizas represent an effective strategy for P uptake, because thin mycorrhizal hyphae incur smaller carbon (C)‐construction costs than root morphological and physiological specializations (e.g.…”

“…Surveys of arbuscular mycorrhizal (AM) fungal spores in soil have revealed a high diversity in campos rupestres (de Carvalho et al, ; Coutinho, Fernandes, Berbara, Valério, & Goto, ). However, the proportion of the root length colonized by these fungi is very low (Abrahão, Costa, Lambers, et al, ; Oliveira et al, ; Zemunik, Lambers, Turner, Laliberté, & Oliveira, ). When nutrients, especially nitrogen (N), are available in organic forms (Benites et al, ; Benites, Schaefer, Simas, & Santos, ), dark‐septate fungi, poorly known fungal symbionts with strongly melanized hyphae that colonize roots of plants, can have positive effects on plant growth and nutrient uptake (Berthelot, Chalot, Leyval, & Blaudez, ; Newsham, ).…”

“…When P is severely limiting, as in campos rupestres , root specializations are more efficient than mycorrhizas (Raven et al, ). Dauciform roots, sand‐binding roots forming rhizosheaths (Abrahão, Costa, Lambers, et al, ; Abrahão, Lambers, Sawaya, Mazzafera, & Oliveira, ; Oliveira et al, ) and the recently described vellozioid roots (Teodoro et al, ) are prevalent in campos rupestres . Rhizosheaths are soil sheaths strongly bound to the roots, associated with long root hairs that increase root–soil contact and mucilage release (Brown, George, Neugebauer, & White, ; North & Nobel, ; Pang, Ryan, Siddique, & Simpson, ), which enhances the uptake of poorly mobile P (Brown et al, ; Kidd et al, ; McCully, ; Zhang et al, ).…”