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Background and aims While isotopic enrichment of nitrogen (15N) and carbon (13C) is often used to determine whether carnivorous plant species capture and assimilate nutrients from supplemental sources such as invertebrate prey or mammal excreta (heterotrophic nutrition), little is known about how successful the different strategies deployed by carnivorous plants are at obtaining supplemental nutrition. The collection of mammalian faeces by Nepenthes (tropical pitcher plants) is the result of a highly specialized biological mutualism that results in heterotrophic nitrogen gain; however, it remains unknown how effective this strategy is in comparison to Nepenthes species not known to collect mammalian faeces. Methods We examined how isotopic enrichment varied in the diverse genus Nepenthes, among species producing pitchers for invertebrate capture and species exhibiting mutualisms for the collection of mammal excreta. Enrichment factors were calculated from δ15N and δ13C values from eight Nepenthes species and naturally occurring hybrids along with co-occurring reference (non-carnivorous) plants from three mountain massifs in Borneo: Mount Kinabalu, Mount Tambuyukon and Mount Trus Madi. Results All Nepenthes examined, except N. edwardsiana, were significantly enriched in 15N compared to co-occurring non-carnivorous plants, and 15N enrichment was more than two-fold higher in species with adaptations for the collection of mammal excreta compared with other Nepenthes. Conclusions The collection of mammal faeces clearly represents a highly effective strategy for heterotrophic nitrogen gain in Nepenthes. Species with adaptations for capturing mammal excreta occur exclusively at high elevation (i.e. are typically summit-occurring) where previous studies suggest invertebrate prey are less abundant and less frequently captured. As such, we propose this strategy may maximize nutritional return by specializing towards ensuring the collection and retention of few but higher-value N sources in environments where invertebrate prey may be scarce.

Background and aims: Phosphorus is one of the major nutrients that directly or indirectly affects all aspects of plant growth. Tropical nickel hyperaccumulators, including Phyllanthus rufuschaneyi and Rinorea cf. bengalensis from Borneo Island (in the Malaysian state of Sabah), have evolved to grow in extremely P-impoverished ultramafic soils. This study aimed to establish the response of the root and shoot ionome of these two agromining ‘metal crops’ to soil P availability. Methods: We undertook a soil P dosing trial on P. rufuschaneyi and R. cf. bengalensis in Sabah (Malaysia) over a period of 12 months. We measured the elemental concentrations in the soil solution and roots, as well as in the developed and developing stems and leaves. Results: The results show that root and shoot P accumulation increased markedly as soil P availability increased by 80-fold in P. rufuschaneyi, whereas R. cf. bengalensis did not increase as strongly to P supply, despite a 135-fold increase in soil solution P. The contrasting observations on the root and shoot P accumulation patterns in these species suggests distinct P acquisition strategies in these species. The non-responsiveness of R. cf. bengalensis to increasing soil P availability may be related to its possible association with mycorrhizal fungi. Conclusion: The findings of this study reveal the complexities of phosphate uptake, transport and accumulation in these ‘metal crops’. This information is essential to develop appropriate nutrient management in nickel agromining operations.

International audience; Background and Aims: In tropical ultramafic soils, potassium (K) is typically the most growth limiting nutrient. However, tropical nickel (Ni) hyperaccumulator plants, including Phyllanthus rufuschaneyi and Rinorea cf. bengalensis (which are ‘metal crops’ used in agromining) from Malaysia, have unusually high K shoot accumulation compared to other species, despite naturally growing on severely K-impoverished ultramafic soils. This study aimed to establish the response to soil K availability in relation to uptake of K and other elements in the roots and shoots of P. rufuschaneyi and R. cf. bengalensis.Methodology: We undertook an experiment in which soluble K was dosed to ultramafic soil in pots with P. rufuschaneyi and R. cf. bengalensis in Sabah (Malaysia).Results: The results show that root K concentrations increased markedly as the soil K availability increased by 35-fold, whilst the corresponding effect on K accumulation in the shoots of P. rufuschaneyi and R. cf. bengalensis was not significantly different in relation to soil K dosing. Observed divergent responses between root and shoot K accumulation in these species suggests a separate genetic control of K uptake and xylem loading in P. rufuschaneyi and R. cf. bengalensis.Conclusion: The tight control of root-to-shoot K translocation and constrained K accumulation in shoots under a soil K gradient is likely an adaptive mechanism to the evolution of these species to grow in highly nutrient-impoverished ultramafic soils. This study provides information that will be useful for better nutrient management of tropical Ni metal farms that use K-efficient Ni ‘metal crops’.

The extend of biogeochemical cycling of nickel (Ni) by tropical hyperaccumulator plants in their native habitat is largely unknown, although these unusual plants are suspected to play a major role in the recycling of this element in ultramafic ecosystems. In this study, we have assessed the biogeochemical cycling of Ni (and other elements, including mineral nutrients) by a tropical Ni hyperaccumulator plant, i.e., Phyllanthus rufuschaneyi, which is one of the most promising species for tropical Ni agromining. The study site was a young secondary forest in Sabah (Malaysia) where Phyllanthus rufuschaneyi occurs as the dominant species on an ultramafic Cambisol. For 2 years, we monitored a 100-m2 plot and collected information on weather, biomass increase, soil fertility, water fluxes to the soil and litter fluxes for a wide range of elements, including Ni. The Ni cycle is mainly driven by internal fluxes, notably the degradation and recycling of Ni-rich litter. Over the period of investigation, the Ni litter flux corresponded to the total Ni stock of the litter (5.2 g m−2 year−1). The results further show that Ni turnover varies significantly with the accumulation properties of the plant cover. This points to the major influence of Ni hyperaccumulator plants in building up Ni available stocks in the topsoils, as has also been shown in temperate ultramafic systems. Litterfall and throughfall contribute substantially to the cycling of phosphorus, sulphur and potassium in this ecosystem, with throughfall contributing 2-, 220- and 20-fold higher to the respective nutrient fluxes relative to litterfall. The magnesium:calcium ratio far exceeded 1 in the soil, but was < 1 in the leaves of Phyllanthus rufuschaneyi. The insights from this study should be taken into account when designing tropical agromining operations; as Ni stocks could be more labile than initially thought. The removal of Ni- and nutrients-rich biomass will likely affect available Ni (and major nutrients) for the next cropping seasons, and requires sustainable fertilisation, to be utilized to replenish depleted major nutrients. These findings also have major ecological implications.

International audience; Ultramafic soils are usually marginal in macronutrients (nitrogen (N), phosphorus (P), potassium (K) and calcium (Ca)) for growth of crop plants. Commercial nickel (Ni) agromining is dependent on attaining high yield and high Ni concentration in harvestable biomass of Ni hyperaccumulator species. We previously reported on the biomass responses of two promising tropical ‘metal crops’ (Phyllanthus rufuschaneyi and Rinorea cf. bengalensis) to rates of N, P, and K fertilisers. Calcium, sulphur (S) and organic matter amendments have varied effects on the biomass production and Ni uptake in temperate Ni hyperaccumulator species used in agromining, but the trends in tropical ‘metal crops’ are not reported to-date. We investigated the effects of these amendments on the growth performance and the Ni (and other elements) uptake in P. rufuschaneyi and R. cf. bengalensis The experiments consisted of a large 12-month randomised growth trial in large pots in Sabah (Malaysia) using ultramafic soils under different treatment levels of soluble Ca and S, and organic matter amendments. We found that Ca and S additions had no significant effects on the growth of P. rufuschaneyi and R. cf. bengalensis. Organic matter amendments had strong positive effect on the growth of R. cf. bengalensis (p

International audience; Background and aims: Pioneer plants may improve the ecological restoration of degraded ultramafic areas by plant-soil interaction processes. In this study, we assess the effect of the pioneer actinorhizal tree C. terminale (Casuarinaceae) on the recovery of plant communities and soil functions on degraded tropical ultramafic sites.Methods: Soil and plant samples were collected along a tree-age gradient in two degraded ultramafic sites in Sabah (Northern Borneo, Malaysia): a Technosol and a Leptosol. Chemical composition of plants and soils, and biological activity of soils were assessed at both sites. Plant colonisation was assessed by plot vegetation surveys.Results: An improvement in soil fertility parameters (pH reduction from 8.5 to 6.8, an increase in the concentrations of several nutrients and enhanced soil enzyme activities) was observed along the C. terminale age gradient. However, plant cover and diversity was only improved around mature trees at the site that was not impacted by mining.Conclusion: C. terminale promotes the recovery of several soil functions, mainly related to the storage and recycling of N, P, K, S. Besides plant-soil feedback, other environmental factors (i.e. exposition to sunlight, drought) may play an important role on revegetation of ultramafic soils.

International audience; Aims: The agronomy of tropical ‘metal crops’ had not yet been tested until a recent pot trial was undertaken to test the growth and nickel (Ni) yield of two promising Ni ‘metal crops’ (Phyllanthus rufuschaneyi and Rinorea cf. bengalensis) from Sabah, Malaysia. The present study investigates the growth and Ni yield in P. rufuschaneyi in response to inorganic and organic fertilisation under field conditions.Methods: A two-year field experiment was undertaken on an ultramafic Cambisol in Sabah. Two experiments were set up with different types of fertilisers, either organic or inorganic. Ten 9-m2 plots were amended with either NPK (370 kg ha−1) or N (120 kg ha−1) fertilisation and were monitored during the first year. Another experiment with 25-m2 plots was set up to test three treatments of organic amendment (0, 1 or 2 kg m−2 of shredded P. rufuschaneyi biomass).Results: The results show that despite considerable variability, Ni concentration was generally lower in plant shoots amended with N only (i.e. urea). However, treatments showed no statistical effect on plant biomass and Ni yield in the short-term, even though organic treatments had a strong positive effect on the availability of Ni.Conclusion: The short-term effects of inorganic and organic treatments on Ni yield of the tropical ‘metal crop’ Phyllanthus rufuschaneyi were not apparent (75 kg Ni ha−1 yr−1). The field trials are ongoing to assess long-term effects. The preliminary results suggest that with appropriate agronomic systems and plant breeding, the Ni yield could be substantially increased.

The Island of Borneo is a major biodiversity hotspot, and in the Malaysian state of Sabah, ultramafic soils are extensive and home to more than 31 endemic nickel hyperaccumulator plants. The aim of this study was to characterize the structure and the diversity of the rhizosphere bacterial communities of several of these nickel hyperaccumulator plants and factors that affect these bacterial communities in Sabah. The most abundant phyla were Proteobacteria, Acidobacteria and Actinobacteria. At family level, Burkholderiaceae and Xanthobacteraceae (Proteobacteria phylum) were the most abundant families in the hyperaccumulator rhizospheres. Redundancy analysis based on soil chemical analyses and relative abundances of the major bacterial phyla showed that abiotic factors of the studied sites drove the bacterial diversity. For all R. aff. bengalensis rhizosphere soil samples, irrespective of studied site, the bacterial diversity was similar. Moreover, the Saprospiraceae family showed a high representativeness in the R. aff. bengalensis rhizosphere soils and was linked with the nickel availability in soils. The ability of R. aff. bengalensis to concentrate nickel in its rhizosphere appears to be the major factor driving the rhizobacterial community diversity unlike for other hyperaccumulator species.

Plant and soil 455, 289 ��� 303 (2020). doi:10.1007/s11104-020-04629-7, $Aims$Knowledge on the ecophysiology of cobalt hyperaccumulator species is limited. The nickel hyperaccumulator Rinorea cf. bengalensis from Borneo can accumulate high concentrations of cobalt in nature. This study investigates the cobalt accumulation potential of Rinorea cf. bengalensis in relation to nickel concentrations in soils and the subsequent tissue and cellular-level distributions of cobalt, nickel and major cations.$Methods$Seedlings of Rinorea cf. bengalensis were grown in mixed treatments on ultramafic soil containing a high concentration of available nickel. Cobalt and nickel salts were then added to the soil to study their interactions. The tissue and cellular-level distributions of cobalt, calcium, nickel, and potassium were investigated using synchrotron-based X-ray fluorescence microscopy.$Results$The maximum foliar cobalt concentration reached 1200 ��g g$^{���1}$. Accumulation of cobalt competed with nickel accumulation although nickel seems to stimulate cobalt phloem translocation. Plants suffered toxicity in the treatment with the highest soil cobalt concentration. Cobalt and nickel have contrasting distribution patterns in the leaves of Rinorea cf. bengalensis, with cobalt mainly excreted on the surface of the leaves, whereas nickel is localised in foliar epidermal cells.$Conclusions$Rinorea cf. bengalensis can accumulate high concentrations of cobalt, but is intrinsically more tolerant to nickel. It does not rely on a similar sequestration mechanism for both metals, which could explain the lesser tolerance for cobalt. Nickel appears to be essential for the plant to tolerate high cobalt concentrations. Further studies intending to develop agronomic practices are needed to determine the viability of Rinorea cf. bengalensis for nickel-cobalt agromining., Published by Springer Science + Business Media B.V, Dordrecht [u.a.]

International audience; AimsThis study investigated the physico-geochemical properties of three types of ultramafic substrates in Sabah (Malaysia) and further characterised their influence on nickel (Ni) accumulation in two selected tropical ‘metal crops’ (Phyllanthus rufuschaneyi and Rinorea cf. bengalensis).MethodsThree experiments, consisting of a randomised block growth trial in large pots over 12 months in Sabah, were conducted: i) soil ratio experiment (Cambisol:Ferralsol:Leptosol), ii) soluble Ni dosing experiment with added 0, 60, 240, 600 mg Ni kg−1, and iii) soil pH adjustments (pH 5.2, 5.8 and 6.4) experiment.ResultsThe results show that the low pH status of Ferralsol did not result in increased extractable Ni concentrations, indicating that Ni-bearing phases and mineralogy play a major role in Ni extractability in these substrates. The increasing order of extractable Ni concentrations was Ferralsol < Leptosol < Cambisol. The selected ‘metal crops’ had remarkable shoot biomass (~40 g pot−1) and foliar Ni concentrations (>15 g kg−1 in P. rufuschaneyi) in the Cambisol, >5-fold higher relative to that recorded in Leptosol and Ferralsol. Mixing the Cambisol with the other substrates significantly improved Ni yield in both species relative to the individual substrates. The effect of Ni addition on the selected ‘metal crops’ was species-dependent, whereas reduction of soil pH in Cambisol significantly reduced Ni yield in both species.ConclusionsNickel accumulation patterns in ‘metal crops’ in response to the diverse ultramafic soils in the tropics are influenced by the physico-geochemical characteristics of the soil types. Soil Ni extractability in these soils is more dependent on the Ni-bearing phases and mineralogy rather than the pH status. This study provides useful information on plant-soil interactions required for identifying suitable substrates for implementing tropical Ni agromining.

International audience; Agromining is an emerging technology that utilizes selected ‘metal crops' (= hyperaccumulator plants) to extract valuable target metals from unconventional resources for profit from mineralised soils. Growth characteristics, shoot metal concentrations, and agrominable locations are important considerations in economic agromining. Globally, the greatest potential for nickel (Ni) agromining exists in the tropics. However, the agronomic systems of tropical ‘metal crops' have not been previously tested. Furthermore, it is currently unknown whether nutrient dosing of prospective tropical agromining Ni ‘metal crops’ could possibly cause a shoot Ni‐dilution effect which may ultimately limit economically viable Ni yields. We undertook a pioneering study on Ni uptake and growth responses to nutrient dosing in two promising tropical ‘metal crops' (Phyllanthus rufuschaneyi and Rinorea cf. bengalensis). The experiment consisted of a large randomised block growth trial in large pots over 12 months in Sabah (Malaysia). At 3‐month intervals, the plants were exposed to soluble treatments that altered available concentrations of nitrogen (N), phosphorus (P), and potassium (K). We found strong positive growth responses to N and P additions in P. rufuschaneyi, whereas K additions had negative growth effects. In R. cf. bengalensis, all treatments had positive growth effects. The increases in biomass in response to nutrient dosing did not significantly reduce shoot Ni concentrations in both species, with the exception of N addition in P. rufuschaneyi. This study reveals that Ni uptake and growth responses to nutrient dosing are species‐dependent, primarily influenced by the ecophysiology of the species. Inorganic fertilization could possibly be an important component of the management of local ‘metal crops' to be used in viable commercial agromining in the tropics, but this needs to be tested in the field with different formulations of N, P, and K.

International audience; Surface mining or other disturbing operations on ultramafic outcrops degrade soil conditions and decrease major ecosystem functions in those habitats. Human disturbances exacerbate the harsh conditions of some ultramafic soils, making recovery more difficult. Recovery of ecosystem functions of disturbed areas may vary from passive to active reclamation measures, depending on the starting situation, available resources and expected outcomes. In this study, three treatments (topsoil application, topsoil + non-compacted, and topsoil + non-compacted + organic amendment), representing a gradient of increasing reclamation effort, were tested for the reclamation of a tropical ultramafic Spolic Technosol in Sabah (Malaysia). Soil treatments were tested at the mesocosm-scale for 12 months, and drainage water fluxes, evolution of soil physicochemical parameters, soil microbial activities and spontaneous plant colonisation, diversity and growth were monitored along the duration of the experiment. The results show that application of topsoil improved the plant biomass and water filtration functions in the non-reclaimed sites, with no additional benefit from lesser compaction. The most intensive treatment (topsoil + non-compacted + organic amendment) gave the best improvements in nutrient cycling and biomass production functions, but with a reduction of water filtration function, due to an increase in soluble concentrations and cumulative fluxes of nickel. Introduced species were dominant in the vegetation colonising the mesocosms, and therefore planting of selected native species will be necessary to create habitats for native biodiversity. This information will be useful to select a strategy for the recovery of degraded tropical serpentinite quarries and dump sites.

Localized ultramafic outcrops in Kinabalu Park (encompassing Mount Kinabalu and Mount Tambuyukon) in Sabah (Malaysia) are known for high levels of plant diversity and endemism, which have been stimulated by extreme soil chemistry and biogeographic factors, such as isolation. Characteristic of these outcrops are edaphic endemics of insectivorous pitcher plants from the Nepenthaceae-family including Nepenthes burbidgeae, N. edwardsiana, N. macrovulgaris, N. rajah and N. villosa, all of which (except N. macrovulgaris) are confined solely to the protected area of Kinabalu Park. Although the various aspects of plant taxonomy and nutrition of this genus have been extensively studied, the habitat of these rare species has to date not been studied in detail. It was hypothesized that while the Nepenthes of Mount Kinabalu and Mount Tambuyukon are excluders of excess trace elements, soil chemistry is nevertheless a major driver for creating the specific habitats in which ultramafic edaphic endemic Nepenthes occur, and that this is reflected in vegetation physiognomy and co-occurring species composition as well as in the foliar chemistry of Nepenthes. The results show that the characteristics of the physical environment and soil chemistry ‘induces’ a vegetation physiognomy that varies among sites and produces a series of different niches that are colonised by different Nepenthes-species. Although other plant species associated with these niches do not directly influence the distributions of the Nepenthes-species, some are characteristic. The unusual ultramafic soil chemistry is not reflected in the foliar chemistry of Nepenthes and they appear to be ‘Excluders’ of potentially toxic soil trace element concentrations. The populations of Nepenthes burbidgeae, N. edwardsiana, N, rajah, N. villosa are small (in particular, N. burbidgeae) and these species are thus likely to be vulnerable to the potential effects of climate change-induced drought and fire.

Background and AimsNepenthes attracts wide attention with its spectacularly shaped carnivorous pitchers, cultural value and horticultural curiosity. Despite the plant’s iconic fascination, surprisingly little anatomical detail is known about the genus beyond its modified leaf tip traps. Here, the wood anatomical diversity of Nepenthes is explored. This diversity is further assessed with a phylogenetic framework to investigate whether the wood characters within the genus are relevant from an evolutionary or ecological perspective, or rather depend on differences in developmental stages, growth habits, substrates or precipitation. Methods Observations were performed using light microscopy and scanning electron microscopy. Ancestral states of selected wood and pith characters were reconstructed using an existing molecular phylogeny for Nepenthes and a broader Caryophyllales framework. Pairwise comparisons were assessed for possible relationships between wood anatomy and developmental stages, growth habits, substrates and ecology. Key Results Wood anatomy of Nepenthes is diffuse porous, with mainly solitary vessels showing simple, bordered perforation plates and alternate intervessel pits, fibres with distinctly bordered pits (occasionally septate), apotracheal axial parenchyma and co-occurring uni- and multiseriate rays often including silica bodies. Precipitation and growth habit (stem length) are linked with vessel density and multiseriate ray height, while soil type correlates with vessel diameter, vessel element length and maximum ray width. For Caryophyllales as a whole, silica grains, successive cambia and bordered perforation plates are the result of convergent evolution. Peculiar helical sculpturing patterns within various cell types occur uniquely within the insectivorous clade of non-core Caryophyllales. Conclusions The wood anatomical variation in Nepenthes displays variation for some characters dependent on soil type, precipitation and stem length, but is largely conservative. The helical-banded fibre-sclereids that mainly occur idioblastically in pith and cortex are synapomorphic for Nepenthes, while other typical Nepenthes characters evolved convergently in different Caryophyllales lineages. This is a pre-copyedited, author-produced version of an article accepted for publication in nnals of Botany following peer review. The version of record is available online at: https://doi.org/10.1093/aob/mcx010

Tropical mountains are hot spots of biodiversity and endemism,but the evolutionary origins of their unique biotas are poorlyunderstood. In varying degrees, local and regional extinction,long-distance colonization, and local recruitment may all contribute to the exceptional character of these communities. Also, it isdebated whether mountain endemics mostly originate from locallowland taxa, or from lineages that reach the mountain by long-range dispersal from cool localities elsewhere. Here we investigatethe evolutionary routes to endemism by sampling an entire tropical mountain biota on the 4,095-metre-high Mount Kinabalu inSabah, East Malaysia. We discover that most of its unique biodiversity is younger than the mountain itself (6 million years), andcomprises a mix of immigrant pre-adapted lineages and descendants from local lowland ancestors, although substantial shiftsfrom lower to higher vegetation zones in this latter group wererare. These insights could improve forecasts of the likelihood ofextinction and ‘evolutionary rescue in montane biodiversity hotspots under climate change scenarios.

Sabah (Malaysia) has one of the largest surface expressions of ultramafic rocks on Earth and in parallel hosts one of the most species-rich floras. Despite the extensive knowledge of the botanical diversity and the chemistry of these substrates, until recently the records for nickel (Ni) hyperaccumulator plants in the area have been scant. Recent intensive screening has resulted in 19 new records, adding to the 5 previously known from Sabah. The results of this study indicate that most Ni hyperaccumulator plants in Sabah are restricted to successional habitats (ridges, river banks, secondary vegetation) at elevations