Capture of mammal excreta by Nepenthes is an effective heterotrophic nutrition strategy.

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.

Evolution of endemism on a young tropical mountain.

Tropical mountains are hot spots of biodiversity and endemism, but the evolutionary origins of their unique biotas are poorly understood. 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 is debated whether mountain endemics mostly originate from local lowland taxa, or from lineages that reach the mountain by long-range dispersal from cool localities elsewhere. Here we investigate the evolutionary routes to endemism by sampling an entire tropical mountain biota on the 4,095-metre-high Mount Kinabalu in Sabah, East Malaysia. We discover that most of its unique biodiversity is younger than the mountain itself (6 million years), and comprises a mix of immigrant pre-adapted lineages and descendants from local lowland ancestors, although substantial shifts from lower to higher vegetation zones in this latter group were rare. These insights could improve forecasts of the likelihood of extinction and 'evolutionary rescue' in montane biodiversity hot spots under climate change scenarios.

Bacterial community diversity in the rhizosphere of nickel hyperaccumulator plant species from Borneo Island (Malaysia).

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.

Evolution of wood anatomical characters in Nepenthes and close relatives of Caryophyllales.

Background and Aims: Nepenthes 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.

Nickel stocks and fluxes in a tropical agromining 'metal crop' farming system in Sabah (Malaysia).

Nickel hyperaccumulator plants play a major role in nickel recycling in ultramafic ecosystems, and under agromining the nickel dynamics in the farming system will be affected by removal of nickel-rich biomass. We investigated the biogeochemical cycling of nickel as well as key nutrients in an agromining operation that uses the metal crop Phyllanthus rufuschaneyi in the first tropical metal farm located in Borneo (Sabah, Malaysia). For two years, this study monitored nine 25-m2 plots and collected information on weather, biomass exportation, water, and litter fluxes to the soil. Without harvesting, nickel inputs and outputs had only minor contributions (<1 %) to the total nickel budget in this system. The nickel cycle was mainly driven by internal fluxes, particularly plant uptake, litterfall and throughfall. After two years of cropping, the nickel litter flux corresponded to 50 % of the total nickel stock in the aerial biomass (3.1 g m-2 year-1). Nickel was slowly released from the litter; after 15 months of degradation, 60 % of the initial biomass and the initial nickel quantities were still present in the organic layer. Calcium, phosphorus and potassium budgets in the system were negative without fertilisation. Unlike what is observed for nickel, sustained agromining would thus lead to a strong depletion of calcium stocks if mineral weathering cannot replenish it.

Phyllanthus rufuschaneyi: a new nickel hyperaccumulator from Sabah (Borneo Island) with potential for tropical agromining.

BACKGROUND: Nickel hyperaccumulator plants are of much interest for their evolution and unique ecophysiology, and also for potential applications in agromining-a novel technology that uses plants to extract valuable metals from soil. The majority of nickel hyperaccumulators are known from ultramafic soils in tropical regions (Cuba, New Caledonia and Southeast Asia), and one genus, Phyllanthus (Phyllanthaceae), is globally the most represented taxonomic entity. A number of tropical Phyllanthus-species have the potential to be used as 'metal crops' in agromining operations mainly because of their ease in cultivation and their ability to attain high nickel concentrations and biomass yields. RESULTS: One of the most promising species globally for agromining, is the here newly described species Phyllanthus rufuschaneyi. This species can be classified in subgenus Gomphidium on account of its staminate nectar disc and pistillate entire style and represents the most western species of this diverse group. The flower structure indicates that this species is probably pollinated by Epicephala moths. CONCLUSIONS: Phyllanthus rufuschaneyi is an extremely rare taxon in the wild, restricted to Lompoyou Hill near Kinabalu Park in Sabah, Malaysia. Its utilization in agromining will be a mechanism for conservation of the taxon, and highlights the importance of habitat and germplasm preservation if rare species are to be used in novel green technologies.