Phyllanthus rufuschaneyi: a new nickel hyperaccumulator from Sabah (Borneo Island) with potential for tropical agromining
© The Author(s) 2018
Received: 10 January 2018
Accepted: 17 March 2018
Published: 27 March 2018
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.
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.
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.
Whereas the great majority of plants growing on naturally nickel (Ni) rich ultramafic soils exclude it from uptake and translocation, a minority of plants display a highly unusual response with enhanced uptake and transfer to the shoots (Reeves 2003; Van der Ent et al. 2013a). These plants are called ‘hyperaccumulators’ and they have the ability to accumulate trace elements to extreme concentrations in their living tissues (Jaffré et al. 1976; Van der Ent et al. 2013a). The Ni concentrations in some species can reach up to 16.9 Wt% in the phloem sap (Van der Ent and Mulligan 2015). Although there are over 400 known Ni hyperaccumulators species (> 0.1 Wt% shoot dry weight), there are just ca. 50 hypernickelophores (e.g. hyperaccumulator species with > 1 Wt% Ni shoot dry weight) known globally (Reeves 2003; Reeves et al. 2017). Hyperaccumulator plants can be used as ‘metal crops’ in agromining (phytomining) operations to generate metal-rich biomass for commercial gain (Chaney et al. 1998; Van der Ent et al. 2015a). This innovative approach enables access to resources not accessible by conventional mining techniques such as abundant low-grade sources of valuable elements (Li et al. 2003; Van der Ent et al. 2015a). Agromining can also benefit local communities, by providing new income opportunities for farmers in developing countries (Bani et al. 2015; Chaney et al. 2018). The greatest potential for agromining is in tropical regions (Cuba, New Caledonia and Southeast Asia) where some of the world’s largest low-grade nickel sources are located (Van der Ent et al. 2013b).
On a global scale, Ni hyperaccumulation occurs most frequently in the order Malpighiales, particularly in the families Dichapetalaceae, Phyllanthaceae, Salicaceae and Violaceae.
The Phyllanthaceae has the greatest numbers of hyperaccumulators with representatives in the genera Actephila Blume, Antidesma L., Breynia J.R.Forst. & G.Forst., Cleistanthus Hook.f. ex Planch., Glochidion J.R.Forst. & G.Forst. and Phyllanthus L. The latter is pantropical and the most speciose genus of the family with over 800 species globally (Govaerts et al. 2000; Kathriarachchi et al. 2006; Bouman et al. under review). Due to its great diversity in morphology, Phyllanthus is currently classified in many subgenera and (sub)sections, which were often former separate genera. The genus is characterized by its unisexual flowers, the absence of petals and a characteristic branching system called phyllanthoid branching (see Fig. 2a; Webster 1956). Species with this particular type of branching have deciduous, plagiotropic branchlets that are subtended by reduced scale-like leaves (cataphylls) (Webster 1956). Normal leaves and flowers are only found on the plagiotropic branchlets. This branching system has been lost several times (Kathriarachchi et al. 2006) and in species with non-phyllanthoid branching, leaves can be found on all axes and the branchlets are not deciduous and subtended by normal leaves. The genus Phyllanthus is currently paraphyletic with the genera Breynia, Glochidion and Synostemon F.Muell. nested within (Kathriarachchi et al. 2006; Pruesapan et al. 2012). Discussions on how to resolve the paraphyly of the genus Phyllanthus are still ongoing (see Hoffmann et al. 2006; Van Welzen et al. 2014). One of the most speciose subgenera is subgenus Gomphidium (Baill.) G.L.Webster. Species in the subgenus are characterised by phyllanthoid branching in combination with flowers with biseriate sepals, stamens with free filaments (but connate in one section) and three duplex nectar glands (sometimes divided and then 6 or absent). The phylogenetic position of subgenus Gomphidium was not consistent between the markers used in the study of Kathriarachchi et al. (2006) and requires further study.
Major centres of diversity for Phyllanthus are in New Caledonia with over 100 species of which 15 species are Ni hyperaccumulators (Kersten et al. 1979; Schmid 1991; Jaffré et al. 2013), in Cuba with at least 40 species of which 17 species are Ni hyperaccumulators (Leon and Alain 1953; Reeves et al 1996), and in the Malesian Region about 100 species of which 5 species are Ni hyperaccumulators (Van der Ent et al. 2015a, b, c; Wu et al. 2016; Galey et al. 2017).
A number of taxa in the genus Phyllanthus are among the most promising ‘metal crops’ due to their fast growth and other favourable growth characteristics, including easy propagation and pest resistance (Nkrumah et al. 2016). Some Phyllanthus-species also reach some of the highest Ni concentrations known in any hyperaccumulator plants, with 3.8 Wt% in the leaves of P. serpentinus S.Moore from New Caledonia (Jaffré 1977; Kersten et al. 1979; as P. favieri M.Schmid), 3.9 Wt% in the leaves of Phyllanthus insulae-japen Airy Shaw from Indonesia (Reeves 2003), and 6 Wt% in the leaves P. × pallidus C.Wright ex Griseb. from Cuba (Reeves et al. 1996).
Further study of other genera within the Phyllanthaceae continues to yield new Ni hyperaccumulator records, such as in the genus Antidesma (Nkrumah et al. 2018), and even new species that are hyperaccumulators, such as the recently described Actephila alanbakeri Welzen & Ent (Van der Ent et al. 2016a). Kinabalu Park is the world’s most species-rich hotspot with over 5000 species in 1000 genera and 200 families recorded to date (Beaman and Beaman 1990; Beaman 2005) of which 2542 plant species have been found on the ultramafic soils inside the Park (Van der Ent et al. 2015c). In Sabah, a total of 8 species of Phyllanthus occur, of which two are known Ni hyperaccumulators: P. balgooyi Petra Hoffm. & A.J.M.Baker which can accumulate up to 1.6 Wt% Ni in the leaves and up to 16.9 Wt% Ni in the phloem sap and the here newly described Phyllanthus rufuschaneyi (Hoffmann et al. 2008; Van der Ent and Mulligan 2015; Mesjasz-Przybylowicz et al. 2016). Phyllanthus balgooyi, also occurs in the Philippines, in addition to Phyllanthus securinegioides Merr. (which can accumulate up to 3.5 Wt% in the leaves), and a third Ni hyperaccumulator species from the genus, P. erythrotrichus C.B.Rob. which can accumulate up to 1.1 Wt% Ni in the leaves (Baker et al. 1992; Quimado et al. 2015). The extreme levels of Ni accumulation in these species poses important questions about the ways in which these plants take up, transport and store Ni, while avoiding the potential effects of metabolic toxicity. In leaves, Ni appears to be associated mainly with organic acids, such as citrate, malate and malonate (Kersten et al. 1980; Homer 1991; Montargès-Pelletier et al. 2008; Van der Ent et al. 2017).
The material studied comprised of herbarium specimens loaned from the Sabah Parks Herbarium (SNP) in Sabah, Malaysia. Descriptions were made using standard taxonomical techniques and morphological terminology follows Beentje (2016).
The IUCN conservation status was assessed applying the IUCN Red List Categories (IUCN 2001) that considers (i) extent of occurrence (EOO), and (ii) area of occurrence (AOO) in order to generate applicable IUCN threat categories.
Collection of plant samples for chemical analysis
Plant tissue samples (leaves, wood, bark, flowers) for bulk chemical analysis were collected in the habitat (6°06′29.6″N 116°47′36.7″E) near Kinabalu Park in Sabah, Malaysia. These samples were dried at 70 °C for 5 days in a drying oven and subsequently packed for transport to Australia and gamma irradiated at Steritech Pty. Ltd. in Brisbane following Quarantine Regulations in Australia. The dried plant tissue samples were subsequently ground and digested using 4 mL HNO3 (70%) and 1 mL H2O2 (30%) in a microwave oven (Milestone Start D) for a 45-min programme and diluted to 30 mL with ultrapure water (Millipore 18.2 MΩ cm at 25 °C) before analysis with ICP-AES (Varian Vista Pro II) (Huang et al. 2004). The elemental concentrations originate from previously reported data (Van der Ent and Mulligan 2015; Van der Ent et al. 2015b, 2017) augmented with new data from plant tissue samples collected for this study.
This species is most similar to P. securinegoides from the Philippines, from which it can be distinguished by its smaller leaves, staminate flowers with connate filaments and pistillate flowers with connate tubular stigmas.
Shrub to tree(let), up to 6 m high, monoecious, phyllanthoid branching present, main branches often hollow. Indument generally absent, on some parts asperities (stiff, short, papillae-like hairs) on orthotropic and plagiotropic branches and sometimes petioles and pedicels. Plagiotropic branches 1‒1.5 mm wide, not flattened, with 2 narrow longitudinal wings, to 0.3 mm wide, asperities usually present between wings. Stipules ovate, 1.5‒6 by 0.8‒1 mm, persistent, becoming brown when dry, basally eared, ears sometimes elongated. Leaves distichous, simple, dimorphous (reduced on orthotropic branch to cataphylls (scale leaves), not reduced on plagiotropic branches). Cataphylls on main trunk below branches, stipule-like, ovate to triangular, c. 3 mm long, early caducous. Leaves on plagiotropic branches: petiole more or less dorsoventrally flattened, 1‒1.5 mm long, glabrous or with asperities, transversely wrinkled when dry; blade ovate to elliptic, 1.6‒3.7 (without mucro) by 0.5‒1.2 cm, 2.2‒3.7 times longer than wide, coriaceous, base attenuate, asymmetric, margin entire, somewhat thickened, slightly revolute, apex rounded to acuminate, mucronate up to 5.2 mm, mucron usually breaking off, upper and lower surface glabrous, smooth, lower surface glaucous; venation pinnate, above hardly visible, slightly raised underneath, secondary veins 6‒8 per side, looped and closed near margin, higher order veins reticulate. Inflorescences consisting of unisexual or bisexual fascicles, flowers 1‒4 per node; staminate flowers single or a few, generally in lower axils but sometimes at end of branches, usually together with a single pistillate flower; latter also single in upper axils. Staminate flowers 1.4‒2 mm diameter, remaining closed, actinomorphic; pedicel slender, 6.7‒12 mm long, apically somewhat thickened; sepals 6, upright, tightly packed, margin entire, apex rounded; outer three smaller (when young) to slightly longer than inner ones, 1.9‒2 by 0.9‒1 mm, central part thickened, pink, margins and upper half thin, white to whitish pink; inner 3 1.4‒2.3 by 1.3‒1.4 mm, lower part almost nail-like, central midrib area thickened and darker coloured, basal central part inside attached to androphore via a ^-like structure; disc lobes 6, paired, vertical, kidney-like, c. 0.6 mm long, greyish blue when dry, attached to broad part of flower receptacle, smooth; stamens 3, filaments connate, c. 1 mm high, broadly cone-shaped, apically with erect anthers, these elliptic, c. 0.7 by 0.4 mm, opening extrorse via lengthwise slits, apically on connective a c. 0.3 mm long slender appendix. Pistillate flowers 1.4‒1.6 mm diameter, actinomorphic; pedicel 1‒2 mm long, round, glabrous or with asperities; sepals 6, tight to ovary in flower, spreading in fruit, base very thickened, attached to receptacle, margin entire, outer 3 slightly smaller than inner 3, elliptic, 1.7‒2 by c. 1 mm, apex truncate to erose, inner 3 elliptic, c. 2 by 1.2‒1.6 mm, apex rounded; disc lobes 6, small, globose, less than 0.2 mm in diameter; gynophore c. 0.3 mm high, ovary ovoid, c. 1.3 by 1.1‒1.3 mm, 3-locular, 2 ovules per locule, smooth, glabrous, three stigmas united into a cone of 0.8‒1 mm high, apically somewhat erose (slightly split stigmas) and hollow inside. Fruits c. 7.5 mm in diameter, c. 4.5 mm high, opening completely septicidal and partly to completely loculicidal, exocarp separating from meso- and endocarp, wall thin, woody when dry, smooth, glabrous; columella broadly triangular, 2‒2.3 mm high. Seed ovoid-triangular, c. 2.8 by 1.8 mm, brown, smooth, not seen mature.
The specific epithet “rufuschaneyi” honours Dr. Rufus L. Chaney (b. 1942), an agronomist who is widely credited for inventing phytomining (agromining) (Chaney 1983), leading to the technology being patented (Chaney et al. 1998). Dr. Chaney has worked for 47 years at the USDA Agricultural Research Service (USA) on risk assessment for metals in soils and crops, and the food-chain transfer and bioavailability of soil and crop metals to humans. He published over 490 publications and won the Gordon Award for Lifetime Achievement and Excellence in Phytoremediation Research. The fact that P. rufuschaneyi is the most promising tropical Ni ‘metal crop’ presently known, makes this recognition fitting.
Phenology and pollination
The species flowers and fruits all year round. Especially young plants growing in open habitats flower profusely on many branches. Flowering is less frequent when plants grow under more shaded conditions in developing forest. Many Phyllanthus species are pollinated by moths of the genus Epicephala Meyrick. Females of these moths actively pollinate the flowers and then deposit eggs into the floral ovaries, after which the larvae consume some of the developing seeds (Kawakita 2010). Phyllanthus rufuschaneyi, like all other species in subgenus Gomphidium, is likely pollinated by Epicephala moths (Kato and Kawakita 2017) as the staminate flowers are highly closed (inner sepals even grown together with the broad androphore) and possess vertical anthers, the pistillate flowers have grown together, cone-like, non-opening stigmas. Although pollination has not been specifically studied in this species, Epicephala larvae were observed in the fruit capsules of P. rufuschaneyi in the field. The similarity with Glochidion flowers, also pollinated by Epicephala moths, is remarkable. The co-evolution and high specificity for Epicephala-species for Phyllanthus-species has been linked to the extensive diversification of this genus in New Caledonia (Kawakita and Kato 2004).
Distribution, habitat and ecology of Phyllanthus rufuschaneyi
Phyllanthus rufuschaneyi is known only from two populations; one (very small) population at the foot of Bukit Hampuan, and another larger population on Lompoyou Hill approximately 5 km from the first population. The habitat in both localities is open secondary scrub that has been affected by recurring forest fires (Fig. 1). Lompoyou Hill is close to the villages of Nalumad and Pahu. The hill (400 m asl) has been burnt at least once as a result of an uncontrolled forest fire in 1998. Prior to burning, the site was already disturbed by logging. The area has a short and open scrub community (dominated by shrubs 1–3 m tall) with pioneer species such as Macaranga kinabaluensis Airy Shaw (Euphorbiaceae). In this habitat type several other Ni hyperaccumulator plant species occur, including Phyllanthus balgooyi, Actephila alanbakeri, Mischocarpus sundaicus Blume (Sapindaceae), and Xylosma luzonensis Clos (Salicaceae). The local conditions are xeric, and the soils are shallow and heavily eroded with limited amounts of organic matter. In pot experiments P. rufuschaneyi responded negatively to increasing organic matter amendments (Nkrumah et al. 2017). Phyllanthus rufuschaneyi occurs exclusively on these young eroded soils (hypermagnesian Cambisols) that occur at low elevation (700 m asl) on strongly serpentinised bedrock. These soils have extremely high magnesium (Mg) to calcium (Ca), circum-neutral pH, and high available Ni as a result of the disintegration of phyllosilicates and re-sorption onto secondary iron (Fe)-oxides or high-charge clays (Echevarria 2018). In Sabah, Ni hyperaccumulator plant species are restricted to these soils with a pH > 6.3 and relatively high total soil Ni concentrations > 630 μg g−1 (Van der Ent et al. 2016b).
Elemental concentrations in the plant tissues
Elemental concentration (macro elements: Al, Ca, K, Mg, Na, P, S) ranges and means in parentheses
Elemental concentration (trace elements: Co, Cr, Cu, Fe, Mn, Ni, Zn) ranges and means in parentheses
The habitat of P. rufuschaneyi is outside any protected areas, in patches of remaining scrub in an area devastated by recurring forest fires. The restriction of this species to just one main population (the second population is very small) and the small area of occupancy (< 10 km2) means that this species is sensitive to disturbances which could ultimately lead to its extinction. Therefore, the species can be classified as Critically Endangered (CR) on the basis of IUCN Red List Criteria (Version 3.1: IUCN 2001) considering Criterion B. Geographic range; B2. Area of occupancy estimated to be less than 10 km2, and a. Severely fragmented or known to exist at only a single location; b. Continuing decline in (i) extent of occurrence; and (iii) area, extent and/or quality of habitat.
The taxonomic position of P. rufuschaneyi is noteworthy as it represents the most western species of its subgenus. It is placed in Phyllanthus subgenus Gomphidium section Nymania (K.Schum) J.J.Sm. on account of its three paired staminate disc glands and its connate stamens (Fig. 3c). Section Nymania is mainly distributed in Papua New Guinea, but a few species also occur in the Philippines. Phyllanthus rufuschaneyi is most similar to P. securinegioides, however, it differs in its significantly smaller leaves, its smaller fascicled inflorescences with pinkish flowers (Fig. 1a; vs larger fascicles with yellow flowers in P. securinegioides), the completely fused anther filaments (Fig. 3c) and the fused style (Fig. 3e). The other Philippine species of Gomphidium, P. apiculatus Merr., P. ramosii Quisumb., P. glochidioides Elmer and P. cordatulus Rob., all have staminate flowers with free stamens. Though P. cordatulus has a similarly fused style of c. 1.3 mm long, it is spreading for about the same distance, whereas the style of P. rufuschaneyi is only fused for up to 1 mm and slightly erose at the end. The style is quite prominent and emerges out of the pistillate flowers (Fig. 3d, e). The other species of Phyllanthus occurring in Borneo are from other subgenera and differ either in their branching system (e.g. phyllanthoid vs non-phyllanthoid in subgenus Macraea (Wight) Jean F.Brunel) or in the morphology of their flowers (e.g. no difference between inner and outer sepals in subgenera Emblica (Gaertn.) Kurz, Kirganelia (A.Juss.) Kurz and Eriococcus (Hassk.) Croizat & Metcalf). The structure on top of the anther connective is slightly reminiscent of the apiculate anthers in subgenus Phyllanthodendron (Hemsl.) G.L.Webster. However, P. rufuschaneyi does not have the characteristic ligulate nectar disc and apiculate anthers that are also found in subgenus Gomphidium. Nickel hyperaccumulators are found in several subgenera within the genus Phyllanthus, which suggests that it evolved several times.
The restricted distribution of P. rufuschaneyi cannot be easily explained. In Sabah, Ni hyperaccumulators are restricted to circum-neutral soils with relatively high phytoavailable calcium, magnesium and Ni concentrations with at least 20 μg g−1 carboxylic acid extractable Ni or 630 μg g−1 total nickel, and a soil pH > 6.3 (Van der Ent et al. 2016b). However, these types of Cambisols derived from serpentinized bedrock are relatively widespread in Sabah, but P. rufuschaneyi has not been found elsewhere despite extensive fieldwork on all major ultramafic outcrops in Sabah (Van der Ent et al. 2015b). Although some Ni hyperaccumulators are comparatively common (P. balgooyi, Psychotria sarmentosa Blume, Rubiaceae, Xylosma luzonensis) on several ultramafic outcrops in Sabah, the situation of P. rufuschaneyi mirrors that of Actephila alanbakeri, which is also restricted to a single site at the same location (Van der Ent et al. 2016a). Experience in cultivation shows that P. rufuschaneyi is highly shade-intolerant and requires exposed conditions with minimal light competition (Fig. 5). It suffers from fungal infections when grown under shaded and moist conditions, and stops flowering. The dependence on a specific pollinator that is characteristic for the Phyllanthus-Epicephala mutualism and limited dispersal capabilities might be possible explanations why this species is not more widespread in Borneo.
Phyllanthus rufuschaneyi has particularly attractive characteristics for cultivation as ‘metal crop’ in agromining operations. These favourable properties include its multi-stemmed habit, the rapid re-growth after coppicing, and high Ni concentrations in woody parts of the biomass. Other Phyllanthus-species, such as P. balgooyi, albeit having equally high foliar Ni concentrations, have lower growth rates and do not tolerate open and exposed conditions on bare soils. A major uncertainty currently pertains to the effective mass-propagation of P. rufuschaneyi, however, and the specialised pollination strategy of this species presents a challenge for using seed stock.
More than any other species, obligate hyperaccumulator plants that have a restricted distribution on isolated ultramafic outcrops are susceptible to habitat degradation (Galey et al. 2017). Phyllanthus rufuschaneyi is known only from a site that has been severely affected by over-logging and (man-made) forest fires for clearing of agricultural land, and neither the area nor the species has statutory protection. The current expansion of oil palm plantations on Lompoyou Hill cast a further shadow over its continued existence in the wild. As such, the case of P. rufuschaneyi highlights the importance of habitat and germplasm preservation if rare species are to be used in green technologies such as agromining. Therefore, concerted efforts must be made to screen for hyperaccumulator species (Whiting et al. 2004), followed by appropriate methods for conserving them both in and ex situ (Erskine et al. 2012). The utilization of P. rufuschaneyi in agromining operations means that there are now likely to be more plants in cultivation than in the wild, and this will for now safeguard its future survival.
AvdE, PE and GE conducted the fieldwork and collected the plant specimens in Sabah. RB and PvW carried out the taxonomical study. AvdE undertook the laboratory analyses. All authors read and approved the final manuscript.
We thank Rimi Repin, Rositti Karim (Sabah Parks) and Postar Miun (Sabah Forestry Department) for their help during the fieldwork in Malaysia.
The authors declare that they have no competing interests.
Availability of data and materials
Specimens are deposited at the L and SNP herbaria as indicated.
Consent for publication
Ethics approval and consent to participate
The Sabah Biodiversity Council issued research permits for conducting research in Sabah, and Sabah Parks granted permission to conduct research in Kinabalu Park.
The French National Research Agency through the national “Investissements d’ avenir” program (ANR-10-LABX-21, LABEX RESSOURCES21) and through the ANR-14-CE04-0005 Project “Agromine” is acknowledged for funding support to G. Echevarria and A. van der Ent. A. van der Ent is the recipient of a Discovery Early Career Researcher Award (DE160100429) from the Australian Research Council.
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- Baker AJM, Proctor J, van Balgooy MMJ, Reeves RD (1992) Hyperaccumulation of nickel by the flora of the ultramafics of Palawan, Republic of the Philippines. In: Baker AJM, Proctor J, Reeves RD (ed) The vegetation of ultramafic (serpentine) soils. Proceedings of the first international conference on serpentine ecology. Intercept, Andover pp 291–304Google Scholar
- Bani A, Echevarria G, Zhang X, Benizri E, Laubie B, Morel J-L, Simonnot M-O (2015) The effect of plant density in nickel-phytomining field experiments with Alyssum murale in Albania. Aust J Bot 63:72–77Google Scholar
- Beaman JH (2005) Mount Kinabalu: hotspot of plant diversity in Borneo. Biol Skr 55:103–127Google Scholar
- Beaman JH, Beaman RS (1990) Diversity and distribution patterns in the flora of Mount Kinabalu. In: Baas P, Kalkman K, Geesink R (eds) The plant diversity of Malesia. Kluwer Academic Publishers, Dordrecht, pp 147–160View ArticleGoogle Scholar
- Beentje H (2016) The Kew plant glossary: an illustrated dictionary of plant terms. Kew Royal Botanic Gardens, RichmondGoogle Scholar
- Chaney RL (1983) Plant uptake of inorganic waste constituents. In: Parr JF, Marsh PB, Kla JM (eds) Land treatment of hazardous wastes. Noyes Data Corp, Park Ridge, pp 50–76Google Scholar
- Chaney RL, Angle JS, Baker AJM, Li YM (1998) Method for phytomining of nickel, cobalt and other metals from soil. US Patent 5: 711–784, 27 January 1998Google Scholar
- Chaney RL, Baker AJM, Morel JL (2018) The long road to developing agromining/phytomining. In: Van der Ent A, Echevarria G, Baker AJM, Morel JL (eds) Agromining: farming for metals. Mineral resource reviews. Springer, ChamGoogle Scholar
- Echevarria G (2018) Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry. In: Van der Ent A, Echevarria G, Baker AJM, Morel JL (eds) Agromining: farming for metals. Mineral resource reviews. Springer, ChamGoogle Scholar
- Erskine P, van der Ent A, Fletcher A (2012) Sustaining metal-loving plants in mining regions. Science 337:1172–1173View ArticlePubMedGoogle Scholar
- Galey MC, van der Ent A, Iqbal MCM, Rajakaruna N (2017) Ultramafic geoecology of south and southeast asia. Bot Stud 58:18View ArticlePubMedPubMed CentralGoogle Scholar
- Govaerts R, Frodin DG, Radcliffe-Smith A (2000) World checklist and bibliography of Euphorbiaceae (with Pandaceae), vol 4. Royal Botanic Gardens, KewGoogle Scholar
- Hoffmann P, Kathriararachchi H, Wurdack KJ (2006) A phylogenetic classification of Phyllanthaceae (Malpighiales; Euphorbiaceae sensu lato). Kew Bull 61:37–53Google Scholar
- Hoffmann P, Baker AJM, Proctor J, Madulid D (2008) Phyllanthus balgooyi (Euphorbiaceae s.l.), a new nickel-hyperaccumulating species from Palawan and Sabah. Blumea 48:193–199View ArticleGoogle Scholar
- Homer F (1991) Chemical studies on some plants that hyperaccumulate nickel. Ph.D. thesis, Massey University, pp 1–285Google Scholar
- Huang L, Bell RW, Dell B, Woodward J (2004) Rapid nitric acid digestion of plant material with an open-vessel microwave system. Commun Soil Sci Plant Anal 35:427–440View ArticleGoogle Scholar
- IUCN (2001) IUCN red list categories and criteria: version 3.1. IUCN Species Survival Commission, GlandGoogle Scholar
- Jaffré T (1977) Composition chimique élémentaire des tissus foliaires des espèces végétales colonisatrices des anciennes mines de nickel en Nouvelle Calédonie. Cah. O.R.S.T.O.M., sér. Biol. XII: 323–330Google Scholar
- Jaffré T, Brooks RR, Lee J, Reeves RD (1976) Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia. Science 193:579–580View ArticlePubMedGoogle Scholar
- Jaffré T, Pillon Y, Thomine S, Merlot S (2013) The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00279/abstract PubMedPubMed CentralGoogle Scholar
- Kathriarachchi H, Samuel R, Hoffmann P, Mlinarec J, Wurdack KJ, Ralimanana H, Stuessy TF, Chase MW (2006) Phylogenetics of tribe Phyllantheae (Phyllanthaceae; Euphorbiaceae sensu lato) based on nrITS and plastid matK DNA sequence data. Am J Bot 93:637–655View ArticlePubMedGoogle Scholar
- Kato M, Kawakita A (2017) Obligate pollination mutualism, XII edn. Springer, Tokyo, p 309View ArticleGoogle Scholar
- Kawakita A (2010) Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae). Plant Species Biol 25:3–19View ArticleGoogle Scholar
- Kawakita A, Kato M (2004) Evolution of obligate pollination mutualism in New Caledonian Phyllanthus (Euphorbiaceae). Am J Bot 91:410–415View ArticlePubMedGoogle Scholar
- Kersten W, Brooks R, Reeves R, Jaffré T (1979) Nickel uptake by New Caledonian species of Phyllanthus. Taxon 28:529–534View ArticleGoogle Scholar
- Kersten WJ, Brooks RR, Reeves RD, Jaffré A (1980) Nature of nickel complexes in Psychotria douarrei and other nickel-accumulating plants. Phytochemistry 19:1963–1965View ArticleGoogle Scholar
- Leon B, Alain B (1953) Flora de Cuba. III. Euphorbiaceae. Contribuciones Ocasionales del Museo de Historia Natural del Colegio de la Salle 13:44–59Google Scholar
- Li Y-M, Chaney R, Brewer E, Roseberg R, Angle JS, Baker A, Reeves R, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115View ArticleGoogle Scholar
- Mesjasz-Przybylowicz J, Przybylowicz W, Barnabas A, van der Ent A (2016) Extreme nickel hyperaccumulation in the vascular tracts of the tree Phyllanthus balgooyi from Borneo. New Phytol 209:1513–1526View ArticlePubMedGoogle Scholar
- Montargès-Pelletier E, Chardot V, Echevarria G, Michot LJ, Bauer A, Morel J-L (2008) Identification of nickel chelators in three hyperaccumulating plants: an X-ray spectroscopic study. Phytochemistry 69:1695–1709View ArticlePubMedGoogle Scholar
- Nkrumah PN, Baker AJM, Chaney RL, Erskine PD, Echevarria G, Morel J-L, van der Ent A (2016) Current status and challenges in developing nickel phytomining: an agronomic perspective. Plant Soil 406:55–69View ArticleGoogle Scholar
- Nkrumah P, Echevarria G, Erskine, PD, van der Ent A, Sumail S (2017) First growth trial of tropical ‘metal shrubs’ to be used in economic agromining. In: Proceedings of the 9th international conference on Serpentine ecology, 5–9th June 2017. Tirana-Pogradec, Albania, p 169Google Scholar
- Nkrumah P, Echevarria G, Erskine PD, van der Ent A (2018) The discovery of nickel hyper-accumulation in Antidesma montis-silam: from herbarium identification to field re-discovery. Ecol Res. https://doi.org/10.1007/s11284-017-1542-4 Google Scholar
- Pruesapan K, Telford IRH, Bruhl JJ, Van Welzen PC (2012) Phylogeny and proposed circumscription of Breynia, Sauropus and Synostemon (Phyllanthaceae), based on chloroplast and nuclear DNA sequences. Aust Syst Bot 25:313–330View ArticleGoogle Scholar
- Quimado MO, Fernando ES, Trinidad LC, Doronila A (2015) Nickel-hyperaccumulating species of Phyllanthus (Phyllanthaceae) from the Philippines. Aus J Bot 63(2):103–110Google Scholar
- Reeves RD (2003) Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant Soil 249(1):57–65View ArticleGoogle Scholar
- Reeves RD, Baker AJM, Borhidi A, Berazaín R (1996) Nickel-accumulating plants from the ancient serpentine soils of Cuba. New Phytol 133:217–224View ArticleGoogle Scholar
- Reeves RD, Baker AJM, Jaffré T, Erskine PD, Echevarria G, van der Ent A (2017) A global database for hyperaccumulator plants of metal and metalloid trace elements. New Phytol. https://doi.org/10.1111/nph.14907 PubMedGoogle Scholar
- Schmid M (1991) Phyllanthus. In: Morat P, Mackee HS (eds) Flore de la Nouvelle-Calédonie et Dépendances, vol 17. Muséum National d’Histoire Naturelle, Paris, pp 31–320Google Scholar
- Van der Ent A, Mulligan D (2015) Multi-element concentrations in plant parts and fluids of Malaysian nickel hyperaccumulator plants and some economic and ecological considerations. J Chem Ecol 41:396–408View ArticlePubMedGoogle Scholar
- Van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013a) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334View ArticleGoogle Scholar
- Van der Ent A, Baker AJM, van Balgooy MMJ, Tjoa A (2013b) Ultramafic nickel laterites in Indonesia (Sulawesi, Halmahera): mining, nickel hyperaccumulators and opportunities for phytomining. J Geochem Explor 128:72–79View ArticleGoogle Scholar
- Van der Ent A, Mulligan D, Erskine PD (2013c) Discovery of nickel hyperaccumulators from Kinabalu Park, Sabah (Malaysia) for potential utilization in phytomining. In: Enviromine 2013, Santiago, Chile, 4–6 December 2013. pp 213–221Google Scholar
- Van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CWN, Meech JA, Erskine PD, Simonnot M-O, Vaughan J, Morel J-L et al (2015a) Agromining: farming for metals in the future? Environ Sci Technol 49:4773–4780View ArticlePubMedGoogle Scholar
- Van der Ent A, Erskine P, Sumail S (2015b) Ecology of nickel hyperaccumulator plants from ultramafic soils in Sabah (Malaysia). Chemoecology 25:243–259View ArticleGoogle Scholar
- Van der Ent A, Repin R, Sugau J, Wong KM (2015c) Plant diversity and ecology of ultramafic outcrops in Sabah (Malaysia). Aust J Bot 63:204–215View ArticleGoogle Scholar
- Van der Ent A, van Balgooy M, van Welzen P (2016a) Actephila alanbakeri (Phyllanthaceae): a new nickel hyperaccumulating plant species from localised ultramafic outcrops in Sabah (Malaysia). Bot Stud 57:19View ArticleGoogle Scholar
- Van der Ent A, Echevarria G, Tibbett M (2016b) Delimiting soil chemistry thresholds for nickel hyperaccumulator plants in Sabah (Malaysia). Chemoecology 26:67–82View ArticleGoogle Scholar
- Van der Ent A, Damien L, Callahan DL, Noller BN, Mesjasz-Przybylowicz J, Przybylowicz WJ, Barnabas A, Harris HH (2017) Nickel biopathways in tropical nickel hyperaccumulating trees from Sabah (Malaysia). Sci Rep 7:41861View ArticlePubMedPubMed CentralGoogle Scholar
- Van Welzen PC, Pruesapan K, Telford IRH, Esser H, Bruhl JJ (2014) Phylogenetic reconstruction prompts taxonomic changes in Sauropus, Synostemon and Breynia (Phyllanthaceae tribe Phyllantheae). Blumea 59(2):77–94View ArticleGoogle Scholar
- Vaughan J, Riggio J, Chen J, Peng H, Harris HH, van der Ent A (2017) Characterisation and hydrometallurgical processing of nickel from tropical agromined bio-ore. Hydrometallurgy 169:346–355View ArticleGoogle Scholar
- Webster GL (1956) A monographic study of the West Indian species of Phyllanthus. J Arnold Arbor 37: 91–122, 217–268, 340–359Google Scholar
- Whiting S, Reeves RD, Richards D, Johnson M, Cooke J, Malaisse F, Paton A, Smith J, Angle J, Chaney R et al (2004) Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restor Ecol 12:106–116View ArticleGoogle Scholar
- Wu M-J, Huang T-C, Liu C-C, Chen Y-J, Chang Y-S, Hsu C-L, Wu S-Y, Tseng A-Y, Chang Y-C, Liu C-C, Kaewmuan A (2016) Pollen morphology and taxonomy in Malesian Phyllanthus (Phyllanthaceae). J Jpn Bot 91:257–292Google Scholar