van der Ent et al. Bot Stud (2016) 57:6 DOI 10.1186/s40529-016-0122-1 ORIGINAL ARTICLE Open Access Actephila alanbakeri (Phyllanthaceae): a new nickel hyperaccumulating plant species from localised ultramafic outcrops in Sabah (Malaysia) Antony van der Ent1,2* , Max van Balgooy3 and Peter van Welzen3,4 Abstract The Malaysian state of Sabah on the Island of Borneo is emerging as a hotspot for nickel hyperaccumulator species with at least 25 such species discovered to date. New discoveries of the hyperaccumulation trait in described taxa, as well as taxonomical novelties that are nickel hyperaccumulators, continue to be made. Here we describe a new nickel hyperaccumulating species of Actephila (Phyllanthaceae) originating from two known populations on ultramafic soils in Sabah. The most characteristic feature of Actephila alanbakeri are its knobbly fruits, but other diagnostic morpho- logical characters are discussed and information about its ecology and rhizosphere and plant tissue chemistry is provided. This new species is one of the strongest known nickel hyperaccumulator plants in Southeast Asia with up to 1 14,700 μg g− (1.47 %) nickel in its leaves. The occurrences of Actephila alanbakeri on just two sites, both of which lie outside protected areas and are disturbed by recurring forest fires, combined with the small total numbers of indi- viduals, render this species Endangered (EN) on the basis of IUCN Red List Criteria. Keywords: Actephila, Malaysia, Phyllanthaceae, Sabah, Ultramafic Background hyperaccumulators when having in excess of 1000 ug Ultramafic soils represent a category of substrates g−1 Ni in their leaves (Jaffré et al. 1976; Reeves 1992, derived from ultramafic bedrock and are sparsely dis- 2003; Van der Ent et al. 2013a). This phenomenon is tributed around the world (Brooks 1987). These soils are rare and known in approximately 450 species worldwide known for relatively high concentrations of potentially in many different plant families (Reeves 2003; Van der phytotoxic trace elements, mainly nickel (Ni), as well Ent et al. 2013a). Nickel hyperaccumulators can be cat- as major cation imbalance and nutrient-deficiencies egorized into ‘obligate’ and ‘facultative’ hyperaccumula- (Proctor 2003). The ultramafic soils of the Malaysian tors (Pollard et al. 2014). Obligate hyperaccumulators state of Sabah on Borneo Island are extensive, occu- are exclusively found on ultramafic soil and all popula- pying an area of about 3500 km2 (Proctor et al. 1988) tions of the particular species are hyperaccumulators. and are renowned for their high species richness with However, species that are ‘facultative’ hyperaccumu- at least 2500 different plant species known to date lators have populations on ultramafic soils that are Ni (Van der Ent et al. 2015a). Some plants restricted to hyperaccumulators, and populations on other soils that ultramafic soils have evolved ecophysiological mecha- are not (Van der Ent et al. 2013a; Pollard et al. 2014). nisms to tolerate and accumulate Ni, and are termed Ni Hyperaccumulation is hypothesized to have evolved to interfere with other competing plant species (‘elemen- tal allelopathy’) or to protect against insect herbivores *Correspondence: [email protected] (‘elemental herbivory defense’), although a variety of 2 Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, St Lucia, Brisbane, QLD 4072, Australia other explanations have also been proposed (Boyd and Full list of author information is available at the end of the article Martens 1998; Boyd and Jaffré 2001; Boyd 2012). Recent © 2016 van der Ent et al. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. van der Ent et al. Bot Stud (2016) 57:6 Page 2 of 8 research activities have revealed the existence of at least Results 25 different Ni hyperaccumulator species in Sabah, Taxonomic treatment making it a global hotspot for such plants (Van der Ent Actephila alanbakeri Welzen and Ent, sp. nov. —TYPE: et al. 2013c, 2015b, c). The majority of Ni hyperaccumu- MALAYSIA. Sabah. Near Kinabalu Park, Nalumad, lating species in Sabah appear to be restricted to a sin- Antony Van der Ent et al. SNP 38,539 (holo SNP; iso gle site or a few ultramafic outcrops and are hence rare L). Paratype: SAN 145750, Malawali Island Kudat Dis- and possibly threatened (Van der Ent et al. 2015b). trict, Sabah, Malaysia, John B. Sugau and Dauni Seligi (L, Actephila Blume is a plant genus in the tribe Poran- SAN). thereae of the family Phyllanthaceae (Hoffmann et al. This species differs in the knobbly fruits from all other 2006). The genus comprises approximately 40 spe- species of Actephila, which have smooth fruits. The cies ranging from Southeast Asia to the Pacific Islands leaves dry to a distinct yellowish green. (Govaerts et al. 2000). Typical for the genus are the gen- Shrub, 3 m high, monoecious; flowering branchlets erally single, axillary flowers with the petals smaller than angular when dry, striate, c. 2 mm diam., greenish. Indu- the sepals. In the staminate flowers disc lobes are present mentum of simple hairs, most parts glabrous. Stipules and the stamens are free (or basally united) and centred triangular, 1.4–1.5 by 1–1.2 mm, persistent, stiff, brown around a three-fid pistillode. The pistillate flowers have a when dry, base triangular in transverse section, mar- ring-like disc and a three-locular ovary with two ovules gins slightly erose, glabrous except for basal row of up to per locule. During fieldwork undertaken in 2011–2013 0.4 mm long papillae-like hairs. Leaves alternate, simple; a new species of Actephila was collected on a hill near petiole 2.5–8 mm long, deeply grooved above, smooth, Nalumad, at the boundary of Kinabalu Park in Sabah, glabrous; blade elliptic, 5.1–15.5 by 1–3.3 cm, 4.7–5.1 Malaysia. Later we also found a herbarium specimen that times as long as wide, symmetric, coriaceous, base matched this taxon that was collected from Malawali slightly rounded, margins entire, revolute, apex acute, tip Island, also in Sabah. blunt, glabrous, drying yellowish green, duller and lighter below, venation pinnate, slightly raised above, raised Methods below, secondary nerves 13–17 pairs, arching and closed Specimens were examined in Leiden, The Netherlands, near margin, higher order veins reticulate. Inflorescences from herbarium material sent from the Sabah Parks axillary fascicles, containing a single flower in the type; Herbarium (SNP) in Malaysia. The first author under- bracts as stipules, slightly smaller, outer one c. 1 by 1 mm. took fieldwork in Malaysia during 2011–2013. Soil sam- Staminate flower c. 3 mm diam.; pedicel c. 3 mm long, ples (n = 3) were collected near the roots of the new somewhat angular when dry, pink and round when fresh, Actephila species and air-dried at room temperature glabrous; sepals 5, ovate, c. 2 by 1 mm, free, apex acute, for 3 weeks before laboratory analyses. The soil pH was central part thicker, margins more membranous, pink- measured in a 1:2.5 soil:water mix. Soil sub-samples ish red, outside hairy, glabrous inside; petals five, alterni- were extracted with DTPA (for phytoavailable trace ele- sepalous, shorter than sepals, spade-like, c. 1 by 1 mm, ments, such as Ni) and with silverthiorea (for exchange- membranous, pinkish white, glabrous; disc thick, ring- able cations, including calcium, magnesium, potassium like to partly free lobes, lobes episepalous, emarginate, and sodium) solutions (Becquer et al. 1995; Dohrmann whitish; stamens 5, epipetalous, glabrous, filaments c. 2006). Soil sub-samples were also digested with con- 1.2 mm long, apically bent outwards, slightly tapering centrated nitric (70 %) and hydrochloric (37 %) acid in a towards the apex, anthers basifixed, c. 0.4 by 0.5 mm, specialised microwave. Plant part samples (roots, twigs, 2-thecate, thecae separate from each other, opening with bark, phloem, wood, leaves) collected from mature apical transverse slit, pollen yellow; pistillode c. 1 mm plants of the new Actephila were immediately washed long, tri-partite, hairy, pinkish red. Pistillate flowers not with demineralised water, oven-dried at 70 °C and then seen. Fruits 5- or 3-locular, lobes around seeds, knobbly digested with concentrated nitric acid (70 %) and hydro- all over. Similar fruits are known in Euphorbiaceae s.l. gen peroxide (30 %) in a specialised microwave. The soil e.g., Dimorphocalyx, but not in Phyllanthaceae, formerly and plant part sample extracts were finally measured included in Euphorbiaceae (Van Balgooy 1997). with ICP-AES (Varian Vista Pro II) for Ni, Co, Mn, Fe, Mg, Ca, Na, K and P. The ICP-AES instrument was cali- Etymology brated using a 6-point multi-element standard (Ni, Co, The specific epithet “alanbakeri” honours Professor Alan Mn, Fe, Mg, Ca, Na, K, P) prepared in each extraction J. M. Baker, who is a leading pioneer in the discovery and solution. The laboratory work was undertaken at The global research on hyperaccumulator plants and in devel- University of Queensland, Australia. oping phytomining technology. Research by Professor van der Ent et al. Bot Stud (2016) 57:6 Page 3 of 8 Baker and his international collaborators since the late Table 1 Soil chemistry in the rooting zone of Actephila 1970s led to the discovery of most of the hyperaccumula- alanbakeri (the number of samples is three with ranges and means provided) tor plants known to science today. Parameter Range Phenology pH 6.4–7.0 [6.7] As far as known this species flowers and fruits all year 1 Co (total) μg g− 122–670 [369] round.