Actephila alanbakeri (Phyllanthaceae): a new nickel hyperaccumulating plant species from localised ultramafic outcrops in Sabah (Malaysia)
© van der Ent et al. 2016
Received: 14 October 2015
Accepted: 28 January 2016
Published: 9 February 2016
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 morphological 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 14,700 μg g−1 (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 individuals, render this species Endangered (EN) on the basis of IUCN Red List Criteria.
Ultramafic soils represent a category of substrates derived from ultramafic bedrock and are sparsely distributed around the world (Brooks 1987). These soils are known for relatively high concentrations of potentially phytotoxic trace elements, mainly nickel (Ni), as well as major cation imbalance and nutrient-deficiencies (Proctor 2003). The ultramafic soils of the Malaysian state of Sabah on Borneo Island are extensive, occupying an area of about 3500 km2 (Proctor et al. 1988) and are renowned for their high species richness with at least 2500 different plant species known to date (Van der Ent et al. 2015a). Some plants restricted to ultramafic soils have evolved ecophysiological mechanisms to tolerate and accumulate Ni, and are termed Ni hyperaccumulators when having in excess of 1000 ug g−1 Ni in their leaves (Jaffré et al. 1976; Reeves 1992, 2003; Van der Ent et al. 2013a). This phenomenon is rare and known in approximately 450 species worldwide in many different plant families (Reeves 2003; Van der Ent et al. 2013a). Nickel hyperaccumulators can be categorized into ‘obligate’ and ‘facultative’ hyperaccumulators (Pollard et al. 2014). Obligate hyperaccumulators are exclusively found on ultramafic soil and all populations of the particular species are hyperaccumulators. However, species that are ‘facultative’ hyperaccumulators have populations on ultramafic soils that are Ni hyperaccumulators, and populations on other soils that are not (Van der Ent et al. 2013a; Pollard et al. 2014). Hyperaccumulation is hypothesized to have evolved to interfere with other competing plant species (‘elemental allelopathy’) or to protect against insect herbivores (‘elemental herbivory defense’), although a variety of other explanations have also been proposed (Boyd and Martens 1998; Boyd and Jaffré 2001; Boyd 2012). Recent research activities have revealed the existence of at least 25 different Ni hyperaccumulator species in Sabah, making it a global hotspot for such plants (Van der Ent et al. 2013c, 2015b, c). The majority of Ni hyperaccumulating species in Sabah appear to be restricted to a single site or a few ultramafic outcrops and are hence rare and possibly threatened (Van der Ent et al. 2015b).
Actephila Blume is a plant genus in the tribe Poranthereae of the family Phyllanthaceae (Hoffmann et al. 2006). The genus comprises approximately 40 species ranging from Southeast Asia to the Pacific Islands (Govaerts et al. 2000). Typical for the genus are the generally single, axillary flowers with the petals smaller than the sepals. In the staminate flowers disc lobes are present and the stamens are free (or basally united) and centred around a three-fid pistillode. The pistillate flowers have a ring-like disc and a three-locular ovary with two ovules per locule. During fieldwork undertaken in 2011–2013 a new species of Actephila was collected on a hill near Nalumad, at the boundary of Kinabalu Park in Sabah, Malaysia. Later we also found a herbarium specimen that matched this taxon that was collected from Malawali Island, also in Sabah.
Specimens were examined in Leiden, The Netherlands, from herbarium material sent from the Sabah Parks Herbarium (SNP) in Malaysia. The first author undertook fieldwork in Malaysia during 2011–2013. Soil samples (n = 3) were collected near the roots of the new Actephila species and air-dried at room temperature for 3 weeks before laboratory analyses. The soil pH was measured in a 1:2.5 soil:water mix. Soil sub-samples were extracted with DTPA (for phytoavailable trace elements, such as Ni) and with silverthiorea (for exchangeable cations, including calcium, magnesium, potassium and sodium) solutions (Becquer et al. 1995; Dohrmann 2006). Soil sub-samples were also digested with concentrated nitric (70 %) and hydrochloric (37 %) acid in a specialised microwave. Plant part samples (roots, twigs, bark, phloem, wood, leaves) collected from mature plants of the new Actephila were immediately washed with demineralised water, oven-dried at 70 °C and then digested with concentrated nitric acid (70 %) and hydrogen peroxide (30 %) in a specialised microwave. The soil and plant part sample extracts were finally measured with ICP-AES (Varian Vista Pro II) for Ni, Co, Mn, Fe, Mg, Ca, Na, K and P. The ICP-AES instrument was calibrated using a 6-point multi-element standard (Ni, Co, Mn, Fe, Mg, Ca, Na, K, P) prepared in each extraction solution. The laboratory work was undertaken at The University of Queensland, Australia.
Actephila alanbakeri Welzen and Ent, sp. nov. —TYPE: MALAYSIA. Sabah. Near Kinabalu Park, Nalumad, Antony Van der Ent et al. SNP 38,539 (holo SNP; iso L). Paratype: SAN 145750, Malawali Island Kudat District, Sabah, Malaysia, John B. Sugau and Dauni Seligi (L, SAN).
This species differs in the knobbly fruits from all other species of Actephila, which have smooth fruits. The leaves dry to a distinct yellowish green.
Shrub, 3 m high, monoecious; flowering branchlets angular when dry, striate, c. 2 mm diam., greenish. Indumentum of simple hairs, most parts glabrous. Stipules triangular, 1.4–1.5 by 1–1.2 mm, persistent, stiff, brown when dry, base triangular in transverse section, margins slightly erose, glabrous except for basal row of up to 0.4 mm long papillae-like hairs. Leaves alternate, simple; petiole 2.5–8 mm long, deeply grooved above, smooth, glabrous; blade elliptic, 5.1–15.5 by 1–3.3 cm, 4.7–5.1 times as long as wide, symmetric, coriaceous, base slightly rounded, margins entire, revolute, apex acute, tip blunt, glabrous, drying yellowish green, duller and lighter below, venation pinnate, slightly raised above, raised below, secondary nerves 13–17 pairs, arching and closed near margin, higher order veins reticulate. Inflorescences axillary fascicles, containing a single flower in the type; bracts as stipules, slightly smaller, outer one c. 1 by 1 mm. Staminate flower c. 3 mm diam.; pedicel c. 3 mm long, somewhat angular when dry, pink and round when fresh, glabrous; sepals 5, ovate, c. 2 by 1 mm, free, apex acute, central part thicker, margins more membranous, pinkish red, outside hairy, glabrous inside; petals five, alternisepalous, shorter than sepals, spade-like, c. 1 by 1 mm, membranous, pinkish white, glabrous; disc thick, ring-like to partly free lobes, lobes episepalous, emarginate, whitish; stamens 5, epipetalous, glabrous, filaments c. 1.2 mm long, apically bent outwards, slightly tapering towards the apex, anthers basifixed, c. 0.4 by 0.5 mm, 2-thecate, thecae separate from each other, opening with apical transverse slit, pollen yellow; pistillode c. 1 mm long, tri-partite, hairy, pinkish red. Pistillate flowers not seen. Fruits 5- or 3-locular, lobes around seeds, knobbly all over. Similar fruits are known in Euphorbiaceae s.l. e.g., Dimorphocalyx, but not in Phyllanthaceae, formerly included in Euphorbiaceae (Van Balgooy 1997).
The specific epithet “alanbakeri” honours Professor Alan J. M. Baker, who is a leading pioneer in the discovery and global research on hyperaccumulator plants and in developing phytomining technology. Research by Professor Baker and his international collaborators since the late 1970s led to the discovery of most of the hyperaccumulator plants known to science today.
As far as known this species flowers and fruits all year round.
Distribution and habitat
The species appears restricted to a ridge (‘Lompoyou Hill’) near the villages of Nalumad and Pahu, and from Malawali Island, both in Sabah, Malaysia. At the site near Nalumad, the hill (400 masl) has been burnt at least once as a result of an uncontrolled forest fire in the late 2000s. Prior to burning, the site had already been disturbed by logging. At present the site 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 plants occur, including Phyllanthus balgooyi Petra Hoffm. and A. J. M. Baker and P. cf. securinegioides Merr. (Phyllanthaceae), Mischocarpus sundaicus Blume (Sapindaceae), Rinorea javanica Kuntze (Violaceae), Psychotria sarmentosa Blume (Rubiaceae) and Xylosma luzonensis Clos (Salicaceae). The local conditions are pronouncedly xeric, and the soils are shallow and heavily eroded, revealing the underlying saprolite. Actephila alanbakeri occurs sporadically in this scrub with scattered individuals mainly on the ridges. Little information is available for the collection from Malawali Island, except that the Actephila grew on ultramafic soil at 79 masl in forest.
Soil chemistry in the rooting zone of Actephila alanbakeri (the number of samples is three with ranges and means provided)
Co (total) μg g−1
Mg (exch.) μg g−1
K (exch.) μg g−1
P (total) μg g−1
Co (DTPA) μg g−1
Cr (total) μg g−1
Ca (total) μg g−1
Ca (exch.) μg g−1
Fe (total) mg g−1
Mg (total mg g−1
Mn (total) mg g−1
Ni (total) μg g−1
Ni (DTPA) μg g−1
Plant foliar chemistry
Plant part chemistry of Actephila alanbakeri (number of samples indicated, for leaves and twigs ranges and means are provided)
Al μg g−1
Ca μg g−1
Co μg g−1
Fe μg g−1
K μg g−1
Mg μg g−1
Mn μg g−1
Ni μg g−1
P μg g−1
S μg g−1
Zn μg g−1
Phylogenetic occurrence of Ni hyperaccumulation
The habitats of Actephila alanbakeri are outside any protected areas, on a hill close to Kinabalu Park, and on Malawali Island. The restriction of this species to just two populations, the small area of occupancy (<10 km2), and the small number of individuals (no more than 100 individuals have been observed to date, although no information is available about the population-dynamics and hence trends in population size) means that this species is sensitive to disturbances which could ultimately lead to its extinction. This is a real possibility because Actephila alanbakeri occurs in patches of remaining scrub in an area devastated by recurring forest fires. Therefore, the species can be classified as Endangered (EN) on the basis of IUCN Red List Criteria (Version 3.1: IUCN 2001).
Outlook and further research
AVDE conducted the fieldwork and collected the plant specimens in Sabah. PVW carried out the taxonomical study. AVDE undertook the laboratory analyses. AVDE, MVB and PVW prepared the manuscript. All authors read and approved the final manuscript.
The Sabah Parks Herbarium (SNP) is gratefully acknowledged for the loan of the herbarium material. We would like to express our gratitude to Sabah Parks for the joint research project with Rimi Repin during which this species was discovered, and in particular to Sukaibin Sumail and Rositti Karim for their help and expertise in the field and in the herbarium. We would like to acknowledge the Sabah Biodiversity Council for granting permission for conducting research in Sabah. Finally, the French National Research Agency through the national “Investissements d’avenir” program (ANR-10-LABX-21—LABEX RESSOURCES21) is gratefully acknowledged for funding A. van der Ent’s post-doctoral position in 2014–2015.
The authors declare that they have no competing interests.
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