Nickel hyperaccumulation in Antidesma montis-silam: from herbarium discovery to collection in the native habitat Philip Nti Nkrumah, Guillaume Echevarria, Peter Damian Erskine, Antony van der Ent To cite this version: Philip Nti Nkrumah, Guillaume Echevarria, Peter Damian Erskine, Antony van der Ent. Nickel hyperaccumulation in Antidesma montis-silam: from herbarium discovery to collection in the native habitat. Ecological Research, Ecological Society of Japan, 2018, 33 (3), pp.675-685. 10.1007/s11284- 017-1542-4. hal-02622004 HAL Id: hal-02622004 https://hal.inrae.fr/hal-02622004 Submitted on 26 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. 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Distributed under a Creative Commons Attribution| 4.0 International License Ecol Res (2018) 33: 675–685 DOI 10.1007/s11284-017-1542-4 SPECIAL FEATURE Ultramafic Ecosystems: Proceedings of the 9th International Conference on Serpentine Ecology Philip Nti Nkrumah • Guillaume Echevarria Peter Damian Erskine • Antony van der Ent Nickel hyperaccumulation in Antidesma montis-silam: from herbarium discovery to collection in the native habitat Received: 18 September 2017 / Accepted: 22 November 2017 / Published online: 8 December 2017 Ó The Author(s) 2017, corrected publication 2018 Abstract The majority of nickel hyperaccumulator plant screening can lead to discovery of taxa with unique species have been discovered by screening using a field properties. spot test based on dimethylglyoxime. Recently, the use of a portable X-ray fluorescence spectroscopy instru- Keywords Co-accumulation Æ Dimethylglyoxime Æ ments has enabled non-destructive analyses of existing Hyperaccumulator Æ Nickel Æ XRF scanning herbarium collections. Given that the family Phyllan- thaceae globally has the greatest numbers of hyperac- cumulators, all available specimens from this family, Introduction including the speciose genus Antidesma, at the Forest Research Centre Herbarium in Sabah, Malaysia, were Hyperaccumulators are plants that accumulate extraor- analysed. The results reveal 9 new manganese hyperac- dinary concentrations of trace elements in their shoot cumulators in the genus Antidesma, including Antidesma while growing in their natural habitats (Reeves 1992; puncticulatum, with manganese concentrations reaching van der Ent et al. 2013). The worldwide ‘standard ref- up to 46,400 lggÀ1. Prior to this study, only one erence plant’ has elemental concentrations of Ni manganese hyperaccumulator had been recorded in Sa- (1.5 lggÀ1), and Mn (200 lggÀ1) (Markert 1994; Dunn bah. The present study is the first to discover nickel 2007), but in hyperaccumulators these concentrations hyperaccumulator plant species (four species) in the can be thousands of times higher (see van der Ent et al. genus Antidesma, including Antidesma montis-silam with 2013). Understanding the ways in which hyperaccumu- concentrations reaching up to 32,700 lggÀ1. Further lator plants take up and store metals is critical to opti- collection and analyses of plant material of Antidesma mizing their use in agromining (also called montis-silam in the native habitat confirmed the high phytomining), a technology that uses hyperaccumulator foliar nickel concentrations. The high nickel hyperac- plants to sequester valuable metals from sub-economic cumulating characteristic and ostensibly fast growth rate ore bodies such as ultramafic soils (Van der Ent et al. of Antidesma montis-silam infer potential for use in 2015a; Nkrumah et al. 2016). Although there are over agromining technology. Some species in the genus An- 400 Ni hyperaccumulators species (> 0.1 Wt% shoot tidesma exhibit co-accumulation of manganese and dry weight), there are just 50 hypernickelophores nickel. This case-study shows how herbarium XRF (species with > 1 Wt% shoot dry weight) known globally that have the greatest utilization for agromining (Angle et al. 2001;Lietal.2003). Many of these The original version of this article was revised due to a retrospec- hypernickelophores occur in tropical regions such as tive Open Access order. Cuba, New Caledonia and Southeast Asia (Reeves 2003). Among the most promising of these species are a Electronic supplementary material The online version of this article (https://doi.org/10.1007/s11284-017-1542-4) contains supplemen- large number of taxa in the Phyllanthaceae. On a global tary material, which is available to authorized users. scale, Ni hyperaccumulation occurs most frequently in the order Malpighiales, particularly in the families P. N. Nkrumah Æ P. D. Erskine Æ A. van der Ent (&) Centre for Mined Land Rehabilitation, Sustainable Minerals Dichapetalaceae, Phyllanthaceae, Salicaceae and Vio- Institute, The University of Queensland, Queensland, Australia laceae (Reeves 1992, 2003). The Malpighiales is one of E-mail: [email protected] the largest orders of flowering plants, containing approximately 16,000 species in 42 families globally, G. Echevarria Æ A. van der Ent accounting for approximately 7.8% of Eudicots (Wur- Universite´de Lorraine-INRA, Laboratoire Sols et Environnement, UMR 1120, Vandoeuvre-Le` s-Nancy, France dack and Davis 2009). The Phyllanthaceae have the 676 greatest numbers of hyperaccumulators with represen- have been identified by botanical experts at the SAN tatives in the genera Actephila, Breynia, Cleistanthus, herbarium, and we followed the taxonomical nomen- Glochidion and Phyllanthus (Reeves 2003; Van der Ent clature in The Plant List (http://www.theplantlist.org/). et al. 2015b, c; Galey et al. 2017). Apart from representatives from many different families, Some of the world’s largest ultramafic exposures oc- all available specimens from the Phyllanthaceae were cur in Southeast Asia and in Sabah (Malaysia, on the scanned. Given that this family globally hosts the island of Borneo) total 3500 km2 (Proctor et al. 1988; greatest numbers of hyperaccumulators, the explicit aim Repin 1998). Sabah has an estimated 8000 plant species, was to uncover further hyperaccumulators that may of which, over half are known to occur on ultramafic exist in the Sabah flora. Up to now, no Ni hyperaccu- soils (Van der Ent et al. 2015c). This region is a global mulators are known from the genus Antidesma. hotspot for Ni hyperaccumulator plants with at least 25 Antidesma (Phyllanthaceae) is a highly variable genus different species discovered to date (Van der Ent et al. ( 150 species) of dioecious shrubs and trees common in 2015b, c). The family Violaceae has two species of Ri- the understorey of the tropical rain forest (Baker et al. norea (R. aff. bengalensis (Wall.) Gagnep. in Humbert 1998). The genus is distributed in the palaeotropics from and R. aff. Javanica Kuntze) that are Ni hyperaccumu- West Africa to the Pacific, with the greatest numbers of lators. In the genus Phyllanthus there are two known species ( 90) occurring in Malesia (the biogeographical hyperaccumulators (P. cf. securinegioides Merr. and P. region encompassing the Malay Peninsula and the Ma- balgooyi Petra Hoffm. & A. J. M. Baker), at least 9 lay Archipelago) especially Borneo (Baker et al. 1998). species in the genus Glochidion, one in the genus Acte- Antidesma are hardwoods and can have a bole up to phila (A. alanbakeri Welzen and Ent), Flacourtia kina- 30 m high with a diameter up to 1 m, whereas the leaves baluensis Sleumer and Xylosma luzonensis Merr. in the are usually evergreen and 1.5–60 by 0.4–30 cm in size Salicaceae and one species of Dichapetalum (D. gelo- (Hoffmann 2006). The inflorescences are raceme-like nioides subsp. tuberculatum Leenh.) of the Dichapeta- 0.5–35 cm long with the flowers usually light coloured, laceae. There are several Ni hyperaccumulators scattered and the immature fruits green, maturing to bright col- in other families of other orders, including Shorea ours (Hoffmann 2006). Many species of Antidesma are tenuiramulosa P.S.Ashton (Dipterocarpaceae), Walsura ubiquitous in lowland mixed dipterocarp forests on a pinnata Hassk. (Meliaceae), Kibara coriacea (Blume) variety of different soils derived from sedimentary, vol- Hook. f. & A. Thomps (Monimiaceae), Psychotria sar- canic and ultramafic bedrock. Antidesma montis-silam mentosa Blume (Rubiaceae), Mischocarpus sundaicus Airy Shaw is a tree up to 20 m with a clear bole up to Blume (Sapindaceae) (van der Ent et al. 2015b). In Sa- 10 m and diameter up to 22 cm (Airy Shaw 1973). The bah, nickel hyperaccumulators are restricted to circum- bark is whitish, 6 mm thick, and the leaves are oblong neutral ultramafic soils with relatively high phytoavail- 15–33 by 6–11 cm (Airy Shaw 1973). The infructescences able nickel concentrations (van der Ent et al. 2016a). are 14–28 cm long, and the fruits are ellipsoid 10–14 by A feature of woody tropical Ni hyperaccumulator 6–10 mm (Hoffmann 2006). plants is the extreme enrichment of Ni in the phloem The present study focussed on herbarium screening of tissue, literally colouring the phloem green from Ni ions all specimens in the genus Antidesma held at the FRC (Mesjasz-Przybylowicz et al. 2016; Van der Ent et al. herbarium in Sabah, which led to the discovery of Ni 2017a). This phenomenon has so far been described hyperaccumulation in Antidesma montis-silam, which is from Rinorea aff. bengalensis, R. aff. javanica (Vio- known only from a few collections at the type locality. laceae), Dichapetalum gelonioides subsp. tuberculatum We then undertook field survey to investigate the rhi- (Dichapetalaceae), Actephila alanbakeri, Phyllanthus cf. zosphere soil chemistry as well as the elemental con- securinegoides, and P. balgooyi (Phyllanthaceae) with the centrations in the various plant parts of Antidesma latter exuding a dark green phloem sap containing up to montis-silam occurring in the native habitat. 16.9% Ni (van der Ent and Mulligan 2015; Mesjasz- Przybylowicz et al.