Chemoecology DOI 10.1007/s00049-015-0192-7 CHEMOECOLOGY RESEARCH PAPER Ecology of nickel hyperaccumulator plants from ultramafic soils in Sabah (Malaysia) Antony van der Ent • Peter Erskine • Sukaibin Sumail Received: 25 May 2014 / Accepted: 16 February 2015 Ó Springer Basel 2015 Abstract Sabah (Malaysia) has one of the largest surface herbivory-induced leaf damage on Ni hyperaccumulators expressions of ultramafic rocks on Earth and in parallel in Sabah was common, and specialist (Ni-tolerant) insect hosts one of the most species-rich floras. Despite the ex- herbivores were found on several species in this study. The tensive knowledge of the botanical diversity and the identification of Ni hyperaccumulators is necessary to fa- chemistry of these substrates, until recently the records for cilitate their conservation and potential future utilisation in nickel (Ni) hyperaccumulator plants in the area have been Ni phytomining. scant. Recent intensive screening has resulted in 19 new records, adding to the 5 previously known from Sabah. The Keywords Allelopathy Á Dimethylglyoxime Á results of this study indicate that most Ni hyperaccumulator Elemental herbivory defense Á Kinabalu Park plants in Sabah are restricted to successional habitats (ridges, river banks, secondary vegetation) at elevations \1200 m a.s.l. Moreover, Ni hyperaccumulators are lo- Introduction cally common both in terms of number of individuals and relative number of species. Nickel hyperaccumulation oc- Ultramafic soils represent a category of substrates derived curs most frequently in the Order Malpighiales (families from ultramafic bedrock and are sparsely distributed Dichapetalaceae, Phyllanthaceae, Salicaceae, Violaceae), around the world. Such soils are known for relatively high and is particularly common in the Phyllanthaceae (genera concentrations of potentially phytotoxic trace elements, Phyllanthus, Glochidion). Comparison of soil chemistry including nickel (Ni), cobalt (Co) and chromium (Cr) while with elements accumulated in hyperaccumulator foliage concomitantly having cation imbalances and general nu- showed significant correlation between soil exchangeable trient deficiencies (Brooks 1987; Proctor 2003). Of the Ca, K, P and the foliar concentrations of these elements. trace elements enriched in ultramafic soils, Ni is a mi- No direct relationship was found between soil Ni and foliar cronutrient that is essential for some plant species, and Ni, although foliar Ni was negatively correlated with influences plant senescence, nitrogen metabolism, germi- soil pH. Nickel hyperaccumulation has been hypothesised nation and plant disease resistance (Brown et al. 1987; to fulfil herbivory protection functions, but extensive Welch 1995). On ultramafic soils, however, this trace element can be phytotoxic and symptoms indicating excess can include leaf chlorosis and reduced growth (Brune and Handling Editor: Marko Rohlfs. Dietz 1995; Kukier and Chaney 2001; Weng et al. 2003). Some plants restricted to ultramafic soils have evolved A. van der Ent (&) Á P. Erskine Centre for Mined Land Rehabilitation, Sustainable Minerals ecophysiological mechanisms to tolerate and accumulate Institute, The University of Queensland, St Lucia QLD 4072, Ni, and are termed Ni hyperaccumulators when having in Brisbane, Australia excess of 1000 lgg-1 Ni in the foliage (Reeves 1992; Van e-mail: [email protected] der Ent et al. 2013a). The phenomenon is exceptionally S. Sumail rare and known in approximately 400 species worldwide Sabah Parks, Kota Kinabalu, Sabah, Malaysia in a range of different plant families. The Salicaceae, 123 A. van der Ent et al. Buxaceae, Phyllanthaceae and Rubiaceae are the most 1998). However, whereas the synthesis of organic toxic common families for Ni hyperaccumulators in tropical re- molecules by plants is relatively flexible in evolutionary gions (Reeves 2006). Nickel hyperaccumulators can be terms, Ni accumulation is not (Cheruiyot et al. 2013). categorised into ‘strict’ and ‘facultative’ hyperaccumula- The ultramafic soils of the Malaysian state of Sabah on tors. Strict hyperaccumulators are exclusively confined to the Island of Borneo are extensive, occupying a total area ultramafic soil and all populations of the particular species of about 3500 km2 (Proctor et al. 1988) and is renowned are hyperaccumulators. However, species that are ‘facul- for high species richness (Van der Ent et al. 2014). The tative’ hyperaccumulators have populations on ultramafic flora of Sabah has an estimated 8000 vascular plant species soils that are hyperaccumulators, and populations on other (Wong 1992) with over 5000 plant species in the soils that are not (Pollard et al. 2014). An example of a \1200 km2 Kinabalu Park (Beaman 2005). Prior to this facultative Ni hyperaccumulator which occurs in Sabah is study, the following Ni hyperaccumulators were known to Rinorea bengalensis (Violaceae), that has Ni concentra- occur in Sabah: Rinorea bengalensis and R. javanica tions of 1000–17,750 lgg-1 in the foliage of specimens of (Violaceae) (Brooks and Wither 1977; Brooks et al. 1977), this species growing on ultramafic soils, and 1–300 lgg-1 Phyllanthus balgooyi (Phyllanthaceae) (Baker et al. 1992; in foliage of specimens of this species growing on non- Hoffmann et al. 2003), Dichapetalum gelonioides ultramafic soils (Reeves 2003; Van der Ent et al. 2013a). (Dichapetalaceae) (Baker et al. 1992), Psychotria cf. gra- Hyperaccumulation is hypothesised to have evolved to cilis (Rubiaceae) (Reeves 2003) and Shorea tenuiramulosa interfere with other competing plant species (‘elemental (Dipterocarpaceae) (Proctor et al. 1989). The objective of allelopathy’), or to protect against insect herbivores (‘ele- this study was to screen the flora of ultramafic outcrops in mental herbivory defense’), although a variety of other Sabah, mainly Kinabalu Park, for the occurrence of (more) explanations have also been suggested (Martens and Boyd Ni hyperaccumulators. Further aims were to elucidate 1994; Boyd and Jaffre´ 2001). The first hypothesis suggests general phylogenetic patterns of Ni hyperaccumulation, that hyperaccumulators increase Ni concentrations in the habitat characteristics, overall plant-soil relationships and soil area around the plant base (‘phyto-enrichment’) via potential ecological interactions relating to herbivory and leaf litter deposition as a result of leaf senescence and allelopathy. abscission which, as a result of toxicity effects, might re- duce growth performance and germination of competing plant species (Boyd and Martens 1998). Given the inherent Materials and methods Ni-tolerance of hyperaccumulators, this might also provide advantages in survival of seedlings of the same hyper- Study area and field collection accumulator species (or indeed, of different Ni hyperaccumulator species if these occur in the same habi- As part of a larger study on the relationships between plant tat). The second hypothesis suggests that high foliar Ni diversity and soil chemistry of ultramafic outcrops at concentrations protect against insect herbivores. As a Mount Kinabalu and Mount Tambuyukon in Sabah, consequence, Ni hyperaccumulators suffer less damage as Malaysia, plants were screened for Ni hyperaccumulators a result of insect herbivory, and hence have competitive (Van der Ent et al. 2013c). During the fieldwork on the advantages. Further refinements of this model led to the ultramafic soils in Kinabalu Park (January 2011–September formulation of the ‘Defensive Enhancement Hypothesis’, 2012), leaf samples were collected from all plants in plots which proposes that after an initial defensive benefit re- (there were a total of 101 plots, ranging is size from 2000 sulting from relatively low initial foliar Ni concentrations, to 250 m2 and as many different plants as possible in the increased concentrations provided increased plant fitness, surrounding vegetation). In addition, plants were screened and led to a step-wise increase in foliar Ni accumulation during fieldwork in the following Forest Reserves else- (Boyd 2012). Furthermore, the ‘Joint Effects Hypothesis’ where in Sabah: Mount Tavai, Bidu-Bidu Hills, Mount proposes that Ni accumulation in combination with organic Silam and Bukit Hampuan. Figure 1 shows a map of Sabah chemicals (such as alkaloids) could have synergistic effects (Malaysia) with the study localities. In the field, the leaf (Boyd 2012). In the context of ‘elemental herbivory de- samples were pressed against white test paper impregnated fense’, foliar Ni accumulation has the distinct benefit of with the Ni-specific colorimetric reagent, dimethylgly- requiring limited energetic resources (although the uptake oxime (‘DMG’), which changes colour, to purple, upon and transport physiology requires Ni complexing ligands contact with Ni. Approximately 5000 plant samples have such as citrate) because Ni is not produced but rather been tested using this method. All samples that tested vi- translocated from the soil and, contrary to organic mole- sually positive were re-collected (fully grown sun leaves, at cules, Ni cannot be broken down or metabolised to avoid least 2 m above the soil surface) by hand. Fresh plant toxicity (Martens and Boyd, 1994; Boyd and Martens leaves were put in paper bags to prevent decomposition 123 Ecology of nickel hyperaccumulator plants Fig. 1 Map of Sabah (Malaysia) with study localities. The insert shows the location of Sabah on the Island of Borneo. Satellite imagery is Landsat, from Google Earth with insert from ArcGIS (esri) before transport to the field station.