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<title xml:lang="en">Ultramafic geoecology of South and Southeast Asia</title>
<author>
<name sortKey="Galey, M L" sort="Galey, M L" uniqKey="Galey M" first="M. L." last="Galey">M. L. Galey</name>
<affiliation>
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<institution-id institution-id-type="GRID">grid.17635.36</institution-id>
<institution>Center for Water and Environment, Natural Resources Research Institute,</institution>
<institution>University of Minnesota,</institution>
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Duluth, MN 55811 USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Van Der Ent, A" sort="Van Der Ent, A" uniqKey="Van Der Ent A" first="A." last="Van Der Ent">A. Van Der Ent</name>
<affiliation>
<nlm:aff id="Aff2">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.1003.2</institution-id>
<institution>Centre for Mined Land Rehabilitation, Sustainable Minerals Institute,</institution>
<institution>The University of Queensland,</institution>
</institution-wrap>
Brisbane, QLD Australia</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="Aff3">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.29172.3f</institution-id>
<institution>Laboratoire Sols et Environnement,</institution>
<institution>Université de Lorraine-INRA,</institution>
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UMR 1120, Nancy, France</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Iqbal, M C M" sort="Iqbal, M C M" uniqKey="Iqbal M" first="M. C. M." last="Iqbal">M. C. M. Iqbal</name>
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<institution-id institution-id-type="GRID">grid.419020.e</institution-id>
<institution>Plant Biology Laboratory,</institution>
<institution>National Institute of Fundamental Studies,</institution>
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Kandy, 20000 Sri Lanka</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Rajakaruna, N" sort="Rajakaruna, N" uniqKey="Rajakaruna N" first="N." last="Rajakaruna">N. Rajakaruna</name>
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<institution-id institution-id-type="GRID">grid.253547.2</institution-id>
<institution>Biological Sciences Department,</institution>
<institution>California Polytechnic State University,</institution>
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San Luis Obispo, CA 93407 USA</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="Aff6">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.25881.36</institution-id>
<institution>Unit for Environmental Sciences and Management,</institution>
<institution>North-West University,</institution>
</institution-wrap>
Potchefstroom, 2520 South Africa</nlm:aff>
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<idno type="RBID">PMC:5432931</idno>
<idno type="doi">10.1186/s40529-017-0167-9</idno>
<date when="2017">2017</date>
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<title xml:lang="en" level="a" type="main">Ultramafic geoecology of South and Southeast Asia</title>
<author>
<name sortKey="Galey, M L" sort="Galey, M L" uniqKey="Galey M" first="M. L." last="Galey">M. L. Galey</name>
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<nlm:aff id="Aff1">
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<institution-id institution-id-type="GRID">grid.17635.36</institution-id>
<institution>Center for Water and Environment, Natural Resources Research Institute,</institution>
<institution>University of Minnesota,</institution>
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Duluth, MN 55811 USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Van Der Ent, A" sort="Van Der Ent, A" uniqKey="Van Der Ent A" first="A." last="Van Der Ent">A. Van Der Ent</name>
<affiliation>
<nlm:aff id="Aff2">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.1003.2</institution-id>
<institution>Centre for Mined Land Rehabilitation, Sustainable Minerals Institute,</institution>
<institution>The University of Queensland,</institution>
</institution-wrap>
Brisbane, QLD Australia</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="Aff3">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.29172.3f</institution-id>
<institution>Laboratoire Sols et Environnement,</institution>
<institution>Université de Lorraine-INRA,</institution>
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UMR 1120, Nancy, France</nlm:aff>
</affiliation>
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<author>
<name sortKey="Iqbal, M C M" sort="Iqbal, M C M" uniqKey="Iqbal M" first="M. C. M." last="Iqbal">M. C. M. Iqbal</name>
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<nlm:aff id="Aff4">
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<institution-id institution-id-type="GRID">grid.419020.e</institution-id>
<institution>Plant Biology Laboratory,</institution>
<institution>National Institute of Fundamental Studies,</institution>
</institution-wrap>
Kandy, 20000 Sri Lanka</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Rajakaruna, N" sort="Rajakaruna, N" uniqKey="Rajakaruna N" first="N." last="Rajakaruna">N. Rajakaruna</name>
<affiliation>
<nlm:aff id="Aff5">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.253547.2</institution-id>
<institution>Biological Sciences Department,</institution>
<institution>California Polytechnic State University,</institution>
</institution-wrap>
San Luis Obispo, CA 93407 USA</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="Aff6">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.25881.36</institution-id>
<institution>Unit for Environmental Sciences and Management,</institution>
<institution>North-West University,</institution>
</institution-wrap>
Potchefstroom, 2520 South Africa</nlm:aff>
</affiliation>
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<series>
<title level="j">Botanical Studies</title>
<idno type="ISSN">1817-406X</idno>
<idno type="eISSN">1999-3110</idno>
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<date when="2017">2017</date>
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<div type="abstract" xml:lang="en">
<p>Globally, ultramafic outcrops are renowned for hosting floras with high levels of endemism, including plants with specialised adaptations such as nickel or manganese hyperaccumulation. Soils derived from ultramafic regoliths are generally nutrient-deficient, have major cation imbalances, and have concomitant high concentrations of potentially phytotoxic trace elements, especially nickel. The South and Southeast Asian region has the largest surface occurrences of ultramafic regoliths in the world, but the geoecology of these outcrops is still poorly studied despite severe conservation threats. Due to the paucity of systematic plant collections in many areas and the lack of georeferenced herbarium records and databased information, it is not possible to determine the distribution of species, levels of endemism, and the species most threatened. However, site-specific studies provide insights to the ultramafic geoecology of several locations in South and Southeast Asia. The geoecology of tropical ultramafic regions differs substantially from those in temperate regions in that the vegetation at lower elevations is generally tall forest with relatively low levels of endemism. On ultramafic mountaintops, where the combined forces of edaphic and climatic factors intersect, obligate ultramafic species and hyperendemics often occur. Forest clearing, agricultural development, mining, and climate change-related stressors have contributed to rapid and unprecedented loss of ultramafic-associated habitats in the region. The geoecology of the large ultramafic outcrops of Indonesia’s Sulawesi, Obi and Halmahera, and many other smaller outcrops in South and Southeast Asia, remains largely unexplored, and should be prioritised for study and conservation.</p>
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<pmc article-type="review-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Bot Stud</journal-id>
<journal-id journal-id-type="iso-abbrev">Bot Stud</journal-id>
<journal-title-group>
<journal-title>Botanical Studies</journal-title>
</journal-title-group>
<issn pub-type="ppub">1817-406X</issn>
<issn pub-type="epub">1999-3110</issn>
<publisher>
<publisher-name>Springer Berlin Heidelberg</publisher-name>
<publisher-loc>Berlin/Heidelberg</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">28510201</article-id>
<article-id pub-id-type="pmc">5432931</article-id>
<article-id pub-id-type="publisher-id">167</article-id>
<article-id pub-id-type="doi">10.1186/s40529-017-0167-9</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Review</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Ultramafic geoecology of South and Southeast Asia</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Galey</surname>
<given-names>M. L.</given-names>
</name>
<address>
<email>galey004@umn.edu</email>
</address>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>van der Ent</surname>
<given-names>A.</given-names>
</name>
<address>
<email>a.vanderent@uq.edu.au</email>
</address>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff3">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Iqbal</surname>
<given-names>M. C. M.</given-names>
</name>
<address>
<email>mcmif2003@yahoo.com</email>
</address>
<xref ref-type="aff" rid="Aff4">4</xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Rajakaruna</surname>
<given-names>N.</given-names>
</name>
<address>
<email>nrajakaruna@gmail.com</email>
</address>
<xref ref-type="aff" rid="Aff5">5</xref>
<xref ref-type="aff" rid="Aff6">6</xref>
</contrib>
<aff id="Aff1">
<label>1</label>
<institution-wrap>
<institution-id institution-id-type="GRID">grid.17635.36</institution-id>
<institution>Center for Water and Environment, Natural Resources Research Institute,</institution>
<institution>University of Minnesota,</institution>
</institution-wrap>
Duluth, MN 55811 USA</aff>
<aff id="Aff2">
<label>2</label>
<institution-wrap>
<institution-id institution-id-type="GRID">grid.1003.2</institution-id>
<institution>Centre for Mined Land Rehabilitation, Sustainable Minerals Institute,</institution>
<institution>The University of Queensland,</institution>
</institution-wrap>
Brisbane, QLD Australia</aff>
<aff id="Aff3">
<label>3</label>
<institution-wrap>
<institution-id institution-id-type="GRID">grid.29172.3f</institution-id>
<institution>Laboratoire Sols et Environnement,</institution>
<institution>Université de Lorraine-INRA,</institution>
</institution-wrap>
UMR 1120, Nancy, France</aff>
<aff id="Aff4">
<label>4</label>
<institution-wrap>
<institution-id institution-id-type="GRID">grid.419020.e</institution-id>
<institution>Plant Biology Laboratory,</institution>
<institution>National Institute of Fundamental Studies,</institution>
</institution-wrap>
Kandy, 20000 Sri Lanka</aff>
<aff id="Aff5">
<label>5</label>
<institution-wrap>
<institution-id institution-id-type="GRID">grid.253547.2</institution-id>
<institution>Biological Sciences Department,</institution>
<institution>California Polytechnic State University,</institution>
</institution-wrap>
San Luis Obispo, CA 93407 USA</aff>
<aff id="Aff6">
<label>6</label>
<institution-wrap>
<institution-id institution-id-type="GRID">grid.25881.36</institution-id>
<institution>Unit for Environmental Sciences and Management,</institution>
<institution>North-West University,</institution>
</institution-wrap>
Potchefstroom, 2520 South Africa</aff>
</contrib-group>
<pub-date pub-type="epub">
<day>3</day>
<month>4</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>3</day>
<month>4</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection">
<month>12</month>
<year>2017</year>
</pub-date>
<volume>58</volume>
<elocation-id>18</elocation-id>
<history>
<date date-type="received">
<day>28</day>
<month>10</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>1</day>
<month>3</month>
<year>2017</year>
</date>
</history>
<permissions>
<copyright-statement>© The Author(s) 2017</copyright-statement>
<license license-type="OpenAccess">
<license-p>
<bold>Open Access</bold>
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
), 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.</license-p>
</license>
</permissions>
<abstract id="Abs1">
<p>Globally, ultramafic outcrops are renowned for hosting floras with high levels of endemism, including plants with specialised adaptations such as nickel or manganese hyperaccumulation. Soils derived from ultramafic regoliths are generally nutrient-deficient, have major cation imbalances, and have concomitant high concentrations of potentially phytotoxic trace elements, especially nickel. The South and Southeast Asian region has the largest surface occurrences of ultramafic regoliths in the world, but the geoecology of these outcrops is still poorly studied despite severe conservation threats. Due to the paucity of systematic plant collections in many areas and the lack of georeferenced herbarium records and databased information, it is not possible to determine the distribution of species, levels of endemism, and the species most threatened. However, site-specific studies provide insights to the ultramafic geoecology of several locations in South and Southeast Asia. The geoecology of tropical ultramafic regions differs substantially from those in temperate regions in that the vegetation at lower elevations is generally tall forest with relatively low levels of endemism. On ultramafic mountaintops, where the combined forces of edaphic and climatic factors intersect, obligate ultramafic species and hyperendemics often occur. Forest clearing, agricultural development, mining, and climate change-related stressors have contributed to rapid and unprecedented loss of ultramafic-associated habitats in the region. The geoecology of the large ultramafic outcrops of Indonesia’s Sulawesi, Obi and Halmahera, and many other smaller outcrops in South and Southeast Asia, remains largely unexplored, and should be prioritised for study and conservation.</p>
</abstract>
<kwd-group xml:lang="en">
<title>Keywords</title>
<kwd>Adaptations</kwd>
<kwd>Conservation</kwd>
<kwd>Edaphic endemism</kwd>
<kwd>Edaphic flora</kwd>
<kwd>Extreme environments</kwd>
<kwd>Geobotany</kwd>
<kwd>Plant–soil relations</kwd>
<kwd>Serpentine vegetation</kwd>
<kwd>Ultramafic plants</kwd>
<kwd>Metal hyperaccumulators</kwd>
</kwd-group>
<funding-group>
<award-group>
<funding-source>
<institution-wrap>
<institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100000923</institution-id>
<institution>Australian Research Council</institution>
</institution-wrap>
</funding-source>
<award-id>DE160100429</award-id>
<principal-award-recipient>
<name>
<surname>van der Ent</surname>
<given-names>A.</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group>
<funding-source>
<institution>Fulbright US Scholar Program</institution>
</funding-source>
</award-group>
</funding-group>
<custom-meta-group>
<custom-meta>
<meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2017</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
<body>
<sec id="Sec1">
<title>Background</title>
<p>Ultramafic soils are weathered products of lithologies, such as peridotite and serpentinite bedrock, consisting predominantly of ferromagnesian silicate minerals (Cardace et al.
<xref ref-type="bibr" rid="CR47">2014</xref>
; Moores
<xref ref-type="bibr" rid="CR125">2011</xref>
). Ultramafic soils are generally deficient in essential plant mineral nutrients (phosphorus, potassium), have major cation imbalances (low calcium-to-magnesium molar ratios), and have high concentrations of certain phytotoxic elements, including nickel, cobalt and manganese (Brady et al.
<xref ref-type="bibr" rid="CR34">2005</xref>
; Kazakou et al.
<xref ref-type="bibr" rid="CR98">2008</xref>
; O’Dell and Rajakaruna
<xref ref-type="bibr" rid="CR136">2011</xref>
). Tropical ultramafic soils, unlike those in temperate regions (Alexander
<xref ref-type="bibr" rid="CR6">2009</xref>
; Alexander and DuShey
<xref ref-type="bibr" rid="CR7">2011</xref>
), can be strongly weathered due to rainfall intensity and high temperature, and depending on elevation, can develop as laterites (e.g. Ferralsols) (Kruckeberg
<xref ref-type="bibr" rid="CR107">2002</xref>
; Mandal et al.
<xref ref-type="bibr" rid="CR115">2015</xref>
; van der Ent et al.
<xref ref-type="bibr" rid="CR218">2013a</xref>
; Vithanage et al.
<xref ref-type="bibr" rid="CR234">2014</xref>
).</p>
<p>Depauperate ultramafic soils may generate selective pressures promoting speciation and the evolution of ultramafic endemism (Anacker
<xref ref-type="bibr" rid="CR10">2014</xref>
; Kay et al.
<xref ref-type="bibr" rid="CR97">2011</xref>
; Rajakaruna
<xref ref-type="bibr" rid="CR164">2004</xref>
), often leading to distinctive plant communities worldwide (Anacker
<xref ref-type="bibr" rid="CR9">2011</xref>
; Brooks
<xref ref-type="bibr" rid="CR39">1987</xref>
). The biota of ultramafic soils has contributed greatly to the development of ecological and evolutionary theory (Harrison and Rajakaruna
<xref ref-type="bibr" rid="CR79">2011</xref>
; Strauss and Cacho
<xref ref-type="bibr" rid="CR198">2013</xref>
) and to the study of the genetics of adaptation and speciation (Brady et al.
<xref ref-type="bibr" rid="CR34">2005</xref>
; Palm and Van Volkenburgh
<xref ref-type="bibr" rid="CR143">2014</xref>
; von Wettberg and Wright
<xref ref-type="bibr" rid="CR235">2011</xref>
). Ultramafic floras are, however, threatened by deforestation, agricultural development, mining, and climate change-associated stressors (Boyd et al.
<xref ref-type="bibr" rid="CR33">2009</xref>
; Harrison et al.
<xref ref-type="bibr" rid="CR80">2009</xref>
; Rajakaruna and Boyd
<xref ref-type="bibr" rid="CR167">2008</xref>
; Vallano et al.
<xref ref-type="bibr" rid="CR210">2012</xref>
). These threats to ultramafic biota provide opportunities for conservation and restoration-oriented research (Elam et al.
<xref ref-type="bibr" rid="CR64">1998</xref>
; O’Dell and Claassen
<xref ref-type="bibr" rid="CR135">2011</xref>
; Weiss
<xref ref-type="bibr" rid="CR238">1999</xref>
; Whiting et al.
<xref ref-type="bibr" rid="CR240">2004</xref>
; Wolf
<xref ref-type="bibr" rid="CR243">2001</xref>
).</p>
<p>South and Southeast Asia contain several globally significant biodiversity hotspots (Mittermeier et al.
<xref ref-type="bibr" rid="CR121">2005</xref>
), including areas in Indo-Burma, Philippines, Sundaland (western half of the Indo-Malayan archipelago), and Western Ghats and Sri Lanka. The Borneo lowlands is the only ecoregion globally to surpass 10,000 plant species (Kier et al.
<xref ref-type="bibr" rid="CR101">2005</xref>
) and North Borneo is one of the top five biodiversity centres in the world (Barthlott et al.
<xref ref-type="bibr" rid="CR22">2007</xref>
). Despite South and Southeast Asia harboring several important biodiversity hotspots, the influence of edaphic factors on biodiversity is largely unknown (van der Ent et al.
<xref ref-type="bibr" rid="CR222">2015a</xref>
). Compared to research on ultramafic outcrops in temperate and Mediterranean regions (Alexander et al.
<xref ref-type="bibr" rid="CR8">2007</xref>
; Rajakaruna et al.
<xref ref-type="bibr" rid="CR169">2009</xref>
), ultramafic geoecology in this part of the world is also substantially understudied (Proctor
<xref ref-type="bibr" rid="CR151">1992</xref>
,
<xref ref-type="bibr" rid="CR152">2003</xref>
). In terms of tropical regions, most research related to ultramafic floras to date has focussed on New Caledonia (Isnard et al.
<xref ref-type="bibr" rid="CR89">2016</xref>
; Jaffré et al.
<xref ref-type="bibr" rid="CR93">2010</xref>
,
<xref ref-type="bibr" rid="CR94">2013</xref>
; Pillon et al.
<xref ref-type="bibr" rid="CR148">2010</xref>
; Pillon
<xref ref-type="bibr" rid="CR147">2012</xref>
). Although ultramafic outcrops of New Caledonia are of a similar latitude and general climate to South and Southeast Asia, the evolutionary histories of its flora and fauna are distinct. New Caledonia is on the east of the Lydekker’s Line, which separates the eastern edge of Wallacea from the Australian Region (which lies on the Sahul Shelf), marking a distinct change in floristic affinities. In this review, we also exclude New Guinea (Indonesian West Papua and Papua New Guinea) for the same reason, but note that despite the concomitant occurrence of ultramafic outcrops and exceptionally high biodiversity, virtually nothing is known about the ultramafic geoecology of this island. Research on the floristics and ecology of the understudied ultramafics of South and Southeast Asia is critical to provide a comprehensive assessment of the ultramafic geoecology of tropical Asia.</p>
<p>This review examines the literature on the geoecology of ultramafic areas in South and Southeast Asia, covering India, Pakistan, and Sri Lanka to the west, Myanmar and Cambodia to the north, and Malaysia, Indonesia (excluding West Papua), and the Philippines to the east (Fig. 
<xref rid="Fig1" ref-type="fig">1</xref>
; Table 
<xref rid="Tab1" ref-type="table">1</xref>
); all of which lie on the western side of Lydekker’s line and share a similar climate. We focus on (i) soil–plant relations, including studies on floristic diversity, soil–plant elemental relations, and soil microbes; (ii) ecological aspects, including studies on vegetation structure and composition and plant endemism; (iii) cross-kingdom interactions, including studies on herbivory, mycorrhizal associations, and invertebrate diversity; (iv) evolutionary aspects; (v) physiology and genetics; (vi) phytotechnologies; and finally, (vii) threats and conservation. We conclude the review by highlighting countries within South and Southeast Asia requiring further study, drawing attention to major gaps in knowledge.
<fig id="Fig1">
<label>Fig. 1</label>
<caption>
<p>Map of South and Southeast Asia showing the distribution of ultramafic outcrops in the region.
<italic>Bottom inset</italic>
is a more detailed outline of ultramafic outcrops in Borneo, Palawan, Mindanao, Sulawesi, and Halmahera. Not all regions of India have complete geologic surveys, and we were unable to locate precise information about ultramafic outcrops in Burma and Laos. The ultramafic outcrop location in Northern Thailand is approximate. The extent of each outcrop shown is not to scale</p>
<p>[Figure compiled with data from Central Energy Resources Team (
<xref ref-type="bibr" rid="CR48">1999</xref>
), Datta et al. (
<xref ref-type="bibr" rid="CR57">2015</xref>
), Kfayatullah et al. (
<xref ref-type="bibr" rid="CR99">2001</xref>
), Shi et al. (
<xref ref-type="bibr" rid="CR190">2012</xref>
), Baker et al. (
<xref ref-type="bibr" rid="CR16">1992</xref>
), Van der Ent et al. (
<xref ref-type="bibr" rid="CR218">2013a</xref>
,
<xref ref-type="bibr" rid="CR222">2015a</xref>
), Tan and Khoo (
<xref ref-type="bibr" rid="CR200">1993</xref>
), MacDonald and Barr (
<xref ref-type="bibr" rid="CR114">1984</xref>
), Geological Survey of India, Geological and Mineral Maps of States and Regions (
<ext-link ext-link-type="uri" xlink:href="http://www.portal.gsi.gov.in/portal/page%3F_pageid=127%2C603606%26_dad%3Dportal%26_schema%3DPORTAL">http://www.portal.gsi.gov.in/portal/page?_pageid=127,603606&_dad=portal&_schema=PORTAL</ext-link>
), and OneGeology Portal (
<ext-link ext-link-type="uri" xlink:href="http://portal.onegeology.org/OnegeologyGlobal/">http://portal.onegeology.org/OnegeologyGlobal/</ext-link>
)]</p>
</caption>
<graphic xlink:href="40529_2017_167_Fig1_HTML" id="MO1"></graphic>
</fig>
<table-wrap id="Tab1">
<label>Table 1</label>
<caption>
<p>A summary of geoecological studies conducted on ultramafic outcrops in South and Southeast Asia</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th align="left">Country</th>
<th align="left">Area of study</th>
<th align="left">References</th>
</tr>
</thead>
<tbody>
<tr>
<td align="left" rowspan="10">India</td>
<td align="left">Bioremediation of chromite mines and nickel recovery by fungi</td>
<td align="left">Acharya et al. (
<xref ref-type="bibr" rid="CR1">1998</xref>
), Biswas et al. (
<xref ref-type="bibr" rid="CR28">2013</xref>
), Bohidar et al. (
<xref ref-type="bibr" rid="CR29">2009</xref>
), Ghosh and Paul (
<xref ref-type="bibr" rid="CR74">2015</xref>
), Mishra et al. (
<xref ref-type="bibr" rid="CR119">2009</xref>
)</td>
</tr>
<tr>
<td align="left">Discovery of nickel hyperaccumulators</td>
<td align="left">Datta et al. (
<xref ref-type="bibr" rid="CR57">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Forest vegetation structure</td>
<td align="left">Prasad et al. (
<xref ref-type="bibr" rid="CR150">2007</xref>
)</td>
</tr>
<tr>
<td align="left">Heavy metal leaching into groundwater</td>
<td align="left">Dhakate and Singh (
<xref ref-type="bibr" rid="CR60">2008</xref>
)</td>
</tr>
<tr>
<td align="left">Heavy metal tolerance in ultramafic soil-associated microbes</td>
<td align="left">Pal et al. (
<xref ref-type="bibr" rid="CR139">2004</xref>
,
<xref ref-type="bibr" rid="CR140">2005</xref>
,
<xref ref-type="bibr" rid="CR141">2006</xref>
,
<xref ref-type="bibr" rid="CR142">2007</xref>
), Pal and Paul (
<xref ref-type="bibr" rid="CR138">2012</xref>
)</td>
</tr>
<tr>
<td align="left">Origin and serpentinization of ultramafic rocks in the Indo-Myanmar subduction zone</td>
<td align="left">Ningthoujam et al. (
<xref ref-type="bibr" rid="CR133">2012</xref>
), Soibam et al. (
<xref ref-type="bibr" rid="CR193">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Phytoremediation of and bioaccumulation of metals from chromite mines</td>
<td align="left">Mohanty et al. (
<xref ref-type="bibr" rid="CR123">2011</xref>
,
<xref ref-type="bibr" rid="CR124">2012</xref>
)</td>
</tr>
<tr>
<td align="left">Plant–soil elemental relations on a chromite mine</td>
<td align="left">Samantaray et al. (
<xref ref-type="bibr" rid="CR178">2001</xref>
)</td>
</tr>
<tr>
<td align="left">Remote sensing for detecting and mapping ultramafic vegetation</td>
<td align="left">Chaudhury et al. (
<xref ref-type="bibr" rid="CR52">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Ultramafic geology, geochemisty, mineral prospecting</td>
<td align="left">Banerjee (
<xref ref-type="bibr" rid="CR21">1972</xref>
), Chakraborty and Chakraborty (
<xref ref-type="bibr" rid="CR49">1984</xref>
), Bhatta and Ghosh (
<xref ref-type="bibr" rid="CR27">2014</xref>
), Mandal et al. (
<xref ref-type="bibr" rid="CR115">2015</xref>
), Mitra (
<xref ref-type="bibr" rid="CR120">1973</xref>
)</td>
</tr>
<tr>
<td align="left" rowspan="5">Indonesia</td>
<td align="left">Acidification of serpentinite-derived soils</td>
<td align="left">Fujii et al. (
<xref ref-type="bibr" rid="CR72">2011</xref>
)</td>
</tr>
<tr>
<td align="left">Floristics and plant community structure</td>
<td align="left">Proctor et al. (
<xref ref-type="bibr" rid="CR157">1994</xref>
), van Balgooy and Tantra (
<xref ref-type="bibr" rid="CR211">1986</xref>
)</td>
</tr>
<tr>
<td align="left">Geochemistry, petrography and thermobarometry of the ultramafics</td>
<td align="left">Linthout and Helmers (
<xref ref-type="bibr" rid="CR112">1994</xref>
)</td>
</tr>
<tr>
<td align="left">Nickel hyperaccumulators and phytotechnologies</td>
<td align="left">Netty et al. (
<xref ref-type="bibr" rid="CR131">2012</xref>
), van der Ent et al. (
<xref ref-type="bibr" rid="CR218">2013a</xref>
)</td>
</tr>
<tr>
<td align="left">Species discovery on ultramafic soils</td>
<td align="left">Cheek (
<xref ref-type="bibr" rid="CR53">2015</xref>
)</td>
</tr>
<tr>
<td align="left" rowspan="8">Malaysia</td>
<td align="left">Copper accumulation in ultramafic plants</td>
<td align="left">van der Ent and Reeves (
<xref ref-type="bibr" rid="CR213">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Discovery of nickel hyperaccumulators</td>
<td align="left">Hoffmann et al. (
<xref ref-type="bibr" rid="CR86">2003</xref>
), van der Ent and Mulligan (
<xref ref-type="bibr" rid="CR212">2015</xref>
), van der Ent et al. (
<xref ref-type="bibr" rid="CR219">2013b</xref>
,
<xref ref-type="bibr" rid="CR230">2016b</xref>
,
<xref ref-type="bibr" rid="CR231">c</xref>
)</td>
</tr>
<tr>
<td align="left">Ecology of nickel hyperaccumulators: nickel insects</td>
<td align="left">van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Floristics, plant–soil relations, ultramafic endemism</td>
<td align="left">Chen et al. (
<xref ref-type="bibr" rid="CR54">2014</xref>
), Fowlie (
<xref ref-type="bibr" rid="CR71">1985</xref>
), Peng et al. (
<xref ref-type="bibr" rid="CR145">2015</xref>
), Proctor et al. (
<xref ref-type="bibr" rid="CR154">1988a</xref>
,
<xref ref-type="bibr" rid="CR155">b</xref>
,
<xref ref-type="bibr" rid="CR156">1989</xref>
), Sugau and van der Ent (
<xref ref-type="bibr" rid="CR199">2016</xref>
), van der Ent and Wood (
<xref ref-type="bibr" rid="CR217">2013</xref>
), Wood and van der Ent (
<xref ref-type="bibr" rid="CR246">2012</xref>
), Wong and van der Ent (
<xref ref-type="bibr" rid="CR245">2014</xref>
), van der Ent and Wong (
<xref ref-type="bibr" rid="CR215">2015</xref>
), van der Ent and Vanijajiva (
<xref ref-type="bibr" rid="CR214">2014</xref>
)</td>
</tr>
<tr>
<td align="left">Metal localization; nuclear microprobe imaging analyses</td>
<td align="left">Mesjasz-Przybylowicz et al. (
<xref ref-type="bibr" rid="CR117">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Ultramafic forest vegetation structure, plant ecology, community ecology</td>
<td align="left">Adam (
<xref ref-type="bibr" rid="CR2">2002</xref>
), Aiba et al. (
<xref ref-type="bibr" rid="CR5">2015</xref>
), Aiba and Kitayama (
<xref ref-type="bibr" rid="CR4">1999</xref>
), Brearley (
<xref ref-type="bibr" rid="CR36">2005</xref>
), Bruijnzeel et al. (
<xref ref-type="bibr" rid="CR45">1993</xref>
), Kitayama (
<xref ref-type="bibr" rid="CR103">1992</xref>
), Proctor et al. (
<xref ref-type="bibr" rid="CR154">1988a</xref>
,
<xref ref-type="bibr" rid="CR155">b</xref>
), Sawada et al. (
<xref ref-type="bibr" rid="CR182">2015</xref>
), Tashakor et al. (
<xref ref-type="bibr" rid="CR202">2013</xref>
), van der Ent et al. (
<xref ref-type="bibr" rid="CR222">2015a</xref>
,
<xref ref-type="bibr" rid="CR223">b</xref>
,
<xref ref-type="bibr" rid="CR227">f</xref>
,
<xref ref-type="bibr" rid="CR229">2016a</xref>
)</td>
</tr>
<tr>
<td align="left">Ultramafic geochemistry</td>
<td align="left">Tashakor et al. (
<xref ref-type="bibr" rid="CR201">2011</xref>
,
<xref ref-type="bibr" rid="CR202">2013</xref>
)</td>
</tr>
<tr>
<td align="left">Ultramafic plant–other biota interactions</td>
<td align="left">Wells et al. (
<xref ref-type="bibr" rid="CR239">2011</xref>
)</td>
</tr>
<tr>
<td align="left"></td>
<td align="left">Ultramafic-associated insects and soil invertebrates</td>
<td align="left">Chung et al. (
<xref ref-type="bibr" rid="CR55">2013</xref>
), Hasegawa et al. (
<xref ref-type="bibr" rid="CR81">2006</xref>
), Jones et al. (
<xref ref-type="bibr" rid="CR96">2010</xref>
), Leakey and Proctor (
<xref ref-type="bibr" rid="CR110">1987</xref>
)</td>
</tr>
<tr>
<td align="left">Myanmar</td>
<td align="left">Mineralogy of jadeitite and related rocks, including serpentinites</td>
<td align="left">Shi et al. (
<xref ref-type="bibr" rid="CR190">2012</xref>
)</td>
</tr>
<tr>
<td align="left">Pakistan</td>
<td align="left">Ultramafic geochemistry and soil–plant metal relations</td>
<td align="left">Kfayatullah et al. (
<xref ref-type="bibr" rid="CR99">2001</xref>
), Naseem et al. (
<xref ref-type="bibr" rid="CR129">2009</xref>
), Shah et al. (
<xref ref-type="bibr" rid="CR187">2010</xref>
,
<xref ref-type="bibr" rid="CR188">2014</xref>
)</td>
</tr>
<tr>
<td align="left" rowspan="7">Philippines</td>
<td align="left">Discovery of Ni hyperaccumulators</td>
<td align="left">Baker et al. (
<xref ref-type="bibr" rid="CR16">1992</xref>
), Fernando et al. (
<xref ref-type="bibr" rid="CR69">2014</xref>
), Gotera et al. (
<xref ref-type="bibr" rid="CR77">2014</xref>
), Hoffmann et al. (
<xref ref-type="bibr" rid="CR86">2003</xref>
), Quimado et al. (
<xref ref-type="bibr" rid="CR163">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Herbivory on ultramafic soils</td>
<td align="left">Proctor et al. (
<xref ref-type="bibr" rid="CR161">2000a</xref>
)</td>
</tr>
<tr>
<td align="left">Metal tolerance in mycorrhizal fungi of ultramafic soils</td>
<td align="left">Aggangan et al. (
<xref ref-type="bibr" rid="CR3">1998</xref>
)</td>
</tr>
<tr>
<td align="left">Phytomining considerations</td>
<td align="left">Fernando et al. (
<xref ref-type="bibr" rid="CR68">2013</xref>
)</td>
</tr>
<tr>
<td align="left">Species discovery on ultramafic soils</td>
<td align="left">Argent et al. (
<xref ref-type="bibr" rid="CR14">2007</xref>
), Fernando and Rodda (
<xref ref-type="bibr" rid="CR66">2013</xref>
), Fleischmann et al. (
<xref ref-type="bibr" rid="CR70">2011</xref>
)</td>
</tr>
<tr>
<td align="left">Ultramafic forest vegetation structure and soil–plant relations</td>
<td align="left">Bruijnzeel (
<xref ref-type="bibr" rid="CR44">1990</xref>
), Proctor et al. (
<xref ref-type="bibr" rid="CR158">1997</xref>
,
<xref ref-type="bibr" rid="CR159">1998</xref>
,
<xref ref-type="bibr" rid="CR160">1999</xref>
,
<xref ref-type="bibr" rid="CR162">2000b</xref>
)</td>
</tr>
<tr>
<td align="left">Ultramafic soil and forest litter invertebrates</td>
<td align="left">Thomas and Proctor (
<xref ref-type="bibr" rid="CR205">1997</xref>
)</td>
</tr>
<tr>
<td align="left" rowspan="5">Sri Lanka</td>
<td align="left">Antimicrobial activities of ultramafic-associated plants</td>
<td align="left">Rajakaruna et al. (
<xref ref-type="bibr" rid="CR168">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Ecotypic differentiation of ultramafic taxa</td>
<td align="left">Chathuranga et al. (
<xref ref-type="bibr" rid="CR51">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Phyto- and bio-remediation of ultramafic soils; soil remediation</td>
<td align="left">Bandara et al. (
<xref ref-type="bibr" rid="CR20">2017</xref>
), Herath et al. (
<xref ref-type="bibr" rid="CR82">2014</xref>
), Kumarathilaka et al. (
<xref ref-type="bibr" rid="CR108">2016</xref>
), Seneviratne et al. (
<xref ref-type="bibr" rid="CR185">2016a</xref>
,
<xref ref-type="bibr" rid="CR186">b</xref>
)</td>
</tr>
<tr>
<td align="left">Soil–plant relations including floristics, soil–plant elemental relations, discovery of nickel and copper hyperaccumulators</td>
<td align="left">Brooks (
<xref ref-type="bibr" rid="CR39">1987</xref>
), Rajakaruna and Baker (
<xref ref-type="bibr" rid="CR165">2004</xref>
), Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
), Samithri (
<xref ref-type="bibr" rid="CR180">2015</xref>
), Senevirathne et al. (
<xref ref-type="bibr" rid="CR181">2000</xref>
), Weerasinghe and Iqbal (
<xref ref-type="bibr" rid="CR237">2011</xref>
)</td>
</tr>
<tr>
<td align="left">Ultramafic geology and geochemistry</td>
<td align="left">Dissanayaka (
<xref ref-type="bibr" rid="CR61">1982</xref>
), Dissanayake and Van Riel (
<xref ref-type="bibr" rid="CR62">1978</xref>
), Munasinghe and Dissanayake (
<xref ref-type="bibr" rid="CR127">1980</xref>
), Hewawasam et al. (
<xref ref-type="bibr" rid="CR83">2014</xref>
), Rajapaksha et al. (
<xref ref-type="bibr" rid="CR171">2012</xref>
,
<xref ref-type="bibr" rid="CR172">2013</xref>
), Ranasinghe (
<xref ref-type="bibr" rid="CR173">1987</xref>
), Tennakoon et al. (
<xref ref-type="bibr" rid="CR203">2007</xref>
), Vithanage et al. (
<xref ref-type="bibr" rid="CR234">2014</xref>
)</td>
</tr>
<tr>
<td align="left">Southeast Asia: Regional Overviews</td>
<td align="left">Floristics, plant–soil elemental relations, metal accumulators, quantitative bedrock (including ultramafic) geology of Southeast Asia</td>
<td align="left">Brooks (
<xref ref-type="bibr" rid="CR39">1987</xref>
), Brooks et al. (
<xref ref-type="bibr" rid="CR41">1977a</xref>
,
<xref ref-type="bibr" rid="CR42">b</xref>
), Brooks and Wither (
<xref ref-type="bibr" rid="CR40">1977</xref>
), Peucker-Ehrenbrink and Miller (
<xref ref-type="bibr" rid="CR146">2004</xref>
), Proctor (
<xref ref-type="bibr" rid="CR151">1992</xref>
,
<xref ref-type="bibr" rid="CR152">2003</xref>
), Reeves (
<xref ref-type="bibr" rid="CR174">2003</xref>
), van der Ent et al. (
<xref ref-type="bibr" rid="CR225">2015c</xref>
,
<xref ref-type="bibr" rid="CR225">d</xref>
), Wither and Brooks (
<xref ref-type="bibr" rid="CR242">1977</xref>
)</td>
</tr>
<tr>
<td align="left">Thailand</td>
<td align="left">Petrography and geochemistry of ultramafic rocks</td>
<td align="left">Hisada et al. (
<xref ref-type="bibr" rid="CR84">2004</xref>
), Macdonald and Barr (
<xref ref-type="bibr" rid="CR114">1984</xref>
), Orberger et al. (
<xref ref-type="bibr" rid="CR137">1995</xref>
)</td>
</tr>
<tr>
<td align="left">Vietnam</td>
<td align="left">Heavy metal (Cr, Ni, Co) leaching from chromite mine</td>
<td align="left">Kien et al. (
<xref ref-type="bibr" rid="CR100">2010</xref>
)</td>
</tr>
<tr>
<td align="left"></td>
<td align="left">Ultramafic geology</td>
<td align="left">Thanh et al. (
<xref ref-type="bibr" rid="CR204">2014</xref>
)</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<p>Information within columns organized in alphabetical order</p>
</table-wrap-foot>
</table-wrap>
</p>
</sec>
<sec id="Sec2">
<title>Soil–plant relations</title>
<p>Ultramafic soils worldwide share a distinct suite of chemical and physical features (Rajakaruna et al.
<xref ref-type="bibr" rid="CR169">2009</xref>
); however, tropical ultramafic soils may differ in elemental content, moisture, organic matter content, and soil pedology (Kierczak et al.
<xref ref-type="bibr" rid="CR102">2007</xref>
; Vithanage et al.
<xref ref-type="bibr" rid="CR234">2014</xref>
), compared to those in temperate and Mediterranean regions (Alexander
<xref ref-type="bibr" rid="CR6">2009</xref>
; Alexander et al.
<xref ref-type="bibr" rid="CR8">2007</xref>
). Table 
<xref rid="Tab2" ref-type="table">2</xref>
lists key soil properties of ultramafic soils from South and Southeast Asia, focusing on pH, Ca:Mg molar ratio, Ni, Cr, and the major nutrients, P and K. Plants growing on ultramafic soils have to contend with a suite of edaphic stressors, including low nutrient content, high levels of phytotoxic elements, and, at times, water stress (Brady et al.
<xref ref-type="bibr" rid="CR34">2005</xref>
). Plants and soil microbes of ultramafic soils tolerate these edaphic stressors via efficient uptake of essential nutrients, and exclusion of, or conversely accumulation and localization of high concentrations, of certain phytotoxic elements, among other adaptations (see Palm and Van Volkenburgh
<xref ref-type="bibr" rid="CR143">2014</xref>
for a discussion).
<table-wrap id="Tab2">
<label>Table 2</label>
<caption>
<p>Selected soil chemical properties of ultramafic outcrops in South and Southeast Asia</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th align="left">Country</th>
<th align="left">Altitude (masl)</th>
<th align="left">pH</th>
<th align="left">Ca:Mg</th>
<th align="left">Ca (exch.) cmol (+) kg
<sup>−1</sup>
</th>
<th align="left">Mg (exch.) cmol (+) kg
<sup>−1</sup>
</th>
<th align="left">K (exch.) cmol (+) kg
<sup>−1</sup>
</th>
<th align="left">K (μg g
<sup>−1</sup>
)</th>
<th align="left">P (μg g
<sup>−1</sup>
)</th>
<th align="left">P (extract.) μg g
<sup>−1</sup>
</th>
<th align="left">Ni (μg g
<sup>−1</sup>
)</th>
<th align="left">Ni (extract.) μg g
<sup>−1</sup>
</th>
<th align="left">References</th>
</tr>
</thead>
<tbody>
<tr>
<td align="left">Sulawesi, Indonesia</td>
<td align="left"></td>
<td align="left">5.3–6.3</td>
<td align="left">0.9–5.7</td>
<td align="left">4.6–13.3</td>
<td align="left">11.1–26.2</td>
<td align="left">0.05–0.5</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">825–4050</td>
<td align="left"></td>
<td align="left">Parry (
<xref ref-type="bibr" rid="CR144">1985</xref>
)</td>
</tr>
<tr>
<td align="left">Sulawesi, Indonesia</td>
<td align="left">200–300</td>
<td align="left">5.8–7.0</td>
<td align="left">0.1–1.6</td>
<td align="left">0.2–1.6</td>
<td align="left">0.5–4.6</td>
<td align="left">0.01–0.1</td>
<td align="left">3281–6260</td>
<td align="left">14.4–237</td>
<td align="left">0.23–3.87</td>
<td align="left">3730–10,524</td>
<td align="left">2.1–30.2</td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR218">2013a</xref>
)</td>
</tr>
<tr>
<td align="left">Talaud Island, Indonesia</td>
<td align="left">60–500</td>
<td align="left">6.1–6.4</td>
<td align="left">1.6–32</td>
<td align="left">0.9–16</td>
<td align="left">13.9–27.3</td>
<td align="left">0.19–0.38</td>
<td align="left"></td>
<td align="left"></td>
<td align="left">0.94–6.8</td>
<td align="left"></td>
<td align="left">8.5–37</td>
<td align="left">Proctor et al. (
<xref ref-type="bibr" rid="CR157">1994</xref>
)</td>
</tr>
<tr>
<td align="left">Sibuyan Island, Philippines</td>
<td align="left">325–1540</td>
<td align="left">4.3–5.5</td>
<td align="left">0.3–2.9</td>
<td align="left">0.5–3.4</td>
<td align="left">0.75–3.64</td>
<td align="left">0.04–0.41</td>
<td align="left"></td>
<td align="left"></td>
<td align="left">0.41–2.07</td>
<td align="left"></td>
<td align="left">1–24</td>
<td align="left">Proctor et al. (
<xref ref-type="bibr" rid="CR159">1998</xref>
)</td>
</tr>
<tr>
<td align="left">Palawan, Philippines</td>
<td align="left">50</td>
<td align="left">6.8</td>
<td align="left">0.24</td>
<td align="left">4.27</td>
<td align="left">18.1</td>
<td align="left">0.32</td>
<td align="left"></td>
<td align="left"></td>
<td align="left">1.02</td>
<td align="left">6900</td>
<td align="left">360</td>
<td align="left">Proctor et al. (
<xref ref-type="bibr" rid="CR160">1999</xref>
)</td>
</tr>
<tr>
<td align="left">Sabah, Malaysia</td>
<td align="left">400–2900</td>
<td align="left">3.8–9.7</td>
<td align="left">0.1–136</td>
<td align="left">0.003–35</td>
<td align="left">0.02–76</td>
<td align="left">0.002–0.79</td>
<td align="left">0.1–1056</td>
<td align="left">4.4–585</td>
<td align="left">0.1–32</td>
<td align="left">17–9308</td>
<td align="left">0.17–442</td>
<td align="left">Van der Ent (unpublished)</td>
</tr>
<tr>
<td align="left">Sabah, Malaysia</td>
<td align="left">180</td>
<td align="left">5.3</td>
<td align="left">0.62</td>
<td align="left">0.86</td>
<td align="left">1.38</td>
<td align="left">0.17</td>
<td align="left"></td>
<td align="left">201</td>
<td align="left">0.34</td>
<td align="left">2980</td>
<td align="left">10.8</td>
<td align="left">Brearley (
<xref ref-type="bibr" rid="CR36">2005</xref>
)</td>
</tr>
<tr>
<td align="left">Sabah, Malaysia</td>
<td align="left">280</td>
<td align="left">5.7</td>
<td align="left">0.31</td>
<td align="left">7.7</td>
<td align="left">24.6</td>
<td align="left">0.14</td>
<td align="left"></td>
<td align="left"></td>
<td align="left">4.1</td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Proctor et al. (
<xref ref-type="bibr" rid="CR154">1988a</xref>
)</td>
</tr>
<tr>
<td align="left">Ussangoda, Sri Lanka</td>
<td align="left">15–20</td>
<td align="left">5.3–6.2 (4.3–4.9)</td>
<td align="left">0.6–1.9 (1.4–2.4)</td>
<td align="left">187–905
<sup>a</sup>
(112–212)</td>
<td align="left">311–456
<sup>a</sup>
(60–122)</td>
<td align="left"></td>
<td align="left">140–321 (163–350)</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">101–151 (29–65)</td>
<td align="left">Weerasinghe and Iqbal (
<xref ref-type="bibr" rid="CR237">2011</xref>
), Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Ginigalpalessa, Sri Lanka</td>
<td align="left">70–80</td>
<td align="left">5.7–7.4</td>
<td align="left">0.1–0.6</td>
<td align="left">180–1580
<sup>a</sup>
</td>
<td align="left">2400–3400
<sup>a</sup>
</td>
<td align="left"></td>
<td align="left">70–230</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">15–180</td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Indikolapalessa, Sri Lanka</td>
<td align="left">70–80</td>
<td align="left">4.7–6.1</td>
<td align="left">0.2–2.6</td>
<td align="left">395–1863
<sup>a</sup>
</td>
<td align="left">613–2625
<sup>a</sup>
</td>
<td align="left"></td>
<td align="left">78–1563</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">4–148</td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Yodhagannawa, Sri Lanka</td>
<td align="left">90–100</td>
<td align="left">5.1–5.7</td>
<td align="left">0.1–0.2</td>
<td align="left">123–138
<sup>a</sup>
</td>
<td align="left">838–1000
<sup>a</sup>
</td>
<td align="left"></td>
<td align="left">53–75</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">47–79</td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Andaman, India</td>
<td align="left">50–732</td>
<td align="left">6.0–6.8</td>
<td align="left"></td>
<td align="left"></td>
<td align="left">2300–3600
<sup>a</sup>
</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">3370–9030</td>
<td align="left">397–913</td>
<td align="left">Pal et al. (
<xref ref-type="bibr" rid="CR142">2007</xref>
)</td>
</tr>
<tr>
<td align="left">Andaman, India</td>
<td align="left">50–732</td>
<td align="left">4.4–7.1</td>
<td align="left"></td>
<td align="left"></td>
<td align="left">2.8–3.9
<sup>b</sup>
</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">244–10,107</td>
<td align="left">192–907</td>
<td align="left">Datta et al. (
<xref ref-type="bibr" rid="CR57">2015</xref>
)</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<p>Units are listed under each soil variable except for values with superscripts:
<sup>a</sup>
 μg g
<sup>−1</sup>
;
<sup>b</sup>
 %</p>
</table-wrap-foot>
</table-wrap>
</p>
<sec id="Sec3">
<title>Plant diversity and soil–plant elemental profiles</title>
<p>In Sukinda, India, chromite mine spoils composed of ultramafic substrates have Ni ranging from 187 to 215 µg g
<sup>−1</sup>
and Ca:Mg molar ratios of 1.69–2.27; from which, in total, 113 plant species belonging to 51 families have been recorded (Samantaray et al.
<xref ref-type="bibr" rid="CR178">2001</xref>
). Some species which colonize the substrate exhibit traits typical of plants adapted to ultramafic soils, including sclerophyllous and microphyllous leaves (Brady et al.
<xref ref-type="bibr" rid="CR34">2005</xref>
), but individual plants also show chlorosis, leaf curling, and necrosis.</p>
<p>On the Andaman Islands, India, ultramafic soils with high Ni concentrations (2700–10,100 μg g
<sup>−1</sup>
) harbor eight Ni hyperaccumulator plant species belonging to eight different genera and seven different families (Datta et al.
<xref ref-type="bibr" rid="CR57">2015</xref>
). Of these,
<italic>Dichapetalum gelonioides</italic>
subsp.
<italic>andamanicum</italic>
(Dichapetalaceae) and
<italic>Rinorea bengalensis</italic>
(Violaceae) accumulated up to 30,000 μg g
<sup>−1</sup>
Ni. There is substantial potential for using remote sensing tools to examine the vegetation communities on the ultramafics of the Andaman Islands, where the ultramafic outcrops are mostly inaccessible and the vegetation deserves more intensive exploration (Chaudhury et al.
<xref ref-type="bibr" rid="CR52">2015</xref>
).</p>
<p>In Northern Pakistan, the ultramafics of Mingora and Kabal in the Swat region include assemblages of serpentinite, green schist, talc-carbonate schist, and metabasalts in the Mingora–Shangla mélange zone (Shah et al.
<xref ref-type="bibr" rid="CR187">2010</xref>
). Relatively high accumulation of Ni and Cr has been recorded in the plant tissue of
<italic>Indigofera gerardiana</italic>
(Fabaceae),
<italic>Saccharum griffithii</italic>
(Poaceae),
<italic>Lycopersicon esculentum</italic>
(Solanaceae), and
<italic>Chrysopogon zizanioides</italic>
(Poaceae) growing in the Kot Parang Ghar mélange zone in the Bucha Area, Pakistan (Shah et al.
<xref ref-type="bibr" rid="CR187">2010</xref>
,
<xref ref-type="bibr" rid="CR188">2014</xref>
).</p>
<p>In Sri Lanka, ultramafic rocks occur along a Precambrian suture zone at the boundary of the Vijayan and Highland Series, metamorphic remnants of two ancient tectonic plates (Dissanayaka
<xref ref-type="bibr" rid="CR61">1982</xref>
; Munasinghe and Dissanayake
<xref ref-type="bibr" rid="CR127">1980</xref>
). The geochemistry of these outcrops, particularly of Ussangoda along the southern coast, has been well-documented (Hewawasam et al.
<xref ref-type="bibr" rid="CR83">2014</xref>
; Rajapaksha et al.
<xref ref-type="bibr" rid="CR171">2012</xref>
,
<xref ref-type="bibr" rid="CR172">2013</xref>
; Tennakoon et al.
<xref ref-type="bibr" rid="CR203">2007</xref>
; Vithanage et al.
<xref ref-type="bibr" rid="CR234">2014</xref>
). The floristics of the ultramafic outcrops of Sri Lanka, especially of Ussangoda, have also received considerable attention (Brooks
<xref ref-type="bibr" rid="CR39">1987</xref>
; Rajakaruna and Baker
<xref ref-type="bibr" rid="CR165">2004</xref>
; Rajakaruna and Bohm
<xref ref-type="bibr" rid="CR166">2002</xref>
; Rajakaruna et al.
<xref ref-type="bibr" rid="CR168">2002</xref>
; Samithri
<xref ref-type="bibr" rid="CR180">2015</xref>
; Senevirathne et al.
<xref ref-type="bibr" rid="CR181">2000</xref>
; Weerasinghe and Iqbal
<xref ref-type="bibr" rid="CR237">2011</xref>
).</p>
<p>Research suggests that Sri Lanka’s ultramafic flora is impoverished with respect to the total number of plant species and percent proportion of endemic species. To date, 67 plant species belonging to 61 genera and 30 families have been identified from Ussangoda (Samithri
<xref ref-type="bibr" rid="CR180">2015</xref>
). Combined with an additional 40 taxa reported from three other sites surveyed by Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
), the total ultramafic flora of Sri Lanka stands at a mere 107 species, compared to many-fold more documented from other sites in Southeast Asia (van der Ent et al.
<xref ref-type="bibr" rid="CR222">2015a</xref>
). Of the species documented from ultramafic soils, only
<italic>Vernonia zeylanica</italic>
(Asteraceae) is endemic to Sri Lanka (MOE
<xref ref-type="bibr" rid="CR122">2012</xref>
), although the taxon is not restricted to the substrate.</p>
</sec>
<sec id="Sec4">
<title>Soil microbes</title>
<p>Several recent studies, conducted in temperate and Mediterranean regions of the world, explore the roles microbes play in the ecology of ultramafic habitats as well as in the remediation of metal-contaminated soils (Batten et al.
<xref ref-type="bibr" rid="CR25">2006</xref>
; Ma et al.
<xref ref-type="bibr" rid="CR113">2015</xref>
; Schechter and Branco
<xref ref-type="bibr" rid="CR183">2014</xref>
). Although studies on microbial ecology of ultramafic soils in South and Southeast Asia are minimal, Pal et al. (
<xref ref-type="bibr" rid="CR139">2004</xref>
,
<xref ref-type="bibr" rid="CR140">2005</xref>
,
<xref ref-type="bibr" rid="CR141">2006</xref>
,
<xref ref-type="bibr" rid="CR142">2007</xref>
) and Pal and Paul (
<xref ref-type="bibr" rid="CR138">2012</xref>
) have carried out a series of studies on microbial diversity and ecology of ultramafic soils on the Andaman Islands, India. In one of these studies, Pal et al. (
<xref ref-type="bibr" rid="CR140">2005</xref>
) compared physicochemical and microbial properties of ultramafic soils with those from adjacent non-ultramafic localities. The elemental profiles were characteristic of ultramafic soils, with high concentrations of Mg, Ni, Cr, and Co. Furthermore, the ultramafic soils showed low microbial density (6.2–11.3 × 10
<sup>6</sup>
colony forming unit/g soil) and activity (1.7–3.5 µg fluorescein/g dry soil/h) relative to non-ultramafic soils. The ultramafic-associated microbial population (including bacteria and fungi) was dominated by bacteria and was more resistant to metals than populations from non-ultramafic soils. Among the ultramafic isolates, 8 and 11 bacteria tolerated >12.0 mM Ni and >16.0 mM Cr, respectively, while six fungal isolates showed a minimum inhibitory concentration (MIC) value >8.0 mM Co. The ultramafic strains also showed co-resistance to Cu, Zn, and Mn. Pal et al. (
<xref ref-type="bibr" rid="CR142">2007</xref>
) also examined the soil microflora associated with the rhizosphere of two known Ni hyperaccumulators from the Andaman Islands,
<italic>R. bengalensis</italic>
and
<italic>D. gelonioides</italic>
subsp.
<italic>andamanicum</italic>
. Of the total 123 microbes (99 bacteria and 24 fungi) that were isolated, bacteria were more tolerant of Ni than fungi, showing their greater potential for Ni tolerance.</p>
<p>In a study focusing on medicinal qualities of wild-harvested plants, 32 plant species collected from ultramafic outcrops of Sri Lanka were screened for antimicrobial properties (Rajakaruna et al.
<xref ref-type="bibr" rid="CR168">2002</xref>
). Of these, 29 species belonging to 12 families proved effective against at least one microorganism. Photoactivity was also observed from extracts of 10 species belonging to 10 families. There was no observed correlation between trace element hyperaccumulation (Rajakaruna and Bohm
<xref ref-type="bibr" rid="CR166">2002</xref>
) and antimicrobial activity.</p>
</sec>
</sec>
<sec id="Sec5">
<title>Ecological aspects</title>
<p>Ultramafic outcrops have long-provided model settings for studies on the ecology of plant species and plant communities. Studies range from those investigating aspects of the ecology of edaphically specialized plant populations and plant–plant interactions to those exploring factors and mechanisms driving the assembly of plant communities (see Harrison and Rajakaruna
<xref ref-type="bibr" rid="CR79">2011</xref>
). Compared to other regions of the world, ecological studies on ultramafics of South and Southeast Asia are mostly limited to those examining floristics, plant community structure, and edaphic-floristic associations.</p>
<sec id="Sec6">
<title>Vegetation structure and composition</title>
<p>Mount Silam in Sabah, Malaysia, has been extensively studied, including the general floristics, forest structure, hydrology and chemical analysis of tree foliage and leaf litter (Proctor et al.
<xref ref-type="bibr" rid="CR154">1988a</xref>
,
<xref ref-type="bibr" rid="CR155">b</xref>
,
<xref ref-type="bibr" rid="CR156">1989</xref>
; Bruijnzeel et al.
<xref ref-type="bibr" rid="CR45">1993</xref>
). The study plots on Mount Silam range from 280 to 870 masl in elevation, documenting a broad spectrum of vegetation changes with altitude. The site is extremely species-rich in terms of its tree flora, ranging between 19 species in a 0.04-ha plot at 870 masl to 104 species in a 0.4-ha plot at 480 masl (Proctor
<xref ref-type="bibr" rid="CR151">1992</xref>
). Ultramafic-associated rainforests on Mount Guiting-Guiting, Sibuyan Island, Philippines (Proctor et al.
<xref ref-type="bibr" rid="CR159">1998</xref>
) and those of Mount Silam, Sabah (Proctor et al.
<xref ref-type="bibr" rid="CR154">1988a</xref>
,
<xref ref-type="bibr" rid="CR155">b</xref>
) are similar in their soil features (Ni, Ca:Mg, and depth) and lack of stunted lowland forests. At these locations, small-statured forests are associated with higher elevations.</p>
<p>On Mount Bloomfield in the western Philippines (Palawan), Proctor et al. (
<xref ref-type="bibr" rid="CR160">1999</xref>
) described a very different forest structure from those of Mount Silam and Mount Guiting-Guiting. The soil depths on Mount Bloomfield are much less compared to these other sites; Bruijnzeel (
<xref ref-type="bibr" rid="CR44">1990</xref>
) suggested that drought in the shallow soils is a major cause of forest stunting on ultramafics, perhaps in association with fire (Proctor et al.
<xref ref-type="bibr" rid="CR158">1997</xref>
). Mount Bloomfield lacks tall forests and instead is characterised by trees less than 18 m tall. No statistical relationship could be established between tree height and soil chemistry, although Proctor et al. (
<xref ref-type="bibr" rid="CR160">1999</xref>
) did find a direct proportional relationship between maximum tree height and soil water retention. The authors indirectly linked soil water to fire susceptibility in establishing the particular vegetation pattern on Mount Bloomfield, one that superficially resembles fire-dependent vegetation of New Caledonia.</p>
<p>Proctor et al. (
<xref ref-type="bibr" rid="CR161">2000a</xref>
,
<xref ref-type="bibr" rid="CR162">b</xref>
) compared vegetation on ultramafic soils to those on non-ultramafic (greywacke-derived) soils in Palawan and found that the species richness and diversity of ultramafic and greywacke sites were similar. However, the individual species and familial composition were rather different, with only members of the Saxifragaceae occurring on both ultramafic and greywacke soils. Trees on the serpentinized peridotite had a high proportion of microphyllous leaves, which is not a general feature of ultramafic forests in the region. Differences in water supply and fire frequencies, in combination with edaphic difference, may contribute to the distinct forests overlying these soils (Proctor et al.
<xref ref-type="bibr" rid="CR160">1999</xref>
,
<xref ref-type="bibr" rid="CR161">2000a</xref>
,
<xref ref-type="bibr" rid="CR162">b</xref>
).</p>
<p>Sulawesi and Halmahera in Indonesia have 15,400 and 8000 km
<sup>2</sup>
of ultramafic outcrops, respectively (van der Ent et al.
<xref ref-type="bibr" rid="CR218">2013a</xref>
). Lateritic soils overlaying the bedrock harbor both sclerophyllous ultramafic vegetation and more cryptic tropical rainforest, which are nonetheless inhabited by a high proportion of endemic flora. Proctor et al. (
<xref ref-type="bibr" rid="CR157">1994</xref>
) examined the ultramafic soil–plant relations of Mount Piapi on Karakelong part of the Talaud Islands, North Sulawesi, Indonesia and reported that the short stature of the local vegetation is a result of low water-holding capacity of the soil, while the unusual species assemblage likely results from the soil chemistry typical of ultramafic soils. They also documented an undescribed Ni-hyperaccumulating species of
<italic>Rinorea</italic>
from their study site.</p>
<p>Kinabalu Park, Sabah, one of the world’s most species-rich hotspots with more than 5000 plant species recorded in an area of just 1200 km
<sup>2</sup>
, is also home to extensive ultramafic exposures (van der Ent et al.
<xref ref-type="bibr" rid="CR221">2014</xref>
). Plant diversity on ultramafics of the Park decreases with elevation, with a mid-elevation (circum 1500 masl) ‘hump’ occurring for some plant groups (Orchidaceae, Pteridophytes) resulting from the presence of cloud forests (van der Ent et al.
<xref ref-type="bibr" rid="CR229">2016a</xref>
). Six main vegetation classes with associated soil types are described by van der Ent et al. (
<xref ref-type="bibr" rid="CR229">2016a</xref>
), including Sub-Alpine Scrub and Graminoid Scrub, both associated with Hypermagnesic Cambisols (‘hypermagnesian soils’), Montane Cloud Forest, associated with Cambisols often with accumulation of humus, Mixed Dipterocarp Forest, associated with deep Ferralsols (‘laterites’), and Pioneer Casuarina Scrub and Mature Mixed Casuarina Forest, both associated with Hypermagnesic Leptosols. The ‘adverse’ soil chemistry exacerbates vegetation stunting but no clear correlation between elevation, soil chemistry and plant diversity was found, as some of the most ‘adverse’ soils on the summit of the entirely ultramafic Mount Tambuyukon (2359–2534 masl) had up to 132 species per 250 m
<sup>2</sup>
(van der Ent et al.
<xref ref-type="bibr" rid="CR229">2016a</xref>
).</p>
<p>Samithri (
<xref ref-type="bibr" rid="CR180">2015</xref>
) examined the vegetation community composition and patterns at Ussangoda, Sri Lanka’s most intensively studied ultramafic outcrop. She found a higher diversity of plant species in ‘forest islands’ compared to the extensive ‘plains’ characterizing the site (Fig. 
<xref rid="Fig2" ref-type="fig">2</xref>
c). Although the plains make up over 90% of the outcrop area, they only harbor 18 herbaceous species belonging to 17 genera and 11 families compared to 49 tree, shrub, herb and climber species belonging to 44 genera and 27 families found in the ‘forest islands.’ Although the soil chemical features did not differ significantly between sites on the ‘plains’ versus those in the ‘forest islands,’ soil features such as depth and resulting water holding capacity in ‘forest islands’ may favor the growth of a wide range of species than on the exposed and shallow soils of the ‘plains.’
<fig id="Fig2">
<label>Fig. 2</label>
<caption>
<p>Ultramafic outcrops and vegetation in South and Southeast Asia:
<bold>a</bold>
Oil palm estate in Sabah, Malaysia on eroding ultramafic soils.
<bold>b</bold>
Road cut through strongly serpentinised bedrock in Sabah, Malaysia.
<bold>c</bold>
Bare red Ferralsols at Ussangoda in Sri Lanka.
<bold>d</bold>
River flowing through an ultramafic outcrop in Halmahera, Indonesia.
<bold>e</bold>
Extremely stunted sub-alpine vegetation on ultramafic soils in Kinabalu park, Malaysia.
<bold>f</bold>
Montane cloud forest on ultramafic soils on Mount Silam, Malaysia.
<bold>g</bold>
Exceptionally tall lowland mixed dipterocarp forest on ultramafic soils in Sabah, Malaysia</p>
<p>(all images are by A. van der Ent, except
<bold>c</bold>
by Y.A.S. Samithri and
<bold>g</bold>
by Isabella Zelano)</p>
</caption>
<graphic xlink:href="40529_2017_167_Fig2_HTML" id="MO2"></graphic>
</fig>
</p>
<p>Studies on bryophytes, lichens, and epiphytes on ultramafic outcrops are sparse worldwide (but see Boyd et al.
<xref ref-type="bibr" rid="CR33">2009</xref>
; Briscoe et al.
<xref ref-type="bibr" rid="CR37">2009</xref>
; Favero-Longo et al.
<xref ref-type="bibr" rid="CR65">2004</xref>
; Rajakaruna et al.
<xref ref-type="bibr" rid="CR170">2012</xref>
). In South and Southeast Asia, such studies are mostly non-existent. However, one study from the Philippines (Proctor et al.
<xref ref-type="bibr" rid="CR162">2000b</xref>
) documents epiphytic plants on trees of ultramafic and adjacent greywacke soils. The trees on the greywacke had fewer lianas and much less bole bryophyte cover than those on the serpentinized peridotite. Forty-one percent of trees on peridotite had >10% bryophyte cover, while none of the trees on greywacke soils had >10% bryophyte cover. The greywacke soils also hosted significantly higher densities of ferns, Cyperaceae spp., rattans (Arecaceae: Calamoideae), and Pandanaceae spp. compared to ultramafic soils, while ultramafic soils harbored significantly more herbaceous and bamboo (Poaceae: Bambusoideae) species. Floristic differences between the sites were attributed to differences in geochemistry, hydrology, and fire-frequencies (Proctor et al.
<xref ref-type="bibr" rid="CR160">1999</xref>
,
<xref ref-type="bibr" rid="CR162">2000b</xref>
).</p>
</sec>
<sec id="Sec7">
<title>Plant endemism</title>
<p>Ultramafic soils, often with disproportionately high numbers of endemic species (Anacker
<xref ref-type="bibr" rid="CR9">2011</xref>
), are prime settings to explore the nature of edaphic endemism (Rajakaruna
<xref ref-type="bibr" rid="CR164">2004</xref>
). In New Caledonia, 2150 species occur on ultramafic soils of which 83% are restricted to these soils (Jaffré
<xref ref-type="bibr" rid="CR91">1992</xref>
; Jaffré and L’Huillier
<xref ref-type="bibr" rid="CR92">2010</xref>
), whereas in Cuba, 920 species (approximately one-third of the taxa endemic to Cuba) are found exclusively on ultramafic soils (Borhidi
<xref ref-type="bibr" rid="CR30">1992</xref>
). Similar restrictions and notable floristic associations are also found on ultramafic outcrops of Mediterranean climates (including California; Alexander et al.
<xref ref-type="bibr" rid="CR8">2007</xref>
; Safford et al.
<xref ref-type="bibr" rid="CR177">2005</xref>
), as well as in South Africa/Zimbabwe and Australia (Anacker
<xref ref-type="bibr" rid="CR9">2011</xref>
; Brooks
<xref ref-type="bibr" rid="CR39">1987</xref>
).</p>
<p>The restriction of habitat specialists to ultramafic soils is generally considered a consequence of their inherent slow growth rates that leads them to being outcompeted on more favorable soils (Anacker
<xref ref-type="bibr" rid="CR10">2014</xref>
; Anacker et al.
<xref ref-type="bibr" rid="CR12">2011</xref>
; Kay et al.
<xref ref-type="bibr" rid="CR97">2011</xref>
). Although some growth experiments have shown that habitat specialists can grow faster on more nutrient-rich soils (Kruckeberg
<xref ref-type="bibr" rid="CR106">1954</xref>
), species from the ultramafic maquis in New Caledonia have inherently slow growth, albeit becoming larger under more fertile conditions (Jaffré
<xref ref-type="bibr" rid="CR90">1980</xref>
). Table 
<xref rid="Tab3" ref-type="table">3</xref>
lists the countries within the South and Southeast Asian region with ultramafic floras, including the number of ultramafic-associated species documented and the number of ultramafic endemics described in each country.
<table-wrap id="Tab3">
<label>Table 3</label>
<caption>
<p>Surface area covered by ultramafic rocks, total number of species in the regional flora, number of ultramafic-associated species, and number of ultramafic endemic species along with percent ultramafic endemism in the region’s flora for a number of global hotspots for ultramafic endemism and for regions within South and Southeast Asia</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th align="left">Region</th>
<th align="left">Surface area of ultramafics (km
<sup>2</sup>
)</th>
<th align="left">Total number of vascular plant species in the flora</th>
<th align="left">Number of ultramafic-associated species</th>
<th align="left">Number of ultramafic endemic species (% ultramafic endemism)</th>
<th align="left">References</th>
</tr>
</thead>
<tbody>
<tr>
<td align="left">New Caledonia</td>
<td char="." align="char">5470</td>
<td char="." align="char">3371</td>
<td align="left">2150</td>
<td align="left">1785 (83)</td>
<td align="left">Jaffré (
<xref ref-type="bibr" rid="CR91">1992</xref>
), van der Ent et al. (
<xref ref-type="bibr" rid="CR224">2015d</xref>
), Isnard et al. (
<xref ref-type="bibr" rid="CR89">2016</xref>
)</td>
</tr>
<tr>
<td align="left">California, United States</td>
<td char="." align="char">~6000</td>
<td char="." align="char">5271</td>
<td align="left">492</td>
<td align="left">246 (4.7)</td>
<td align="left">Anacker et al. (
<xref ref-type="bibr" rid="CR12">2011</xref>
), Burge et al. (
<xref ref-type="bibr" rid="CR46">2016</xref>
), Jepson Flora Project (
<xref ref-type="bibr" rid="CR95">2016</xref>
), Safford et al. (
<xref ref-type="bibr" rid="CR177">2005</xref>
)</td>
</tr>
<tr>
<td align="left">Queensland, Australia</td>
<td char="." align="char">818</td>
<td char="." align="char">8500</td>
<td align="left">553</td>
<td align="left">18 (0.2)</td>
<td align="left">Batianoff and Specht (
<xref ref-type="bibr" rid="CR23">1992</xref>
), Batianoff and Singh (
<xref ref-type="bibr" rid="CR24">2001</xref>
)</td>
</tr>
<tr>
<td align="left">Western Australia, Australia</td>
<td char="." align="char">5654</td>
<td char="." align="char">~12,000</td>
<td align="left">1355</td>
<td align="left">14 (0.12)</td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR224">2015d</xref>
)</td>
</tr>
<tr>
<td align="left">New Zealand</td>
<td char="." align="char">~310</td>
<td char="." align="char">2418</td>
<td align="left">~800</td>
<td align="left">15 (0.6)</td>
<td align="left">Lee (
<xref ref-type="bibr" rid="CR111">1992</xref>
), New Zealand Plant Conservation Network (
<xref ref-type="bibr" rid="CR132">2016</xref>
), Van der Ent et al. (
<xref ref-type="bibr" rid="CR224">2015d</xref>
)</td>
</tr>
<tr>
<td align="left">Cuba</td>
<td char="." align="char">5300</td>
<td char="." align="char">6375</td>
<td align="left"></td>
<td align="left">920 (14)</td>
<td align="left">Reeves et al. (
<xref ref-type="bibr" rid="CR175">1999</xref>
)</td>
</tr>
<tr>
<td align="left">Zimbabwe</td>
<td char="." align="char">~3000</td>
<td char="." align="char">6385</td>
<td align="left">322</td>
<td align="left">322 (5)</td>
<td align="left">Wild (
<xref ref-type="bibr" rid="CR241">1965</xref>
), Proctor and Cole (
<xref ref-type="bibr" rid="CR153">1992</xref>
)</td>
</tr>
<tr>
<td align="left">Sabah</td>
<td char="." align="char">~3500</td>
<td char="." align="char">~8000</td>
<td align="left">4252</td>
<td align="left">347 (4.3)</td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR222">2015a</xref>
)</td>
</tr>
<tr>
<td align="left">Sulawesi, Indonesia</td>
<td char="." align="char">~15,400</td>
<td char="." align="char">~5000</td>
<td align="left">na</td>
<td align="left">na</td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR218">2013a</xref>
)</td>
</tr>
<tr>
<td align="left">Palawan, Philippines</td>
<td char="." align="char">~3000</td>
<td char="." align="char">1522</td>
<td align="left">na</td>
<td align="left">na</td>
<td align="left">Davis and Heywood (
<xref ref-type="bibr" rid="CR58">1995</xref>
)</td>
</tr>
<tr>
<td align="left">Sri Lanka</td>
<td char="." align="char">7</td>
<td char="." align="char">3492</td>
<td align="left">107</td>
<td align="left">0</td>
<td align="left">MOE (
<xref ref-type="bibr" rid="CR122">2012</xref>
), Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
), Samithri (
<xref ref-type="bibr" rid="CR180">2015</xref>
)</td>
</tr>
</tbody>
</table>
</table-wrap>
</p>
<p>In Sabah, Malaysia,
<italic>Borneodendron aenigmaticum</italic>
(Euphorbiaceae) is one of the few large rainforest trees restricted to ultramafic soils (Proctor et al.
<xref ref-type="bibr" rid="CR154">1988a</xref>
). Van der Ent and Wood (
<xref ref-type="bibr" rid="CR216">2012</xref>
,
<xref ref-type="bibr" rid="CR217">2013</xref>
) describing orchid species associated with ultramafics in Sabah, Malaysia, documented many endemic species (Orchidaceae) restricted to narrow valleys with steep slopes, dominated by
<italic>Gymnostoma sumatranum</italic>
(Casuarinaceae) and
<italic>Ceuthostoma terminale</italic>
(Casuarinaceae). Further, van der Ent et al. (
<xref ref-type="bibr" rid="CR223">2015b</xref>
) show habitat partitioning among ultramafic endemic
<italic>Nepenthes</italic>
species (Nepenthaceae) of Mount Kinabalu and Mount Tambuyukon, with distinct habitats and elevation ranges for the different
<italic>Nepenthes</italic>
taxa.
<italic>Eriobotrya balgooyi</italic>
(Rosaceae) was described as a new species restricted to ultramafic soils on a hill near the eastern ridge of Mount Kinabalu and on the nearby Mount Tambuyukon in Sabah, Malaysia (Wong and van der Ent
<xref ref-type="bibr" rid="CR245">2014</xref>
). The importance of scientific exploration of the ultramafics of Southeast Asia cannot be stressed enough; a survey on the ultramafic Mount Guiting-Guiting, Philippines (Argent et al.
<xref ref-type="bibr" rid="CR14">2007</xref>
) also led to the discovery of a new species,
<italic>Lobelia proctorii</italic>
(Campanulaceae).</p>
<p>Sri Lanka’s ultramafic outcrops and their flora, compared with ultramafic floras of Southeast Asia and Australia-Pacific region (van der Ent et al.
<xref ref-type="bibr" rid="CR225">2015c</xref>
,
<xref ref-type="bibr" rid="CR224">d</xref>
), have received relatively little attention partly because they do not harbor any endemic species nor many metal hyperaccumulators (Chathuranga et al.
<xref ref-type="bibr" rid="CR51">2015</xref>
). All species so far documented from the ultramafic outcrops of Sri Lanka also have non-ultramafic populations, and it is unclear whether the ultramafic populations are physiologically distinct (i.e. ecotypes).</p>
</sec>
</sec>
<sec id="Sec8">
<title>Cross-kingdom interactions</title>
<p>Edaphically stressful substrates, like ultramafic soils, present plants with challenges that differ from more ‘benign’ substrates. Growing under such stress, ultramafic plants will likely encounter other organisms (herbivores, pathogens, beneficial insects and pathogens) that are also able to tolerate some of the same stressors affecting the plants (Strauss and Boyd
<xref ref-type="bibr" rid="CR197">2011</xref>
). There is evidence to suggest that pressures from enemies will be greater on edaphically stressful substrates than on normal soils (Strauss and Cacho
<xref ref-type="bibr" rid="CR198">2013</xref>
). Additionally, the enriched concentrations of certain trace elements, such as nickel, found in ultramafic soils may provide plants with opportunities for elemental defence (Boyd
<xref ref-type="bibr" rid="CR32">2014</xref>
). A significant body of research exists on plant–other biota interactions on ultramafic soils from temperate and Mediterranean climes, including studies on elemental defence (Boyd
<xref ref-type="bibr" rid="CR31">2009</xref>
), defence against pathogens (Hörger et al.
<xref ref-type="bibr" rid="CR87">2013</xref>
; Springer
<xref ref-type="bibr" rid="CR196">2009</xref>
), herbivory (Lau et al.
<xref ref-type="bibr" rid="CR109">2008</xref>
), mycorrhizal associations (Southworth et al.
<xref ref-type="bibr" rid="CR194">2014</xref>
), plant–pollinator interactions (Meindl et al.
<xref ref-type="bibr" rid="CR116">2013</xref>
; Wolf and Thorp
<xref ref-type="bibr" rid="CR244">2011</xref>
), and seed dispersal (Spasojevic et al.
<xref ref-type="bibr" rid="CR195">2014</xref>
). However, such studies are minimal in tropical Asia.</p>
<sec id="Sec9">
<title>Herbivory</title>
<p>In the only known published study on herbivory in ultramafic ecosystems in the region, Proctor et al. (
<xref ref-type="bibr" rid="CR161">2000a</xref>
) found that the percentage of leaf area consumed was similar for plants found on and off of ultramafic soils on Mount Bloomfield, Palawan (Philippines), although the actual leaf area consumed was greater for the ultramafic forest as it had plants with larger leaves. There was no relationship between herbivory and leaf elemental chemistry; even the metal-accumulating taxa were attacked by herbivores. Proctor et al. (
<xref ref-type="bibr" rid="CR161">2000a</xref>
) speculate that the gall-forming and leaf-mining insects must be tolerant of nickel as they spend their entire juvenile stage in the leaf tissue.</p>
<p>Recent work by van der Ent and Mulligan (
<xref ref-type="bibr" rid="CR212">2015</xref>
) show Ni accumulation in various parts of Ni hyperaccumulator plants occurring in Sabah, Malaysia, with the highest Ni concentration recorded in the phloem tissue (up to 7.9% in
<italic>R. bengalensis</italic>
) and phloem sap (up to 16.9% in
<italic>Phyllanthus balgooyi</italic>
); Ni localization in phloem tissue is visible by the bright green coloration in field-collected samples (Fig. 
<xref rid="Fig3" ref-type="fig">3</xref>
b, f). The discovery of toxic levels of Ni in the phloem tissue suggests that the increased Ni in the phloem provides a defence against phloem-sap feeding insects, pathogens, and other herbivores (Boyd
<xref ref-type="bibr" rid="CR32">2014</xref>
; Hanson et al.
<xref ref-type="bibr" rid="CR78">2004</xref>
). However, Geometric moth larvae (Erebidae: Erebinae:Poaphilini) were found feeding on the leaves of the Ni hyperaccumulator
<italic>P. balgooyi</italic>
, furthermore aphids were found feeding on
<italic>Phyllanthus</italic>
cf.
<italic>securinegioides</italic>
(van der Ent et al.
<xref ref-type="bibr" rid="CR227">2015f</xref>
).
<fig id="Fig3">
<label>Fig. 3</label>
<caption>
<p>Nickel hyperaccumulator plants in South and Southeast Asia:
<bold>a</bold>
<italic>Phyllanthus balgooyi</italic>
(Phyllanthaceae) in Sabah, Malaysia is a small understorey tree.
<bold>b</bold>
Phloem sap exuding from
<italic>Phyllanthus balgooyi</italic>
contains up to 20 wt% Ni.
<bold>c</bold>
<italic>Knema matanensis</italic>
(Myristicaceae) in Sulawesi, Indonesia;
<bold></bold>
<italic>Rinorea bengalensis</italic>
(Violaceae) can be locally dominant in lowland forest, in Sabah, Malaysia.
<bold>e</bold>
<italic>Dichapetalum gelonioides</italic>
subsp.
<italic>tuberculatum</italic>
(Dichapetalaceae) from Mount Silam, Malaysia.
<bold>f</bold>
Main stem of
<italic>Dichapetalum gelonioides</italic>
subsp.
<italic>tuberculatum</italic>
showing its Ni-rich phloem tissue with colorimetric response in dimethylglyoxime test-paper.
<bold>g</bold>
<italic>Sarcotheca celebica</italic>
(Oxalidaceae) from Sulawesi, Indonesia.
<bold>h</bold>
<italic>Psychotria sarmentosa</italic>
(Rubiaceae) is the only known Ni hyperaccumulator in South and Southeast Asia that is a climber</p>
<p>(all images are by A. van der Ent, except
<bold>c</bold>
,
<bold>g</bold>
are by A. Tjoa, Tadulako University, Indonesia)</p>
</caption>
<graphic xlink:href="40529_2017_167_Fig3_HTML" id="MO3"></graphic>
</fig>
</p>
</sec>
<sec id="Sec10">
<title>Mycorrhizal associations</title>
<p>
<italic>Pisolithus tinctorius</italic>
(Sclerodermataceae), an ectomycorrhizal fungus, is found in the rhizosphere of
<italic>Eucalyptus urophylla</italic>
(Myrtaceae) from ultramafic soils in the Philippines, New Caledonia, and Western Australia (Aggangan et al.
<xref ref-type="bibr" rid="CR3">1998</xref>
).
<italic>Pisolithus tinctorius</italic>
was cultured with
<italic>E. urophylla</italic>
to determine the effects of Cr and Ni on the fungal growth rate. The fungus concentrates metals in the extramatrical hyphae and extra-hyphal slime and is particularly tolerant of high concentrations of Ni and Cr. There was geographic variation in terms of metal tolerance in the fungus, with the New Caledonian isolate outperforming both the Australian and the Philippines isolates. The Philippines isolate grew well on agar in the presence of Cr up to 2000 µmol L
<sup>−1</sup>
and Ni up to 200 µmol L
<sup>−1</sup>
, but formed fewer mycorrhizae in vitro and in vivo than its counterparts from New Caledonia and Western Australia.</p>
</sec>
<sec id="Sec11">
<title>Soil invertebrates</title>
<p>A study comparing termite assemblages on ultramafic-derived forest soils to those on non-ultramafic soils in Borneo, Malaysia shows that ultramafic sites have low species density (<35%), low relative abundance (<30%), a virtual absence of soil-feeders, significantly fewer wood-feeders, and a near-absence of species of Rhinotermitidae,
<italic>Amitermes</italic>
-group,
<italic>Termes</italic>
-group,
<italic>Pericapritermes</italic>
-group and
<italic>Oriensubulitermes</italic>
-group (Jones et al.
<xref ref-type="bibr" rid="CR96">2010</xref>
). The authors suggest that metal toxicity, high pH disrupting gut physiology, metal poisoning of essential microbiota in the termite gut, and metal bioaccumulation by gut microbes with subsequent poisoning of the termite host, as possible reasons for the depauperate termite communities on ultramafic soils.</p>
<p>A study on the patterns of Oribatid mite communities in relation to elevation and geology on the slopes of Mount Kinabalu, Sabah, Malaysia, shows that the density and morphospecies richness of Oribatid mites are greater in non-ultramafic soils than in the ultramafic soils at each of the same elevations (Hasegawa et al.
<xref ref-type="bibr" rid="CR81">2006</xref>
). The density and richness of Oribatid mites decreased with elevation on both substrates, but the effects of elevation on their density in non-ultramafic soil were less significant than in the ultramafic substrate.</p>
<p>An investigation of the invertebrate communities in forest litter and soil on Mount Guiting-Guiting in the Philippines, shows that ultramafic soils, even at higher elevations, were not poor in soil invertebrates, including Oligochaeta (Thomas and Proctor
<xref ref-type="bibr" rid="CR205">1997</xref>
), similar to earlier findings on Mount Silam, Sabah (Leakey and Proctor
<xref ref-type="bibr" rid="CR110">1987</xref>
).</p>
</sec>
</sec>
<sec id="Sec12">
<title>Physiology and genetics</title>
<p>There is considerable interest in understanding the physiology and the underlying genetic basis for traits conferring adaptation to ultramafic soils (Bratteler et al.
<xref ref-type="bibr" rid="CR35">2006</xref>
; Palm and Van Volkenburgh
<xref ref-type="bibr" rid="CR143">2014</xref>
; von Wettberg and Wright
<xref ref-type="bibr" rid="CR235">2011</xref>
; Wu et al.
<xref ref-type="bibr" rid="CR248">2008</xref>
). The advent of novel molecular methods has provided unique approaches to exploring stress tolerance (Selby et al.
<xref ref-type="bibr" rid="CR184">2014</xref>
; Visioli and Marmiroli
<xref ref-type="bibr" rid="CR233">2013</xref>
) and ultramafic-associated plants will continue to provide model systems for such investigations (Arnold et al.
<xref ref-type="bibr" rid="CR15">2016</xref>
; von Wettberg et al.
<xref ref-type="bibr" rid="CR236">2014</xref>
). While these advances have not yet been made in tropical Asia, the region provides numerous opportunities for investigating the physiological and genetic aspects of adaptation to ultramafic soils. To date, much of the research in South and Southeast Asia has focused on discovering new hyperaccumulating plant species from ultramafic soils in the region.</p>
<sec id="Sec13">
<title>Trace element hyperaccumulation</title>
<p>Plants found on ultramafic soils have long-been recognized as model systems to explore trace element hyperaccumulation (Gall and Rajakaruna
<xref ref-type="bibr" rid="CR73">2013</xref>
). There are well over 450 Ni hyperaccumulator plant species globally, all occurring on ultramafic soils (van der Ent et al.
<xref ref-type="bibr" rid="CR220">2013c</xref>
). Ultramafic associated plants are known to hyperaccumulate cobalt (Co) and Cu (>300 μg g
<sup>−1</sup>
in their dry leaf tissue), and Ni (>1000 μg g
<sup>−1</sup>
in their dry leaf tissue). For recent reviews of trace element hyperaccumulation, see Reeves (
<xref ref-type="bibr" rid="CR174">2003</xref>
), Krämer (
<xref ref-type="bibr" rid="CR105">2010</xref>
), van der Ent et al. (
<xref ref-type="bibr" rid="CR220">2013c</xref>
,
<xref ref-type="bibr" rid="CR226">2015e</xref>
) and Pollard et al. (
<xref ref-type="bibr" rid="CR149">2014</xref>
). Table 
<xref rid="Tab4" ref-type="table">4</xref>
lists documented hyperaccumulator plants from the South and Southeast Asia region, listing the element hyperaccumulated, country of discovery, and relevant references. Figure 
<xref rid="Fig3" ref-type="fig">3</xref>
documents some of the nickel hyperaccumulator plants discovered from ultramafic soils in parts of South and Southeast Asia.</p>
<p>In one of the earliest geoecological studies of the region, Wither and Brooks (
<xref ref-type="bibr" rid="CR242">1977</xref>
) and Brooks et al. (
<xref ref-type="bibr" rid="CR42">1977b</xref>
) analysed herbarium samples of plants originating from Obi Island (North Moluccas). They identified
<italic>Myristica laurifolia</italic>
var.
<italic>bifurcata</italic>
(Myristicaceae),
<italic>Planchonella oxyhedra</italic>
(Sapotaceae), and
<italic>Trichospermum kjellbergii</italic>
(Malvaceae) as hyperaccumulators of Ni. The authors then analysed Ni concentrations in herbarium specimens of
<italic>T. kjellbergii</italic>
and
<italic>P. oxyhedra</italic>
from throughout their range in Southeast Asia and Oceania. The findings confirmed previously known ultramafic areas in Sulawesi and Indonesian New Guinea, as well as one in Ambon (South Moluccas) which was not documented on geological maps. Their suspicions about the substrate were confirmed by a 1994 geological study that mapped peridotite and serpentinite outcrops in both Ambon and Seram (Linthout and Helmers
<xref ref-type="bibr" rid="CR112">1994</xref>
). A more recent study in Soroako, Sulawesi, examined leaf tissue from 23 plant species from former Ni mining sites in search of hyperaccumulator plants (Netty et al.
<xref ref-type="bibr" rid="CR131">2012</xref>
). As a result,
<italic>Sarcotheca celebica</italic>
(Oxalidaceae) was confirmed as a Ni hyperaccumulator, with 1039 µg g
<sup>−1</sup>
Ni in dry leaf tissue.</p>
<p>In a study describing the general influence of the ultramafic geochemistry on growth patterns of plants overlying two Malaysian massifs, the Bukit Rokan and Petasih along the Bentong-Raub suture zone on the Peninsula, Tashakor et al. (
<xref ref-type="bibr" rid="CR202">2013</xref>
) document that the serpentinite of the area is strongly weathered and gives rise to characteristic red lateritic soils (Ferralsols). They point out that the greatest physiological stress experienced by plants growing on ultramafic soils is due to the low Ca: Mg ratio and the generally low available nutrients, and not due to potentially phytotoxic elements present in the soil, which are, for the most part, not in a plant-available form.</p>
<p>In a study of the Bela Ophiolite in the Wadh area of Balochistan, Pakistan, Naseem et al. (
<xref ref-type="bibr" rid="CR129">2009</xref>
) discovered
<italic>Pteropyrum olivieri</italic>
(Polygonaceae) in a localized population over ultramafic soils. Although the plant did not hyperaccumulate, it had moderate concentrations of Ni, Co, and Cr in its tissues, typical of most plants growing on ultramafic soils.</p>
<p>The ultramafics of Malaysia and Indonesia have received considerable attention with regard to taxa with high metal-accumulating behavior. A chemical analysis of leaf litter from trees growing on ultramafics in Sabah, Malaysia (Proctor et al.
<xref ref-type="bibr" rid="CR156">1989</xref>
) confirmed that trees grow at low foliar nutrient concentrations and can concentrate Ca in their leaf tissue. Leaf litter showed an average Ca:Mg ratio as well as a high level of Ni, suggesting that senescence may act as a way of excreting excess Ni. From analysis of leaf litter, they found that
<italic>Shorea tenuiramulosa</italic>
(Dipterocarpaceae) and an unidentified species of
<italic>Syzygium</italic>
(Myrtaceae) accumulated Ni and Mn, respectively, with 1000 µg g
<sup>−1</sup>
Ni and 13,700 µg g
<sup>−1</sup>
Mn dry leaf weight. Proctor et al. (
<xref ref-type="bibr" rid="CR157">1994</xref>
) also reported a yet to be named Ni-hyperaccumulating species of
<italic>Rinorea</italic>
from Mt Piapi on Karakelong Island, northeast of Sulawesi in Indonesia with up to 1830 µg g
<sup>−1</sup>
foliar Ni.</p>
<p>In an analysis of 51 herbarium specimens from both Malaysia and Indonesia, including from Mount Kinabalu (Sabah), Soroako and Malili (Sulawesi) and Yapen Island, Reeves (
<xref ref-type="bibr" rid="CR174">2003</xref>
) found high Ni values in
<italic>Phyllanthus insulae-japen</italic>
(Phyllanthaceae), which had been collected once in 1961, and in
<italic>R. bengalensis</italic>
,
<italic>Brackenridgea palustris</italic>
subsp.
<italic>kjellbergii</italic>
(Ochnaceae),
<italic>Glochidion</italic>
spp. (Phyllanthaceae), and two species of
<italic>Psychotria</italic>
(Rubiaceae) which could not be identified to species level. One ultramafic subspecies of
<italic>D. gelonioides</italic>
was identified as a Ni hyperaccumulator (subsp.
<italic>tuberculatum</italic>
), whereas another subspecies was confirmed as a Zn hyperaccumulator on non-ultramafic soils (subsp.
<italic>pilosum</italic>
) (Baker et al.
<xref ref-type="bibr" rid="CR16">1992</xref>
).</p>
<p>In recent studies of Mt. Kinabalu, van der Ent et al. (
<xref ref-type="bibr" rid="CR219">2013b</xref>
,
<xref ref-type="bibr" rid="CR222">2015a</xref>
,
<xref ref-type="bibr" rid="CR227">f</xref>
) discovered nine species of Ni hyperaccumulators from the flora of Kinabalu Park in Sabah, Malaysia. Previously known hyperaccumulators from the region included
<italic>R. bengalensis</italic>
(Brooks and Wither
<xref ref-type="bibr" rid="CR40">1977</xref>
a,
<xref ref-type="bibr" rid="CR42">b</xref>
),
<italic>Rinorea javanica</italic>
(Brooks et al.
<xref ref-type="bibr" rid="CR41">1977a</xref>
),
<italic>P. balgooyi</italic>
(Phyllanthaceae; Hoffmann et al.
<xref ref-type="bibr" rid="CR86">2003</xref>
),
<italic>D. gelonioides</italic>
(Baker et al.
<xref ref-type="bibr" rid="CR16">1992</xref>
),
<italic>Psychotria</italic>
cf.
<italic>gracilis</italic>
(Rubiaceae; Reeves
<xref ref-type="bibr" rid="CR174">2003</xref>
), and
<italic>Shorea tenuiramulosa</italic>
(Proctor et al.
<xref ref-type="bibr" rid="CR156">1989</xref>
). Van der Ent et al. (
<xref ref-type="bibr" rid="CR219">2013b</xref>
,
<xref ref-type="bibr" rid="CR227">2015f</xref>
) added several more Ni hyperaccumulators, including
<italic>Actephila alanbakeri</italic>
(
<italic>Cleistanthus</italic>
sp. nov. in the original report) (Phyllanthaceae; 11,520 µg g
<sup>−1</sup>
),
<italic>Flacourtia kinabaluensis</italic>
(Salicaceae; 7280 µg g
<sup>−1</sup>
),
<italic>Glochidion mindorense</italic>
(Phyllanthaceae; 2280 µg g
<sup>−1</sup>
),
<italic>Kibara coriacea</italic>
(Monimiaceae; 5840 µg g
<sup>−1</sup>
),
<italic>Mischocarpus sundaicus</italic>
(Sapindaceae) (4425 µg g
<sup>−1</sup>
),
<italic>Phyllanthus</italic>
cf.
<italic>securinegioides</italic>
(Phyllanthaceae; 23,300 µg g
<sup>−1</sup>
),
<italic>Psychotria sarmentosa</italic>
(Rubiaceae; 24,200 µg g
<sup>−1</sup>
),
<italic>Walsura pinnata</italic>
(Meliaceae; 4580 µg g
<sup>−1</sup>
), and
<italic>Xylosma luzoniensis</italic>
(Salicaceae; 5360 µg g
<sup>−1</sup>
) to the list, thereby documenting the highest number of Ni hyperaccumulators (15) known from any region within South and Southeast Asia.</p>
<p>In an effort to understand the factors contributing to Ni hyperaccumulation in Sabah, Malaysia, van der Ent et al. (
<xref ref-type="bibr" rid="CR230">2016b</xref>
) examined the soil chemistry associated with 18 Ni hyperaccumulator plant species, comparing the chemistry of ultramafic soils where Ni hyperaccumulators were absent. The results showed that Ni hyperaccumulators are restricted to circum-neutral soils with relatively high phytoavailable Ca, Mg, and Ni. They hypothesized that either hyperaccumulators excrete large amounts of root exudates, thereby increasing Ni phytoavailability through intense rhizosphere mineral weathering, or that they have extremely high Ni uptake efficiency, thereby severely depleting Ni and stimulating re-supply of Ni via diffusion from labile Ni pools. Their results, however, tend to favor the latter hypothesis.</p>
<p>Nuclear microprobe imaging (micro-PIXE) shows that in
<italic>P. balgooyi</italic>
collected from ultramafic soils in Sabah, Malaysia, Ni concentrations were very high in the phloem of the stems and petioles, while in the leaves Ni was enriched in the major vascular bundles (Mesjasz-Przybylowicz et al.
<xref ref-type="bibr" rid="CR117">2015</xref>
). The preferential accumulation of Ni in the vascular tracts suggests that Ni is present in a metabolically active form. This research is important as the elemental distribution of
<italic>P. balgooyi</italic>
differs from that of many other Ni hyperaccumulators from temperate and Mediterranean regions where Ni is preferentially accumulated in leaf epidermal cells (Bhatia et al.
<xref ref-type="bibr" rid="CR26">2004</xref>
; Broadhurst et al.
<xref ref-type="bibr" rid="CR38">2004</xref>
; Tylko et al.
<xref ref-type="bibr" rid="CR208">2007</xref>
; Baklanov
<xref ref-type="bibr" rid="CR18">2011</xref>
).</p>
<p>In the Philippines, much of the ultramafic vegetation remains underexplored (Fernando et al.
<xref ref-type="bibr" rid="CR67">2008</xref>
; but see Baker et al.
<xref ref-type="bibr" rid="CR16">1992</xref>
; Fernando et al.
<xref ref-type="bibr" rid="CR68">2013</xref>
; Proctor et al.
<xref ref-type="bibr" rid="CR159">1998</xref>
,
<xref ref-type="bibr" rid="CR161">2000a</xref>
,
<xref ref-type="bibr" rid="CR162">b</xref>
). Studies to date have revealed new Ni hyperaccumulators (e.g. Fernando and Rodda
<xref ref-type="bibr" rid="CR66">2013</xref>
; Hoffmann et al.
<xref ref-type="bibr" rid="CR86">2003</xref>
), including
<italic>Breynia cernua</italic>
(Phyllanthaceae; Gotera et al.
<xref ref-type="bibr" rid="CR77">2014</xref>
) and
<italic>P. balgooyi</italic>
,
<italic>P. erythrotrichus</italic>
, and
<italic>P. securinegioides</italic>
(Phyllanthaceae; Hoffmann et al.
<xref ref-type="bibr" rid="CR86">2003</xref>
; Quimado et al.
<xref ref-type="bibr" rid="CR163">2015</xref>
). A recent study described
<italic>Rinorea niccolifera</italic>
(Violaceae) as a novel taxon and Ni hyperaccumulator from Luzon Island, Philippines (Fernando et al.
<xref ref-type="bibr" rid="CR69">2014</xref>
).</p>
<p>Although in Sri Lanka’s ultramafic outcrops are not associated with many Ni hyperaccumulator species, unlike those in Sabah, Malaysia (van der Ent et al.
<xref ref-type="bibr" rid="CR222">2015a</xref>
), several plant species currently found at Ussangoda hyperaccumulate Ni (see citations in Chathuranga et al.
<xref ref-type="bibr" rid="CR51">2015</xref>
; Samithri
<xref ref-type="bibr" rid="CR180">2015</xref>
). Notable in this regard are
<italic>Evolvulus alsinoides</italic>
(Convolvulaceae),
<italic>Hybanthus enneaspermus</italic>
(Violaceae),
<italic>Flacourtia indica</italic>
(Flacourtiaceae),
<italic>Olax imbricata</italic>
(Olacaceae),
<italic>Toddalia asiatica</italic>
(Rutaceae),
<italic>Euphorbia heterophylla</italic>
(Euphorbiaceae),
<italic>Vernonia cinerea</italic>
(Asteraceae) and
<italic>Crotalaria</italic>
sp. (Fabaceae). Senevirathne et al. (
<xref ref-type="bibr" rid="CR181">2000</xref>
) also document
<italic>Striga euphrasioides</italic>
(Orobanchaceae),
<italic>Cassia mimosoides</italic>
(Fabaceae), and
<italic>Blumea obliqua</italic>
(Asteraceae) from Ussangoda as hyperaccumulating Ni, although subsequent studies have failed to confirm this earlier report. Five Cu hyperaccumulators [
<italic>Geniosporum tenuiflorum</italic>
(Lamiaceae; now
<italic>Ocimum tenuiflorum</italic>
),
<italic>Clerodendrum infortunatum</italic>
(Lamiaceae),
<italic>Croton bonplandianus</italic>
(Euphorbiaceae),
<italic>Waltheria indica</italic>
(Malvaceae), and
<italic>Tephrosia villosa</italic>
(Fabaceae)] are also found on ultramafic outcrops in Sri Lanka (Rajakaruna and Bohm
<xref ref-type="bibr" rid="CR166">2002</xref>
). Based on revised criteria for Cu hyperaccumulation (van der Ent et al.
<xref ref-type="bibr" rid="CR220">2013c</xref>
),
<italic>Calotropis gigantea</italic>
,
<italic>Carissa spinarum</italic>
,
<italic>Cassia auriculata</italic>
,
<italic>Abutilon indicum</italic>
, and
<italic>Phyllanthus</italic>
sp. undet., analysed by Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
), now also qualify as hyperaccumulators of Cu (Table 
<xref rid="Tab4" ref-type="table">4</xref>
). Although Cu hyperaccumulation is not a common phenomenon among ultramafic plants, a recent study has also documented unusual Cu uptake in a number of ultramafic plants in Malaysia and Brazil (van der Ent and Reeves
<xref ref-type="bibr" rid="CR213">2015</xref>
).
<table-wrap id="Tab4">
<label>Table 4</label>
<caption>
<p>Unusual foliar elemental accumulation (Ni, Co, Cu, Mn or Zn—maximum recorded values in μg g
<sup>−1</sup>
) in plants from South and Southeast Asia</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th align="left">Family</th>
<th align="left">Species</th>
<th align="left">Life-form</th>
<th align="left">Locality</th>
<th align="left">Ni</th>
<th align="left">Cu</th>
<th align="left">Co</th>
<th align="left">Mn</th>
<th align="left">Zn</th>
<th align="left">Reference</th>
</tr>
</thead>
<tbody>
<tr>
<td align="left">Acanthaceae</td>
<td align="left">
<italic>Daedalacanthus suffruticosus</italic>
</td>
<td align="left">Shrub</td>
<td align="left">India</td>
<td align="left">1235–1862</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Datta et al. (
<xref ref-type="bibr" rid="CR57">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Acanthaceae</td>
<td align="left">
<italic>Ptyssiglottis</italic>
cf
<italic>. fusca</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">1160</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Amaranthaceae</td>
<td align="left">
<italic>Aerva scandens</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sulawesi, Indonesia</td>
<td align="left"></td>
<td align="left">395</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Brooks et al. (
<xref ref-type="bibr" rid="CR43">1978</xref>
)</td>
</tr>
<tr>
<td align="left">Amaranthaceae</td>
<td align="left">
<italic>Cyathula prostrata</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sulawesi, Indonesia</td>
<td align="left"></td>
<td align="left">553</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Brooks et al. (
<xref ref-type="bibr" rid="CR43">1978</xref>
)</td>
</tr>
<tr>
<td align="left">Apocynaceae</td>
<td align="left">
<italic>Calotropis gigantea</italic>
</td>
<td align="left">Climber</td>
<td align="left">Sri Lanka</td>
<td align="left"></td>
<td align="left">583</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Apocynaceae</td>
<td align="left">
<italic>Carissa spinarum</italic>
</td>
<td align="left">Climber</td>
<td align="left">Sri Lanka</td>
<td align="left"></td>
<td align="left">702</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Asteraceae</td>
<td align="left">
<italic>Vernonia actaea</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sulawesi, Indonesia</td>
<td align="left"></td>
<td align="left">300</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Brooks et al. (
<xref ref-type="bibr" rid="CR43">1978</xref>
)</td>
</tr>
<tr>
<td align="left">Asteraceae</td>
<td align="left">
<italic>Vernonia cinerea</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sri Lanka</td>
<td align="left">1026</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Samithri (
<xref ref-type="bibr" rid="CR180">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Chrysobalanaceae</td>
<td align="left">
<italic>Licania splendens</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Zambales, Philippines</td>
<td align="left">2728</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Fernando et al. (
<xref ref-type="bibr" rid="CR68">2013</xref>
)</td>
</tr>
<tr>
<td align="left">Convolvulaceae</td>
<td align="left">
<italic>Evolvulus alsinoides</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sri Lanka</td>
<td align="left">1478</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Dichapetalaceae</td>
<td align="left">
<italic>Dichapetalum gelonioides</italic>
subsp
<italic>. pilosum</italic>
</td>
<td align="left">Climber/shrub</td>
<td align="left">Sabah, Malaysia</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">7000</td>
<td align="left">Baker et al. (
<xref ref-type="bibr" rid="CR16">1992</xref>
)</td>
</tr>
<tr>
<td align="left">Dichapetalaceae</td>
<td align="left">
<italic>Dichapetalum gelonioides</italic>
subsp
<italic>. sumatranum</italic>
</td>
<td align="left">Shrub</td>
<td align="left">SE Asia</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">30,000</td>
<td align="left">Baker et al. (
<xref ref-type="bibr" rid="CR16">1992</xref>
)</td>
</tr>
<tr>
<td align="left">Dichapetalaceae</td>
<td align="left">
<italic>Dichapetalum geloniodes</italic>
subsp
<italic>. tuberculatum</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Malaysia and Philippines</td>
<td align="left">26,600</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Baker et al. (
<xref ref-type="bibr" rid="CR16">1992</xref>
)</td>
</tr>
<tr>
<td align="left">Dichapetalaceae</td>
<td align="left">
<italic>Dichapetalum gelonioides</italic>
subsp.
<italic>andamanicum</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Andaman Islands, India</td>
<td align="left">3160; 9740–36,100</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Brooks (
<xref ref-type="bibr" rid="CR39">1987</xref>
), Datta et al. (
<xref ref-type="bibr" rid="CR57">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Dipterocarpaceae</td>
<td align="left">
<italic>Shorea tenuiramulosa</italic>
</td>
<td align="left">Tree</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">1790</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Proctor et al. (
<xref ref-type="bibr" rid="CR154">1988a</xref>
,
<xref ref-type="bibr" rid="CR155">b</xref>
), Van der Ent et al. (
<xref ref-type="bibr" rid="CR222">2015a</xref>
,
<xref ref-type="bibr" rid="CR223">b</xref>
,
<xref ref-type="bibr" rid="CR224">c</xref>
,
<xref ref-type="bibr" rid="CR225">d</xref>
,
<xref ref-type="bibr" rid="CR226">e</xref>
,
<xref ref-type="bibr" rid="CR227">f</xref>
,
<xref ref-type="bibr" rid="CR228">g</xref>
)</td>
</tr>
<tr>
<td align="left">Euphorbiaceae</td>
<td align="left">
<italic>Croton bonplandianus</italic>
</td>
<td align="left">Tree</td>
<td align="left">Sri Lanka</td>
<td align="left"></td>
<td align="left">2163</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Euphorbiaceae</td>
<td align="left">
<italic>Euphorbia thymifolia</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Sri Lanka</td>
<td align="left">1074</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Samithri (
<xref ref-type="bibr" rid="CR180">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Fabaceae</td>
<td align="left">
<italic>Cassia auriculata</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Sri Lanka</td>
<td align="left"></td>
<td align="left">885</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Fabaceae</td>
<td align="left">
<italic>Dalbergia beccarii</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">2623</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent and Reeves (
<xref ref-type="bibr" rid="CR213">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Fabaceae</td>
<td align="left">
<italic>Tephrosia villosa</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sri Lanka</td>
<td align="left"></td>
<td align="left">1858</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Lamiaceae</td>
<td align="left">
<italic>Clerodendrum infortunatum</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sri Lanka</td>
<td align="left"></td>
<td align="left">2278</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Lamiaceae</td>
<td align="left">
<italic>Coleus scutellarioides</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sri Lanka</td>
<td align="left"></td>
<td align="left">500</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Brooks et al. (
<xref ref-type="bibr" rid="CR43">1978</xref>
)</td>
</tr>
<tr>
<td align="left">Lamiaceae</td>
<td align="left">
<italic>Ocimum tenuiflorum</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sri Lanka</td>
<td align="left"></td>
<td align="left">2266</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Loganiaceae</td>
<td align="left">
<italic>Strychnos andamanensis</italic>
</td>
<td align="left">Climber</td>
<td align="left">India</td>
<td align="left">2606–6893</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Datta et al. (
<xref ref-type="bibr" rid="CR57">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Loganiaceae</td>
<td align="left">
<italic>Strychnos minor</italic>
</td>
<td align="left">Climber</td>
<td align="left">India</td>
<td align="left">3220–10,214</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Datta et al. (
<xref ref-type="bibr" rid="CR57">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Loganiaceae</td>
<td align="left">
<italic>Strychnos wallichiana</italic>
</td>
<td align="left">Climber</td>
<td align="left">India</td>
<td align="left">2924–15,630</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Datta et al. (
<xref ref-type="bibr" rid="CR57">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Malvaceae</td>
<td align="left">
<italic>Abutilon indicum</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Sri Lanka</td>
<td align="left"></td>
<td align="left">915</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Malvaceae</td>
<td align="left">
<italic>Waltheria indica</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Sri Lanka</td>
<td align="left"></td>
<td align="left">1504</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Meliaceae</td>
<td align="left">
<italic>Walsura monophylla</italic>
</td>
<td align="left">Tree</td>
<td align="left">Malaysia and Philippines</td>
<td align="left">7090</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Baker et al. (
<xref ref-type="bibr" rid="CR16">1992</xref>
)</td>
</tr>
<tr>
<td align="left">Meliaceae</td>
<td align="left">
<italic>Walsura pinnata</italic>
</td>
<td align="left">Tree</td>
<td align="left">SE Asia</td>
<td align="left">4580</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Monimiaceae</td>
<td align="left">
<italic>Kibara coriacea</italic>
</td>
<td align="left">Tree</td>
<td align="left">SE Asia</td>
<td align="left">5840</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Moraceae</td>
<td align="left">
<italic>Ficus brevicuspis</italic>
</td>
<td align="left">Tree</td>
<td align="left">India</td>
<td align="left">28,322–30,564</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Datta et al. (
<xref ref-type="bibr" rid="CR57">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Myristicaceae</td>
<td align="left">
<italic>Knema matanensis</italic>
</td>
<td align="left">Tree</td>
<td align="left">Indonesia</td>
<td align="left">5000</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR218">2013a</xref>
)</td>
</tr>
<tr>
<td align="left">Myristicaceae</td>
<td align="left">
<italic>Myristica laurifolia</italic>
var
<italic>. bifurcata</italic>
</td>
<td align="left">Tree</td>
<td align="left">Indonesia</td>
<td align="left">1100</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Wither and Brooks (
<xref ref-type="bibr" rid="CR242">1977</xref>
)</td>
</tr>
<tr>
<td align="left">Myrtaceae</td>
<td align="left">
<italic>Decaspermum blancoi</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Zambales, Philippines</td>
<td align="left">1996</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Fernando et al. (
<xref ref-type="bibr" rid="CR68">2013</xref>
)</td>
</tr>
<tr>
<td align="left">Ochnaceae</td>
<td align="left">
<italic>Brackenridgea palustris</italic>
subsp.
<italic>foxworthyi</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Philippines</td>
<td align="left">7600</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Baker et al. (
<xref ref-type="bibr" rid="CR16">1992</xref>
)</td>
</tr>
<tr>
<td align="left">Ochnaceae</td>
<td align="left">
<italic>Brackenridgea palustris</italic>
subsp
<italic>. kjellbergii</italic>
</td>
<td align="left">Tree</td>
<td align="left">Sulawesi, Indonesia</td>
<td align="left">1440</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Reeves (
<xref ref-type="bibr" rid="CR174">2003</xref>
)</td>
</tr>
<tr>
<td align="left">Ochnaceae</td>
<td align="left">
<italic>Ochna integerrima</italic>
</td>
<td align="left">Tree</td>
<td align="left">India</td>
<td align="left">2465–5210</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Datta et al. (
<xref ref-type="bibr" rid="CR57">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Olacaceae</td>
<td align="left">
<italic>Olax imbricata</italic>
</td>
<td align="left">Tree</td>
<td align="left">Sri Lanka</td>
<td align="left">1082</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Samithri (
<xref ref-type="bibr" rid="CR180">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Oxalidaceae</td>
<td align="left">
<italic>Sarcotheca celebica</italic>
</td>
<td align="left">Tree</td>
<td align="left">Indonesia</td>
<td align="left">1000</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR218">2013a</xref>
,
<xref ref-type="bibr" rid="CR219">b</xref>
,
<xref ref-type="bibr" rid="CR220">c</xref>
)</td>
</tr>
<tr>
<td align="left">Papilionaceae</td>
<td align="left">
<italic>Cassia sophera</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Sulawesi, Indonesia</td>
<td align="left"></td>
<td align="left">333</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Brooks et al. (
<xref ref-type="bibr" rid="CR43">1978</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Actephila alanbakeri</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">11,520</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR231">2016c</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Aporosa chalarocarpa</italic>
</td>
<td align="left">Tree</td>
<td align="left">SE Asia</td>
<td align="left">1560</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Baccaurea lanceolata</italic>
</td>
<td align="left">Tree</td>
<td align="left">SE Asia</td>
<td align="left">1450</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Breynia cernua</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Zambales, Philippines</td>
<td align="left">3573</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Gotera et al. (
<xref ref-type="bibr" rid="CR77">2014</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Cleistanthus</italic>
sp. 1</td>
<td align="left">Tree</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">2110</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Glochidion</italic>
aff
<italic>. acustylum</italic>
</td>
<td align="left">Tree</td>
<td align="left">Sulawesi, Indonesia</td>
<td align="left">6060</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Reeves (
<xref ref-type="bibr" rid="CR174">2003</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Glochidion brunneum</italic>
</td>
<td align="left">Tree</td>
<td align="left">SE Asia</td>
<td align="left">6200</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Glochidion</italic>
cf
<italic>. lanceisepalum</italic>
</td>
<td align="left">Tree</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">3270</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Glochidion</italic>
cf.
<italic>mindorense</italic>
</td>
<td align="left">Tree</td>
<td align="left">SE Asia</td>
<td align="left">2280</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Glochidion</italic>
cf.
<italic>rubrum</italic>
</td>
<td align="left">Tree</td>
<td align="left">SE Asia</td>
<td align="left">7000</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Glochidion</italic>
cf.
<italic>sericeum</italic>
</td>
<td align="left">Tree</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">2190</td>
<td align="left"></td>
<td align="left">1310</td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
); Van der Ent (unpublished) </td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Glochidion</italic>
sp. ‘bambangan’</td>
<td align="left">Tree</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">16,700</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Glochidion</italic>
sp. ‘nalumad’</td>
<td align="left">Tree</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">9000</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Phyllanthus balgooyi</italic>
</td>
<td align="left">Tree</td>
<td align="left">Malaysia and Philippines</td>
<td align="left">8610</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Hoffmann et al. (
<xref ref-type="bibr" rid="CR86">2003</xref>
), Mesjasz-Przybylowicz et al. (
<xref ref-type="bibr" rid="CR117">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Phyllanthus erythrotrichus</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Zambales, Philippines</td>
<td align="left">17,520</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Quimado et al. (
<xref ref-type="bibr" rid="CR163">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Phyllanthu</italic>
s
<italic>securinegioides</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">23,300</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Baker et al. (
<xref ref-type="bibr" rid="CR16">1992</xref>
), Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Phyllanthaceae</td>
<td align="left">
<italic>Phyllanthus</italic>
sp. undet.</td>
<td align="left">Shrub</td>
<td align="left">Sri Lanka</td>
<td align="left"></td>
<td align="left">821</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Piperaceae</td>
<td align="left">
<italic>Peperomia pellucida</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Sulawesi, Indonesia</td>
<td align="left"></td>
<td align="left">300</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Brooks et al. (
<xref ref-type="bibr" rid="CR43">1978</xref>
)</td>
</tr>
<tr>
<td align="left">Rubiaceae</td>
<td align="left">
<italic>Psychotria</italic>
cf
<italic>. gracilis</italic>
</td>
<td align="left"></td>
<td align="left">Sabah, Malaysia</td>
<td align="left">10,590</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Reeves (
<xref ref-type="bibr" rid="CR174">2003</xref>
)</td>
</tr>
<tr>
<td align="left">Rubiaceae</td>
<td align="left">
<italic>Psychotria sarmentosa</italic>
</td>
<td align="left">Climber</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">24,200</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Rubiaceae</td>
<td align="left">
<italic>Psychotria</italic>
sp. undet.</td>
<td align="left"></td>
<td align="left">Sulawesi, Indonesia</td>
<td align="left">1820</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Reeves (
<xref ref-type="bibr" rid="CR174">2003</xref>
)</td>
</tr>
<tr>
<td align="left">Rubiaceae</td>
<td align="left">
<italic>Urophyllum</italic>
cf.
<italic>macrophyllum</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sabah, Malaysia</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">10,464</td>
<td align="left"></td>
<td align="left">Van der Ent and Reeves (
<xref ref-type="bibr" rid="CR213">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Salicaceae</td>
<td align="left">
<italic>Flacourtia indica</italic>
</td>
<td align="left">Tree</td>
<td align="left">Sri Lanka</td>
<td align="left">1165</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Samithri (
<xref ref-type="bibr" rid="CR180">2015</xref>
)</td>
</tr>
<tr>
<td align="left">Salicaceae</td>
<td align="left">
<italic>Flacourtia kinabaluensis</italic>
</td>
<td align="left">Tree</td>
<td align="left">Sabah, Malaysia</td>
<td align="left">7280</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Salicaceae</td>
<td align="left">
<italic>Xylosma luzonensis</italic>
</td>
<td align="left">Tree</td>
<td align="left">SE Asia</td>
<td align="left">5360</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Sapindaceae</td>
<td align="left">
<italic>Mischocarpus sundaicus</italic>
</td>
<td align="left">Tree</td>
<td align="left">SE Asia</td>
<td align="left">4425</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Van der Ent et al. (
<xref ref-type="bibr" rid="CR227">2015f</xref>
)</td>
</tr>
<tr>
<td align="left">Sapotaceae</td>
<td align="left">
<italic>Planchonella obovata</italic>
</td>
<td align="left">Tree</td>
<td align="left">Zambales, Philippines</td>
<td align="left">1005</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Fernando et al. (
<xref ref-type="bibr" rid="CR68">2013</xref>
)</td>
</tr>
<tr>
<td align="left">Sapotaceae</td>
<td align="left">
<italic>Planchonella oxyedra</italic>
</td>
<td align="left">Tree</td>
<td align="left">Obi Island, Indonesia</td>
<td align="left">19,600</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Wither and Brooks (
<xref ref-type="bibr" rid="CR242">1977</xref>
)</td>
</tr>
<tr>
<td align="left">Tiliaceae</td>
<td align="left">
<italic>Trichospermum kjellbergii</italic>
</td>
<td align="left">Tree</td>
<td align="left">Indonesia</td>
<td align="left">3770</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Wither and Brooks (
<xref ref-type="bibr" rid="CR242">1977</xref>
)</td>
</tr>
<tr>
<td align="left">Urticaceae</td>
<td align="left">
<italic>Laportea ruderalis</italic>
</td>
<td align="left">Herb</td>
<td align="left">Sulawesi, Indonesia</td>
<td align="left"></td>
<td align="left">600</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Brooks et al. (
<xref ref-type="bibr" rid="CR43">1978</xref>
)</td>
</tr>
<tr>
<td align="left">Verbenaceae</td>
<td align="left">
<italic>Callicarpa</italic>
sp. undet.</td>
<td align="left">Shrub</td>
<td align="left">Zambales, Philippines</td>
<td align="left">1052</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Fernando et al. (
<xref ref-type="bibr" rid="CR68">2013</xref>
)</td>
</tr>
<tr>
<td align="left">Violaceae</td>
<td align="left">
<italic>Hybanthus enneaspermus</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Sri Lanka</td>
<td align="left">1862</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
)</td>
</tr>
<tr>
<td align="left">Violaceae</td>
<td align="left">
<italic>Rinorea bengalensis</italic>
</td>
<td align="left">Tree</td>
<td align="left">S & SE Asia and Australia</td>
<td align="left">2723–18,840</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Brooks and Wither (
<xref ref-type="bibr" rid="CR40">1977</xref>
); Datta et al. (
<xref ref-type="bibr" rid="CR57">2015</xref>
) </td>
</tr>
<tr>
<td align="left">Violaceae</td>
<td align="left">
<italic>Rinorea javanica</italic>
</td>
<td align="left">Tree</td>
<td align="left">SE Asia</td>
<td align="left">9680</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Brooks and Wither (
<xref ref-type="bibr" rid="CR40">1977</xref>
)</td>
</tr>
<tr>
<td align="left">Violaceae</td>
<td align="left">
<italic>Rinorea niccolifera</italic>
</td>
<td align="left">Shrub</td>
<td align="left">Luzon Island, Philippines</td>
<td align="left">18,388</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Fernando et al. (
<xref ref-type="bibr" rid="CR69">2014</xref>
)</td>
</tr>
<tr>
<td align="left">Violaceae</td>
<td align="left">
<italic>Rinorea</italic>
sp. nov.</td>
<td align="left">Shrub</td>
<td align="left">Talaud Island, Indonesia</td>
<td align="left">1830</td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left"></td>
<td align="left">Proctor et al. (
<xref ref-type="bibr" rid="CR157">1994</xref>
)</td>
</tr>
</tbody>
</table>
</table-wrap>
</p>
</sec>
</sec>
<sec id="Sec14">
<title>Evolutionary aspects</title>
<p>Ultramafic outcrops often harbor populations which are morphologically and physiologically distinct from those found on non-ultramafic soils. Such intraspecific variation, especially with respect to functionally important traits, is common in many ultramafic taxa worldwide (O’Dell and Rajakaruna
<xref ref-type="bibr" rid="CR136">2011</xref>
). Such variation can result from both local adaptation (i.e., ecotypic differentiation; Sambatti and Rice
<xref ref-type="bibr" rid="CR179">2006</xref>
; Turner et al.
<xref ref-type="bibr" rid="CR207">2010</xref>
) or phenotypic plasticity (Murren et al.
<xref ref-type="bibr" rid="CR128">2006</xref>
; Wu et al.
<xref ref-type="bibr" rid="CR249">2010</xref>
), and must be examined on a case-by-case basis. Suitable methods of examination include reciprocal or unilateral transplant experiments and common garden studies (Wright and Stanton
<xref ref-type="bibr" rid="CR247">2011</xref>
), as well as functional genomic and proteomic approaches (Selby et al.
<xref ref-type="bibr" rid="CR184">2014</xref>
; von Wettberg et al.
<xref ref-type="bibr" rid="CR236">2014</xref>
; von Wettberg and Wright
<xref ref-type="bibr" rid="CR235">2011</xref>
). Detecting intraspecific variation is the first step toward any investigation on the causes and consequences of adaptive evolution. Populations exhibiting intraspecific variation on ultramafic and non-ultramafic soils have led to numerous studies of speciation (Anacker
<xref ref-type="bibr" rid="CR10">2014</xref>
; Kay et al.
<xref ref-type="bibr" rid="CR97">2011</xref>
) and phylogenetic investigations (Anacker
<xref ref-type="bibr" rid="CR9">2011</xref>
; Anacker et al.
<xref ref-type="bibr" rid="CR12">2011</xref>
; Anacker and Harrison
<xref ref-type="bibr" rid="CR11">2012</xref>
), advancing our understanding of evolutionary and ecological theory (Harrison and Rajakaruna
<xref ref-type="bibr" rid="CR79">2011</xref>
). Molecular phylogenetic methods provide a unique protocol for testing and establishing species relationships, helping to shed light on how ultramafic endemics evolve (Baldwin
<xref ref-type="bibr" rid="CR19">2005</xref>
). The analysis of phylogenies for 23 genera from California shows that ultramafic endemics exhibit few transitions out of the endemic state (Anacker et al.
<xref ref-type="bibr" rid="CR12">2011</xref>
), suggesting that adaptation to ultramafics and subsequent diversification can lead to an evolutionary “dead end”. But ultramafic lineages may not always represent evolutionary “dead ends” and may have the potential to further diversify via independent polyploidization and hybridization, even providing a pathway to radiate off ultramafic soils (Kolář et al.
<xref ref-type="bibr" rid="CR104">2012</xref>
).</p>
<p>Compared to these studies from other regions of the world, there is little information on evolutionary aspects of plants associated with ultramafic soils in South and Southeast Asia. A recent study from Sri Lanka shows that the ultramafic and non-ultramafic populations of
<italic>Fimbristylis ovata</italic>
(Cyperaceae) may be locally adapted to their respective soils (Chathuranga et al.
<xref ref-type="bibr" rid="CR51">2015</xref>
). The ultramafic population translocated significantly more Ni from its roots to shoots (translocation factor 0.43) than the non-ultramafic population (translocation factor 0.29). However, additional studies are required to determine whether the populations of
<italic>F. ovata</italic>
, or other species, including those hyperaccumulating metals such as Ni and Cu, deserve ecotypic recognition. Several ultramafic-associated taxa in Sri Lanka might benefit from further observations and additional greenhouse studies to determine whether the ultramafic-associated populations are genetically distinct and are worthy of ecotypic recognition (Rajakaruna and Bohm
<xref ref-type="bibr" rid="CR166">2002</xref>
). These taxa include several Ni-accumulating and -hyperaccumulating species, particularly
<italic>Hybanthus enneaspermus</italic>
(Violaceae),
<italic>Evolvulus alsinoides</italic>
(Convolvulaceae),
<italic>Crotalaria</italic>
sp. (Fabaceae),
<italic>Desmodium triflorum</italic>
(Fabaceae) and
<italic>Fimbristylis</italic>
sp. (Cyperaceae), all of which show detectable phenotypic differences between ultramafic and non-ultramafic populations. Studies exploring causes and consequences of phenotypic differences between populations found on and off ultramafic soils can add much to our understanding of the origins of ultramafic specialists in the South and Southeast Asia region.</p>
</sec>
<sec id="Sec15">
<title>Phytotechnologies</title>
<p>The use of trace element hyperaccumulators to clean up polluted sites, i.e. phytoremediation, is gaining recognition as a viable green technology (Neilson and Rajakaruna
<xref ref-type="bibr" rid="CR130">2014</xref>
). Phytoremediation is based on the premise that plants which remove selected pollutants from the soil and translocate them to their above-ground biomass can then be harvested and disposed of through incineration or elemental recovery, a process known as phytomining (Chaney et al.
<xref ref-type="bibr" rid="CR50">2014</xref>
; van der Ent et al.
<xref ref-type="bibr" rid="CR228">2015g</xref>
). Ultramafic plants in the genera
<italic>Alyssum</italic>
(Brassicaceae),
<italic>Streptanthus</italic>
(Brassicaceae),
<italic>Noccaea</italic>
(Brassicaceae), and
<italic>Berkheya</italic>
(Asteraceae) have been used in phytoremediation and phytomining of Ni-enriched ultramafic sites in temperate and Mediterranean regions (Ho et al.
<xref ref-type="bibr" rid="CR85">2013</xref>
; Morel et al.
<xref ref-type="bibr" rid="CR126">2006</xref>
; Gall and Rajakaruna
<xref ref-type="bibr" rid="CR73">2013</xref>
; Sheoran et al.
<xref ref-type="bibr" rid="CR189">2009</xref>
; van der Ent et al.
<xref ref-type="bibr" rid="CR228">2015g</xref>
). Given the large number of hyperaccumulator species currently known from tropical Asia (Gall and Rajakaruna
<xref ref-type="bibr" rid="CR73">2013</xref>
; Reeves
<xref ref-type="bibr" rid="CR174">2003</xref>
), there should be considerable interest in using these unique plants in the remediation of regional sites contaminated with metal and metalloid pollutants.</p>
<sec id="Sec16">
<title>Phytoremediation and phytomining</title>
<p>Bandara et al. (
<xref ref-type="bibr" rid="CR20">2017</xref>
) investigated the effect of biochar and fungal-bacterial co-inoculation on soil enzymatic activity and immobilization of heavy metals in soil collected from an ultramafic outcrop in Sri Lanka. The addition of biochar to ultramafic soil immobilized heavy metals and decreased soil enzymatic activities while the addition of microbial inoculants improved plant growth by mitigating heavy metal toxicity and enhancing soil enzymatic activities. Additional studies from Sri Lanka confirm the importance of (i) bacterial-fungal inoculation as a soil-quality enhancer and a plant-growth promoter in the presence of heavy metals found in ultramafic soils (Seneviratne et al.
<xref ref-type="bibr" rid="CR185">2016a</xref>
,
<xref ref-type="bibr" rid="CR186">b</xref>
), and, (ii) biochar as a soil amendment to immobilize Cr, Ni, and Mn in ultramafic soil, thereby reducing metal-induced plant toxicities (Herath et al.
<xref ref-type="bibr" rid="CR82">2014</xref>
).</p>
<p>The potential for microbial remediation (reduction) of Cr(VI) by indigenous microbial populations from the ultramafic soils of Sukinda mines in Jaipur, Orissa, India, was investigated by Mishra et al. (
<xref ref-type="bibr" rid="CR119">2009</xref>
). The best reducer of Cr (V1) was
<italic>Staphylococcus aureus</italic>
, a gram-positive bacterium whose thick layer of peptidoglycan acts as a strong absorbent. The taxon tolerated a Cr concentration of 250 mg L
<sup>−1</sup>
and was resistant to Ni up to 1000 mg L
<sup>−1</sup>
. The bacterium was recommended for the bioremediation of both Cr and Ni, showing complete Cr(VI) to Cr(III) degradation in 22 h, and Ni
<sup>2+</sup>
degradation to 90% in 22 h. Similarly, Bohidar et al. (
<xref ref-type="bibr" rid="CR29">2009</xref>
) explored the possibility of Ni recovery from chromite tailings at the Sukinda mines by using three fungal strains.</p>
<p>In another study, Mohanty et al. (
<xref ref-type="bibr" rid="CR123">2011</xref>
) utilized phytoremediation in South Kaliapani, a chromite mining ultramafic area in Orissa, India. Chromium was extracted by growing
<italic>Oryza sativa</italic>
cv. Khandagiri (rice; Poaceae) in contaminated soil and irrigating with mine wastewater. Chromium levels were reduced (70–90%) after 100 days, with accumulation levels ranging from 125 to 498 µg g
<sup>−1</sup>
in leaves, 25 to 400 µg g
<sup>−1</sup>
in stems, and 5 to 23 µg g
<sup>−1</sup>
in the grain. Absorption into roots was higher by two orders of magnitude than into any aerial part of the plant. Mohanty et al. (
<xref ref-type="bibr" rid="CR124">2012</xref>
) also investigated the phytoremediation potential of
<italic>O. sativa</italic>
,
<italic>Brachiaria mutica</italic>
(Poaceae), and
<italic>Eichhornia crassipes</italic>
(Pontederiaceae) to reduce levels of Cr(VI) in mine waste-water.
<italic>Eichhornia crassipes</italic>
was most successful with 25–54% reduction while
<italic>B. mutica</italic>
contributed to an 18–33% reduction.</p>
<p>Kfayatullah et al. (
<xref ref-type="bibr" rid="CR99">2001</xref>
), in a study of plants and soils of the Malakand chromite-rich ultramafic area and Mardan non-ultramafic areas of the North-West Frontier Province, Pakistan, focused on enzyme-bound metal accumulation in plant tissue.
<italic>Verbascum thapsus</italic>
(Scrophulariaceae), an edible plant, accumulated greater than 100 µg g
<sup>−1</sup>
of several metals, including Ni and Cr, but was not recommended for phytoremediation efforts.</p>
<p>Indonesia (Sulawesi and Halmahera Islands) has some of the largest surface exposures of ultramafic bedrock in the world. Lateritic Ni-mining operations have continued in the region since the early twentieth century, setting the stage for exploring the use of native plants for phytoremediation and phytomining. Twelve native species known to hyperaccumulate Ni are recommended by van der Ent et al. (
<xref ref-type="bibr" rid="CR218">2013a</xref>
) for use in phytotechnologies in Indonesia.</p>
</sec>
</sec>
<sec id="Sec17">
<title>Threats and conservation</title>
<p>Ultramafic areas are a high priority for biodiversity conservation because of the relatively large numbers of endemic species, ecotypes, and rare species that they harbour (Boyd et al.
<xref ref-type="bibr" rid="CR33">2009</xref>
). The conservation and restoration of these naturally fragmented, edaphically unique, and biodiverse habitats require special attention (Baker et al.
<xref ref-type="bibr" rid="CR17">2010</xref>
; O’Dell
<xref ref-type="bibr" rid="CR134">2014</xref>
; Thorne et al.
<xref ref-type="bibr" rid="CR206">2011</xref>
; Whiting et al.
<xref ref-type="bibr" rid="CR240">2004</xref>
). It is unclear how stressors, such as atmospheric N deposition (Vallano et al.
<xref ref-type="bibr" rid="CR210">2012</xref>
), suppression of fire (Arabas
<xref ref-type="bibr" rid="CR13">2000</xref>
; Safford and Harrison
<xref ref-type="bibr" rid="CR176">2004</xref>
) and climate change (Damschen et al.
<xref ref-type="bibr" rid="CR56">2012</xref>
; Anacker and Harrison
<xref ref-type="bibr" rid="CR11">2012</xref>
) documented for temperate and Mediterranean ultramafics, impact tropical Asia’s ultramafic ecosystems.</p>
<p>The combined forces of forest clearing, agricultural development and mining contribute to unprecedented habitat loss in South and Southeast Asia (Duckworth et al.
<xref ref-type="bibr" rid="CR63">2012</xref>
; Hughes
<xref ref-type="bibr" rid="CR88">2017</xref>
; Sodhi et al.
<xref ref-type="bibr" rid="CR191">2004</xref>
). In fact, Southeast Asia has a higher annual rate of deforestation than Meso-America, South America, or sub-Saharan Africa, and that rate has continued to increase between 1990 and 2005 (Giam et al.
<xref ref-type="bibr" rid="CR75">2010</xref>
; Sodhi et al.
<xref ref-type="bibr" rid="CR192">2010</xref>
). This is especially of concern as Southeast Asia has a higher proportion of its vascular plant, reptile, bird, and mammal species categorised as globally threatened on the Red List compared to Meso- and South America and sub-Saharan Africa (Sodhi et al.
<xref ref-type="bibr" rid="CR192">2010</xref>
). With such limited study of ultramafics in South and Southeast Asia, it is unclear how increasing habitat loss is impacting biodiverse ultramafic outcrops in the region.</p>
<p>Malaysia has one of the most species-rich ultramafic floras in the world. The over 3500 km
<sup>2</sup>
of ultramafic outcrops in Sabah (4.6% of the total landmass of the state) on the island of Borneo harbor a total of 4252 plant species (van der Ent et al.
<xref ref-type="bibr" rid="CR222">2015a</xref>
). Over 2542 plant species have been documented on ultramafic outcrops in Kinabalu Park alone, of which a large percentage is endemic to either Kinabalu Park or to Borneo (van der Ent et al.
<xref ref-type="bibr" rid="CR222">2015a</xref>
; Fig.
<xref rid="Fig4" ref-type="fig">4</xref>
). Despite the existence of this species-rich flora, the plant diversity and ecology of many ultramafic outcrops in Sabah remain largely unknown because of a lack of focused research. Furthermore, plant diversity in many areas of Sabah is severely threatened by land-use conversion and, because often plant species occur only at a single or a few ultramafic sites, and hence impacts on the ecosystems that support them could eventually result in their extinction. While it is necessary to identify stressors impacting ultramafic habitats of South and Southeast Asia for their proper management, it is even more critical that basic geoecological surveys of ultramafic outcrops, including the extensive exposures in Sulawesi and Halmahera, are prioritised for cataloguing plant diversity and other biota. This is especially critical as many of these outcrops likely harbor rare and endemic species in need of urgent conservation attention.
<fig id="Fig4">
<label>Fig. 4</label>
<caption>
<p>Ultramafic edaphic endemics from South and Southeast Asia:
<bold>a</bold>
The monotypic tree
<italic>Borneodendron aenigmaticum</italic>
(Euphorbiaceae) is endemic to Sabah (Malaysia) on ultramafic soils in the lowlands.
<bold>b</bold>
The world’s largest carnivorous pitcher plant,
<italic>Nepenthes rajah</italic>
(Nepenthaceae) is endemic to Kinabalu Park in Sabah where it occurs in the montane zone.
<bold>c</bold>
The epiphytic or lithophytic orchid
<italic>Porpax borneensis</italic>
(Orchidaceae) is restricted to ultramafic outcrops in Sabah, Malaysia.
<bold>d</bold>
The recently described
<italic>Begonia moneta</italic>
(Begoniaceae) occurs lithophytically in lowland ultramafic forest in Sabah, Malaysia.
<bold>e</bold>
<italic>Scaevola verticillata</italic>
(Goodeniaceae) is endemic to the summit of the ultramafic Mount Tambukon in Sabah, Malaysia.
<bold>f</bold>
The carnivorous
<italic>Drosera ultramafica</italic>
(Droseraceae) is endemic to a limited number of mountainous ultramafic outcrops in Malaysia and the Philippines.
<bold>g</bold>
<italic>Rhododendron baconii</italic>
(Ericaceae) is another hyper-endemic restricted to Kinabalu Park, Sabah, Malaysia.
<bold>h</bold>
The specific epithet of
<italic>Pittosporum peridoticola</italic>
(Pittosporaceae) indicates its habitat is on ultramafic soils in Sabah, Malaysia</p>
<p>(all images are by A. van der Ent)</p>
</caption>
<graphic xlink:href="40529_2017_167_Fig4_HTML" id="MO4"></graphic>
</fig>
</p>
<p>Although Sri Lanka’s ultramafic flora appears to be impoverished with respect to endemic species or hyperaccumulator taxa, the ultramafic sites harbor several taxa worthy of conservation. For example, Ussangoda, the site that has received the most research attention, is home to: four near-threatened species,
<italic>Striga angustifolia</italic>
(Orobanchaceae),
<italic>Maerua arenaria</italic>
(Capparaceae),
<italic>Salvadora percia</italic>
(Salvadoraceae), and
<italic>Olax imbricata</italic>
(Olacaceae); two vulnerable species,
<italic>Cyanotis adscendens</italic>
(Commelinaceae),
<italic>Pachygone ovata</italic>
(Menispermaceae); and one data deficient species,
<italic>Alysicarpus monilifer</italic>
(Fabaceae; MOE
<xref ref-type="bibr" rid="CR122">2012</xref>
). Therefore, it is critical that Sri Lanka’s ultramafic outcrops receive regional and national recognition and are declared as ecologically sensitive sites (i.e. geoecological preserves) to be set aside for future investigations. In 2010, Ussangoda was declared as a National Park with approximately 350 hectares, including areas overlaying ultramafic rock, set aside for conservation purposes (Department of Wildlife Conservation
<xref ref-type="bibr" rid="CR59">2015</xref>
). Without such conservation, proper management, and research, these unique habitats and their physiologically distinct biota are extremely vulnerable.
<italic>Rinorea bengalensis</italic>
(Violaceae) offers an example of why such efforts are urgently needed. Brooks et al. (
<xref ref-type="bibr" rid="CR41">1977a</xref>
,
<xref ref-type="bibr" rid="CR42">b</xref>
) conducted a survey of herbarium specimens from the entire range of this species, encompassing Sri Lanka, the Malay Archipelago, New Guinea, the Solomon Islands and Queensland, Australia, and found that Ni hyperaccumulation is a constitutive trait in this species when growing on ultramafic soil. The herbarium specimen analysed from Sri Lanka contained 10,000 µg g
<sup>−1</sup>
and the locality indicated on the map presented by Brooks et al. (
<xref ref-type="bibr" rid="CR41">1977a</xref>
) suggests a collection in the central part of the island (see Fig. 1 in Rajakaruna and Baker
<xref ref-type="bibr" rid="CR165">2004</xref>
). However, it was not encountered in field exploration by Rajakaruna and Bohm (
<xref ref-type="bibr" rid="CR166">2002</xref>
) and was presumed extinct in Sri Lanka (Ministry of Environment and Renewable Energy
<xref ref-type="bibr" rid="CR118">2012</xref>
). Interestingly, the taxon was recently recollected in southwestern Sri Lanka (Siril Wijesundara, National Institute of Fundamental Studies, Sri Lanka, pers. comm.), however, soil and plant tissue elemental concentrations have yet to be determined.</p>
</sec>
<sec id="Sec18">
<title>Conclusions</title>
<sec id="Sec19">
<title>Information gaps and future directions</title>
<p>Ultramafic outcrops are natural laboratories for experimental and applied research in a wide range of disciplines. They provide numerous opportunities for collaborations among geologists, pedologists, botanists, zoologists, microbiologists, and land managers focusing on conservation and restoration research. However, research on the ultramafic outcrops in South and Southeast Asia has been limited, with most effort to date focused on Malaysia, the Philippines, the Andaman Islands (India), and Sri Lanka (Table 
<xref rid="Tab1" ref-type="table">1</xref>
). We were unable to find any published literature on ultramafic geoecology of other South (Afghanistan, Bhutan, Nepal) and Southeast Asian (Myanmar, Laos, Thailand, Vietnam) countries despite the known occurrences of ultramafic lithologies in these locales. The limited number of published studies we found for Myanmar, Thailand, and Vietnam (Table 
<xref rid="Tab1" ref-type="table">1</xref>
) focused on geological, mineralogical, or geochemical research.</p>
<p>Throughout South and Southeast Asia, detailed and systematic surveys will likely reveal numerous species new to science, including trace element hyperaccumulators. Recent research conducted in Sabah, Malaysia by van der Ent et al. (
<xref ref-type="bibr" rid="CR221">2014</xref>
,
<xref ref-type="bibr" rid="CR222">2015a</xref>
,
<xref ref-type="bibr" rid="CR227">f</xref>
) which led to the discovery of 24 new hyperaccumulator species, is a case in point. Detailed floristic surveys should be undertaken across the region and species showing unusual physiological behavior (such as trace element accumulation) or exhibiting distinct morphological traits relative to populations on non-ultramafic soils may be further studied under laboratory and greenhouse conditions. Additionally, species showing intraspecific variation between ultramafic and non-ultramafic populations may be evaluated via population genetic studies to determine whether ultramafic populations are genetically distinct from those found on non-ultramafic soils. For those species showing intraspecific variation with respect to morphological or physiological features, including flowering times between ultramafic and non-ultramafic populations, common garden and reciprocal transplant experiments can be undertaken to examine whether populations are locally adapted to their substrate. Such types of experimental studies are currently lacking entirely from the region.</p>
<p>In addition to detailed studies of vascular plants, it is important to pay close attention to non-vascular plants such as bryophytes, cryptogamic species such as lichens, soil algae and cyanoprokaryotes, and belowground microbes and soil invertebrates. Such investigations will likely reveal species that are endemic to the substrate or show a high affinity to ultramafic soils, as shown for such research conducted in South Africa (Venter et al.
<xref ref-type="bibr" rid="CR232">2015</xref>
) and California, USA (Rajakaruna et al.
<xref ref-type="bibr" rid="CR170">2012</xref>
).</p>
<p>Species documented as trace element hyperaccumulators may be investigated under controlled conditions for their suitability for phytoremediation or phytomining and tested under field conditions for their effectiveness in site reclamation and restoration. The resulting information can be added to the global database of metal hyperaccumulating species (Global Hyperaccumulator Database
<xref ref-type="bibr" rid="CR76">2016</xref>
:
<ext-link ext-link-type="uri" xlink:href="http://www.hyperaccumulators.org">http://www.hyperaccumulators.org</ext-link>
). Finally, it is critical that tropical Asia’s ultramafic outcrops receive regional, national, and global recognition and that key sites receive appropriate statutory protection so that future scientific research is possible.</p>
<p>One of the options for protection at a national level by the state is the inclusion of ultramafic sites in the Global Geopark Network (GGN). Conservation and protection of landscapes of geological significance at a national and international level is promoted by UNESCO under its Global Geoparks Scheme (UNESCO
<xref ref-type="bibr" rid="CR209">2016</xref>
). At a national level, relevant authorities should pursue this option as a long-term conservation strategy, which would provide a holistic approach to protection by incorporating a management strategy including education and sustainable development. The latter would mobilize the local population for economic benefits by participating in the conservation efforts through local and international ecotourism. This, however, also requires meeting the stringent guidelines laid out by UNESCO to be included in the GGN. Currently, ultramafic sites in South and Southeast Asia are not in the GGN but would meet the basic requirements laid out by UNESCO.</p>
</sec>
</sec>
</body>
<back>
<ack>
<title>Authors’ contributions</title>
<p>Conceptualization, NR, AE, MCMI; writing original manuscript draft, MLG; writing and editing, NR, AE, MCMI; visualization, MLG, AE, NR. All authors read and approved the final manuscript.</p>
<sec id="FPar1">
<title>Acknowledgements</title>
<p>A. van der Ent is the recipient of a Discovery Early Career Researcher Award (DE160100429) from the Australian Research Council. 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 A. van der Ent. N. Rajakaruna is supported by a US Research Scholar Fulbright Award for 2016–2017 and the National Institute of Fundamental Studies, Kandy, Sri Lanka. We would like to thank Ian Medeiros for his constructive comments on an earlier draft of this manuscript.</p>
</sec>
<sec id="FPar2">
<title>Competing interests</title>
<p>The authors declare that they have no competing interests.</p>
</sec>
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