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Aluminium accumulation in leaves of 127 species in Melastomataceae, with comments on the order Myrtales.

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  • 1. Laboratory of Plant Systematics, Institute of Botany and Microbiology, K. U. Leuven, Belgium.
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    • Jansen S 1
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Annals of Botany, 01 Jul 2002, 90(1):53-64
https://doi.org/10.1093/aob/mcf142 PMID: 12125773 PMCID: PMC4233848

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Abstract 

The distribution and systematic significance of aluminium accumulation is surveyed based on semi-quantitative tests of 166 species, representing all tribes and subfamilies of the Melastomataceae as well as a few members of related families within the Myrtales. The character is strongly present in nearly all members of the Memecylaceae and in most primitive taxa of the Melastomataceae, while non-accumulating taxa are widespread in the more derived tribes of the Melastomataceae. The variable distribution of Al accumulation in advanced clades of the latter family is probably associated with the tendency to herbaceousness, although it is unclear whether the more herbaceous representatives have developed more specialized Al-response mechanisms that may exclude high Al levels from the shoot. It is hypothesized that Al accumulation is symplesiomorphic for Melastomataceae and Memecylaceae, and that the feature characterizes the most primitive families in the Myrtales. Indeed, Al accumulation is also characteristic of Crypteroniaceae, Rhynchocalycaceae and Vochysiaceae. Crypteroniaceae and Rhynchocalycaceae probably take a basal position in a sister clade of the Memecylaceae and Melastomataceae, while Al accumulation suggests a basal position for Vochysiaceae in the Myrtaceae clade.

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Ann Bot. 2002 Jul 1; 90(1): 53–64.
PMCID: PMC4233848
PMID: 12125773

Aluminium Accumulation in Leaves of 127 Species in Melastomataceae, with Comments on the Order Myrtales

STEVEN JANSEN,*,1 TOSHIHIRO WATANABE,2,3 and ERIK SMETS1
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Abstract

The distribution and systematic significance of aluminium accumulation is surveyed based on semi‐quantitative tests of 166 species, representing all tribes and subfamilies of the Melastomataceae as well as a few members of related families within the Myrtales. The character is strongly present in nearly all members of the Memecylaceae and in most primitive taxa of the Melastomataceae, while non‐accumulating taxa are widespread in the more derived tribes of the Melastomataceae. The variable distribution of Al accumulation in advanced clades of the latter family is probably associated with the tendency to herbaceousness, although it is unclear whether the more herbaceous representatives have developed more specialized Al‐response mechanisms that may exclude high Al levels from the shoot. It is hypothesized that Al accumulation is symplesiomorphic for Melastomataceae and Memecylaceae, and that the feature characterizes the most primitive families in the Myrtales. Indeed, Al accumulation is also characteristic of Crypteroniaceae, Rhynchocalycaceae and Vochysiaceae. Crypteroniaceae and Rhynchocalycaceae probably take a basal position in a sister clade of the Memecylaceae and Melastomataceae, while Al accumulation suggests a basal position for Vochysiaceae in the Myrtaceae clade.

Key words: Aluminium accumulation, systematics, phylogenetic relationships, Crypteroniaceae, Melastomataceae, Memecylaceae, Myrtales, Rhynchocalycaceae, Vochysiaceae

INTRODUCTION

Only a small fraction of plant species take up high levels of aluminium (Al) in their above‐ground tissues. Generally, plants are classified as accumulators if they accumulate at least 1000 mg kg–1 in their leaves (Hutchinson and Wollack, 1943; Robinson and Edgington, 1945; Chenery, 1948a). Our knowledge of Al accumulators is built mainly on the substantial contributions made by Chenery starting some 50 years ago (Chenery, 1946a, b, 1948a, b, 1949). Chenery and Sporne (1976) concluded that Al accumulation is a primitive character mainly characteristic of woody and tropical representatives of fairly advanced families (e.g. Anisophylleaceae, Hydrangeaceae, Melastomataceae, Rubi aceae, Theaceae, Symplocaceae, Vochysiaceae). The feature has been suggested to provide useful systematic information at different taxonomic levels in recent phylogenetic studies of the angiosperms (Jansen et al., 2002a). With respect to other metals, there is a significant variation in shoot heavy metal content at the classification level of order or above, which implies that these differences can be attributed to rather deep evolutionary processes. Accordingly, it is suggested that phylogeny influences the trait of heavy metal accumulation in flowering plants (Broadley et al., 2001).

To date, Al accumulation has been found in 52 families according to the Angiosperm Phylogeny Group (APG) system, which largely belong to the eudicots (APG, 1998). Although the largest number of Al‐accumulating species is suggested to occur in the Rubiaceae (Gentianales), the family Melastomataceae (Myrtales) probably has just as many accumulators (Chenery, 1948b). Species of the Rubiaceae and Melastomataceae are among the most abundant and diversified plant families throughout the tropics. Moreover, it had already been noticed in the 18th century that leaves of Memecylon edule Roxb. were used by dyers in southern India as a mordant in place of alum (Hutchinson, 1943). Indeed, the traditional use of plants as a mordant has revealed many cases of Al‐accumulating plants, especially in South East Asia. Furthermore, Kukachka and Miller (1980) suggested that within the family Melastomataceae, systematic trends might be evident as all or many of the genera studied in this family show high Al concentrations in the wood.

The Melastomataceae include about 4500 species in approx. 166 genera, while their traditional relatives, the Memecylaceae, comprise approx. 430 species and six genera (Renner, 1993). Their intrafamilial classification was poorly understood and relied largely on the system of Triana (1871). Recently, a cladistic analysis of morphological and anatomical characters resulted in a new subfamilial and tribal classification (Renner, 1993). This system has now been tested, based on analyses of sequences from the rbcL and ndhF genes and the rpl16 intron (Clausing and Renner, 2001). Moreover, rbcL data showed 100 % bootstrap support for a Memecylaceae and Melastomataceae clade (Conti et al., 1996, 1997), and monophyly of these families is also well supported (98 %) in the strict consensus tree according to Clausing and Renner (2001).

Based on semi‐quantitative Al analyses of wood and leaves, we have already given attention to Al accumulators in the family Rubiaceae (Jansen et al., 2000a, b). The present paper focuses on the occurrence of Al accumulators in Melastomataceae. We therefore examined leaves of herbarium material since the leaves of accumulating species generally contain high concentrations of Al. It is our aim to review the distribution of Al in representatives of all tribes and subfamilies, and to determine the systematic value of the feature in view of recent phylogenetic insights. A summary of the literature data allows a comparison of our results with earlier data. Finally, suggestions are presented on the evolution of Al accumulation in the order Myrtales. Further understanding of the distribution and evolution of Al accumulators and the physiological processes may contribute to the development of more resistant crops or plants that can be used for food, forage for animals or for recuperation of degraded lands.

MATERIALS AND METHODS

Leaves of Crypteroniaceae, Melastomataceae, Memecyl aceae and Oliniaceae were mainly collected from the herbarium of the National Botanic Garden of Belgium (BR); only for a few samples was material from other herbaria used. All 166 specimens tested are listed in the Appendix.

High Al concentrations in leaves were detected according to the ‘aluminon’ test as described by Chenery (1948b) and followed by Jansen et al. (2000b). This simple but adequate test allows accumulators and non‐accumulators to be identified by assessing the intensity of colour: crimson to dark red or red for accumulators, and various colours from pink to yellow or dark brown for non‐accumulators.

The feature was plotted on a molecular phylogenetic tree for Melastomataceae and Memecylaceae (Clausing and Renner, 2001), as well as for the order Myrtales (Conti et al., 1997; Savolainen et al., 2000; Wilson et al., 2001) using MacClade 4·0 (Maddison and Maddison, 2000). The classification of Renner (1993) is followed throughout this paper.

Numerous members of the Memecylaceae and Melastomataceae accumulate more than 10 000 mg kg–1 in their leaves and can therefore be labelled as Al ‘hyperaccumulators’. Since precise quantitative data on Al content are beyond the scope of this study, we use the term ‘accumulation’ and ‘accumulators’ throughout this paper for all accumulating plants, even though the exact Al content may well be above 10 000 mg kg–1.

RESULTS

In 57 specimens the leaf tests produced a crimson colour. In 22 specimens the colour turned red to dark red, whereas a negative test was found for all other specimens tested. In only a few specimens did the pinkish or light‐red colour of the reagent remain unchanged; this may indicate that the Al content was slightly above average in the leaves, but cannot be interpreted as typical of accumulators.

Within the Memecylaceae, all specimens tested were positive except one specimen of Memecylon dichotomum. Many accumulators were found in the Kibessieae, Astronieae, Miconieae and Microlicieae. The genera in which the Al‐test produced a red to dark‐red colour included Huberia (Merianeae), Rhexia (Rhexieae), Chaetostoma and Microlicia (Microlicieae), and several members of the Melastomateae and Miconieae. Positive and negative specimens occurred in the Oxyspora alliance of the Sonerileae, while numerous species of the Sonerila–Bertolonia–Gravesia alliance, the Melastomeae and Miconieae reacted negatively. Negative tests were also obtained for all Blakeeae.

Positive tests were found for Rhynchocalyx (Rhynchocalycaceae), Axinandra and Crypteronia (Crypteroniaceae), but a specimen of Dactylocladus (Crypteroniaceae) was negative. Non‐accumulating specimens were obtained for all specimens of Alzateaceae, Combretaceae, Heteropyxidaceae, Myrtaceae, Oliniaceae, Penaeaceae and Psiloxylaceae.

For most species investigated here, only one leaf sample was tested. However, for five species two specimens were investigated. There was a striking difference between the two specimens of Memecylon dichotomum, with one sample producing a crimson colour and the other being clearly negative. The specimens of Crypteronia paniculata differed to a lesser extent. No differences were found between the different specimens of the other species; the specimens of Melastromastrum segregatum were distinctly positive, whereas the samples of Arthrostemma ciliatum and Maieta guianensis were negative.

DISCUSSION

Al accumulation in Memecylaceae and Melastomataceae compared with earlier results

In general, our observations agree well with the earlier Al‐tests for leaves (see Table ​Table1).1). Chenery (1946a, 1948a, b) detected the major groups in which Al accumulation is dominant, namely Memecylaceae, Kibessieae, Astronieae, Merianeae, Rhexia (Rhexieae), Microlicieae and Mico nieae. In only a small proportion of the genera tested are there specimens that proved to be negative according to our tests, while all specimens tested by Chenery (1948a, b) were positive, namely Cambessedesia, Conostegia, Dionycha, Gravesia, Loreya, Mecranium, Osbeckia and Pachyloma. On the other hand, Al accumulation was detected in Dinophora and Sandemania, but the single specimens of these genera were negative according to Chenery (1948b). Moreover, the specimens of Behuria and Meriania tested here gave a light‐red colour, which indicates that Al levels are not very far below 1000 mg kg–1, so that the presence of accumulation is not remarkable in other species or specimens.

Table 1.

Survey of Al‐accumulating taxa in Melastomataceae and Memecylaceae

Family: tribeGenera studied
MemecylaceaeLijndenia (2/2)7; Memecylon1, 5 (9/9)2 (187/192)6 (2/3)7; Mouriri1, 5 (8/8)3 (33/38)6 (1/1)7; Spathandra (1/1)7; Votomita (2/2)7; Warneckea (1/1)3
Melastomataceae
KibessieaePternandra5 (2/2)2 (9/9)3 (1/1)7 (incl. Kibessia5)
AstronieaeAstrocalyx5 (2/2)3; Astronia5 (2/2)4 (7/8)3 (1/1)7; Astronidium5; Beccarianthus5 (2/2)7 (incl. Bamlera)
Sonerileae: (Oxyspora alliance)Anerincleistus (4/4)3 (1/1)7 [incl. Pomatostoma (2/2)3, Creaghiella (1/1)3, Oritrephes (1/1)3, Plagiopetalum (0/1)3, Phaulanthus (4/4)3]; Barthea (2/2)3 (1/1)7; Blastus (1/3)3 (0/1)7; Bredia (1/3)3 (1/1)7; Driessenia (2/3)3 (1/1)7; Ochthocharis (2/2)3(1/1)7; Oxyspora (4/4)3 (1/1)7 [incl. Allomorphia (5/5)2, 3, Campimia (0/1)3]; Poikilogyne (1/3)3 (0/1)7
Sonerileae: (Sonerila–Bertolonia– Gravesia alliance)Amphiblemma (0/2)3; Bertolonia (1/3)3 (0/1)7; Calvoa (0/3)3; Centradenia (0/2)3 (0/1)7; Cincinnobotrys (0/1)3; Cyanandrium (2/2)3; Dicellandra (0/1)3; Diplarpea (0/1)3; Fordiophyton (0/2)3 (0/1)7; Gravesia (2/2)3 (0/1)7 [incl. Veprecella (0/4)3, Petalonema (0/1)3]; Macrocentrum (2/5)3 (1/1)7; Monolena (0/1)3 (0/1)7; Opisthocentra (1/1)3; Phyllagathis (3/5)3 (0/2)7; Preussiella (0/1)3 (0/1)7; Salpinga (0/2)3 (0/1)7; Sarcopyramis (0/1)3 (0/1)7; Sonerila (0/8)3 (0/1)7; Triolena (0/2)3 (0/1)7 [incl. Diolena (0/1)3]
MerianeaeAdelobotrys1,5 (3/4)3; Axinaea (4/5)3 (2/2)7; Behuria (1/1)3 (0/1)7; Centronia5 (4/4)3; Graffenrieda5 (1/1)3 (2/2)7 [incl. Calyptrella5 (2/2)3]; Huberia (3/3)3 (1/1)7; Meriania1, 5 (2/2)3 (0/1)7; Pachyloma5 (3/3)3 (0/1)7
RhexieaeRhexia (5/5)3 (3/3)7
MicrolicieaeBucquetia (1/2)3 (1/2)7; Cambessedesia (2/2)3 (0/1)7; Castratella (1/1)3; Chaetostoma (2/3)3 (1/2)7; Eriocnema (2/2)3; Lavoisiera (6/6)3 (1/1)7; Lithobium (0/1)3; Microlicia (5/6)3 (2/2)7; Rhynchanthera (3/4)3 (1/1)7; Stenodon (1/1)3 (1/1)7; Trembleya (3/4)3 (2/2)7
Melastomeae
Paleotropical generaAmphorocalyx (1/1)7; Antherotoma (1/1)3 (1/1)7; Dichaetanthera5 (4/4)3 (1/1)7 [incl. Sakersia (2/2)3]; Dinophora (0/1)3 (1/1)7; Dionycha (3/3)3 (0/1)7; Dissotis (4/4)2 (10/17)3 (1/2)7; Guyonia (0/1)3 (0/1)7; Heterotis (0/1)7; Melastoma1 (1/1)4 (7/7)2, 3 (41/41)6; Melastomastrum (3/3)7; Nerophila (1/1)3 (1/1)7; Osbeckia1 (7/8)3 (0/1)7 [incl. Rousseauxia (1/1)3, Otanthera (3/3)3 (1/1)7, Pseudobeckia (1/1)7, Tristemma (4/6)3 (0/1)7]
Neotropical generaAcanthella (0/1)3; Aciotis (0/5)3 (0/1)7; Acisanthera (0/2)3 (0/1)7; Appendicularia (0/1)3 (0/1)7; Arthrostemma (0/3) (0/2)7; Brachyotum (1/1)2 (20/21)3 (1/1)7; Chaetolepis (0/3)3 (0/1)7; Comolia (0/1)3 (0/1)7; Desmoscelis (1/1)3 (1/1)7; Ernestia (0/3)3 (0/1)7; Fritzschia (0/2)3 (0/1)7; Heterocentron (0/2)7; Loricalepis (1/1)3; Macairea (1/3)3 (0/1)7; Marcetia (1/5)3 (0/1)7; Microlepis (2/2)3 (1/1)7; Monochaetum (0/12)3 (0/1)7; Nepsera (0/1)3 (0/1)7; Pilocosta (2/2)7; Poteranthera (1/1)3; Pterogastra (1/1)7; Pterolepis (0/2)3 (0/1)7; Sandemania (0/1)3 (1/1)7; Schwackaea (0/1)7; Siphanthera (0/2)3 (0/1)7; Svitramia (1/1)3 (1/1)7; Tibouchina (59/65)3 (1/2)7 [incl. Itatiana (1/1)3]; Tibouchinopsis (0/1)7
Miconieae
Paleotropical generaCatanthera (0/1)7 [incl. Hederella (0/1)3]; Creochiton (1/1)7 [incl. Eisocreochiton (1/1)3; Diplectria (2/2)7 [incl. Anplectrum (1/1)2 (8/8)3]; Dissochaeta (4/4)3 (1/1)7 [incl. Omphalopus (3/3)2, Dalenia (1/1)2, 3]; Kendrickia (0/1)3 (0/1)7; Macrolenes (2/2)7; Medinilla (0/16)3 (0/1)7 [incl. Carionia (1/3)3, Cephalomedinilla (0/1)3]; Pachycentria (0/4)3 (0/1)7; Plethiandra (0/2)3; Pogonanthera (0/2)3 (0/1)7
Neotropical generaAllomaieta (1/1)3; Anaectocalyx (0/1)3 (0/1)7; Bellucia5 (2/2)3 (1/1)7 [incl. Loreya (2/2)3]; Calycogonium (1/2)3 (0/1)7 [incl. Mommsenia (0/1)3]; Catocoryne (0/1)3; Charianthus1, 5 (1/2)3 (0/1)7; Clidemia1, 5 (19/21)2, 3 (1/1)7 [incl. Heterotrichum1 (2/2)3]; Conostegia1, 5 (1/1)2 (5/5)3 (0/1)7; Henriettea1, 5 (4/4)3 (1/1)7; Henrietella1 (1/1)3 (2/2)7; Leandra1 (5/5)2, 3 (137/144)6 (1/1)7 (incl. Platycentrum1); Llewelynia5; Loreya5 (0/1)7; Maieta1(1/2)3 (0/2)7; Mecranium1 (3/3)3 (0/1)7; Miconia1, 5 (62/68)2, 3 (314/384)6 (1/1)7; Myriaspora (2/2)3 (1/1)7; Myrmidone (0/1)3 (0/1)7 [incl. Hormocalyx (1/1)3]; Necramium1; Ossaea1, 5 (4/4)2, 3 (1/1)7; Pachyanthus (1/2)3 (0/1)7; Pleiochiton (0/5)3 (0/1)7; Tetrazygia1, 5 (5/5)2, 3 (1/1)7; Tococa1, 5 (3/3)3 (1/1)7 [incl. Microphysca (1/1)3]
BlakeeaeBlakea1 (1/10)3 (0/1)7; Topobea (0/4)3 (0/1)7

Data according to Chenery (1946a, b)1, Chenery (1948a)2, Chenery (1948b)3, Webb (1954)4, Kukachka and Miller (1980)5, Metcalfe and Chalk (1983)6 and own tests7.

Genera in bold have one or more positive specimens; genera not in bold type are negative; if known, the nominator in parentheses gives the number of Al‐accumulating specimens, the denominator is the total number of specimens tested.

There is also good general agreement between the Al‐tests for leaves and Al accumulation in the secondary xylem, as reported by Kukachka and Miller (1980). However, these authors did not mention negative wood tests in their paper. Except for Dichaetanthera, all genera that reacted positively in wood tests belong to the Memecylaceae, Kibessieae, Astronieae, Merianeae and Miconieae. It is suggested that taxa with positive wood tests largely correspond with genera or species that show Al accumulation in the leaves, but two counter examples exist, namely Charianthus and Loreya. Similar results were obtained by comparing wood and leaf tests in Rubiaceae (Jansen et al., 2000a, b) and it was concluded that Al is more strongly accumulated in leaves than in wood. However, a more detailed study of wood samples is needed to test this hypothesis in members of the Myrtales. Furthermore, most Al accumulators also show high Al levels in tissues of the bark, seeds and fruits. In some representatives of Memecylaceae (Memecylon, Miconia), Myrtaceae (Eugenia) and Vochysiaceae (Qualea, Vochysia), Al concentrations have been reported to be even higher in the bark than in the leaves (Silva, 1990; Masunaga et al., 1998c). The lower Al levels in secondary xylem could be linked with observations that localization of Al in the leaves of some Al accumulators is mainly in the phloem elements (Haridasan et al., 1986). This may indicate that Al in accumulators is transported in higher concentrations through the phloem than the xylem.

The results summarized in Table 1 indicate that Al accumulation is either totally absent or present in a large number of genera. Genera with a very large number of Al accumulators include Clidemia (20 accumulators out of 21 species tested), Leandra (137 out of 144), Melastoma (41 out of 41), Memecylon (187 out of 192), Miconia (314 out of 384), Mouriri (33 out of 38) and Tibouchina (60 out of 67). In contrast, Al accumulation appears to be entirely lacking in Medinilla (zero out of 17), Monochaetum (zero out of 13), Sonerila (zero out of nine) and Pleiochiton (zero out of six). In only a limited number of genera do accumulating and non‐accumulating species occur in more or less equal numbers: Bredia (two out of four), Chaetostoma (three out of five), Dissotis (15 out of 23), Macrocentrum (three out of six), Phyllagathis (three out of seven) and Tristemma (four out of seven). In most other genera, from which a number of representatives have been tested, the majority of specimens are either positive [e.g. Astronia (ten out of 11), Driessenia (three out of four)] or negative [e.g. Bertolonia (one out of four), Blakea (one out of 11), Poikilogyne (one out of four)]. This implies that, in general, the character is rather consistent at the generic level, which is in accordance with the general consistency found in Rubiaceae and several other angiosperm families (Jansen et al., 2000a, b, 2002a).

Table 2 shows a literature survey of Melastomataceae and Memecylaceae with exact Al concentrations in their leaves. The old data summarized by Hutchinson (1943) are not included as these represent Al percentages of ash analyses. Except for a specimen of Memecylon, all species in Table 2 have an Al content above 4000 mg kg–1. A specimen of Miconia acinodendron has even been found to accumulate 66 100 mg kg–1 Al in its leaves—the second highest Al content detected in any plant (Chenery, 1948b). Moreover, nearly all specimens of these genera react positively in the semi‐quantitative tests. It is suggested that the precise Al concentration is correlated with the number of positive and negative specimens for each genus or species. A similar congruence between the mean relative leaf Al content and the number of accumulating species within a genus is demonstrated in Rubiaceae, for instance (Jansen et al., 2002b). However, more quantitative analyses are needed to verify this for the Memecylaceae and Melastomataceae.

Table 2.

Exact quantitative data on Al concentration in leaves of Memecylaceae and Melastomataceae according to literature data

Family: tribeSpeciesAl concentration in leaves (mg kg–1)Reference
Memecylaceae Memecylon arnottianum >10 000Chenery (1946)
Memecylon laurinum 30 500Masunaga et al. (1998a)
Memecylon polyanthemos >10 000Chenery (1946)
Memecylon sp.970 Masunaga et al. (1998c)
Melastomataceae
Kibessieae Pternandra caerulescens 16 640Masunaga et al. (1998c)
Melastomeae Acisanthera uniflora 20 200Sarmiento (1984)
Melastoma malabathricum >10 000Moomaw et al. (1959); Watanabe et al. (1997, 1998b)
Merianeae Graffenrieda latifolia 7028Cuenca and Herrera (1987)
Miconieae Clidemia pustulata 7910Chenery (1948a)
Henriettea succosa 21 900Chenery (1948a)
Miconia acinodendron 66 100Chenery (1948a)
Miconia ciliata 16 500Chenery (1948a)
Miconia dodecandra 5280Cuenca and Herrera (1987)
Miconia ferruginata 4310Haridasan (1982)
Miconia nervosa 9160Chenery (1946)
Miconia pohliana 6630Haridasan (1982)
Miconia stephanthera 6899Mazorra et al. (1987)

The differences noted above between our results and earlier data on Al accumulation might well be caused by inter‐ or intraspecific variation within a certain genus. Moreover, variation in Al concentration among individuals of a species or between different species of a genus may be due, to some extent, to differences in growing conditions. It is well known that environmental influences, especially soil pH, determine the amount of soluble and toxic Al in the soil. Whilst some Al accumulators are restricted to acid soils, others are indifferent, and at least one Al accumulator, namely Callisthene fasciculata (Vochysiaceae), has been reported to occur only in calcareous soils in central Brazil (Haridasan and Araújo, 1987). There is also seasonal variation in Al levels in plant organs (Mazorra et al., 1987). Hence, one must be careful in concluding that a genus or species is an Al accumulator, or that Al accumulation is completely absent, based on a limited number of tests. Also, one may not exclude the possibility that some of the herbarium specimens tested are misidentified. Unfortunately, the publications of Chenery (1948a, b) give no information at the species level and do not refer to herbarium material.

The systematic significance of Al accumulation in Memecylaceae and Melastomataceae

The distribution of Al accumulators is plotted on a molecular phylogenetic tree for Melastomataceae and Memecylaceae (Clausing and Renner, 2001; Fig. 1). It is clear that Al accumulation is most common in the primitive taxa of the Melastomataceae, especially Kibessieae, Astronieae, Merianeae and Miconieae, and, except for a few specimens, the feature characterizes all members of the Memecylaceae, which include primary forest trees or more rarely shrubs. Most of the species in these taxa probably represent strong accumulators. Most interesting is the fact that the primitive status of Al accumulation, as suggested on the basis of statistical correlations (Chenery and Sporne, 1976), is also supported for the study group. Indeed, the tribes that are entirely or almost completely characterized by Al accumulators are primitive. This implies that Al accumulation represents a primitive (plesiomorphic) character state, which is inherited from the common ancestor of Memecylaceae and Melastomataceae. Similarly, the presence of Al accumulators is mainly restricted to the basal Rubioideae among the Rubiaceae (Jansen et al., 2000a, b) and basal alliances within, for instance, the Polygalaceae or the asterids (Jansen et al., 2002a).

An external file that holds a picture, illustration, etc. Object name is mcf142f1.jpg

Fig. 1. The distribution of Al accumulation plotted on the strict consensus tree for Melastomataceae and Memecylaceae based on rbcL, ndhF and rpl16 data (Clausing and Renner, 2001); data summarized from Table 1; the nominator gives the number of Al‐accumulating specimens, the denominator is the total number of specimens tested.

Since the feature is much more variable in the derived members of the Melastomataceae, Al accumulation shows poor phylogenetic signals, and allows only few systematic implications within this family. The genus Macrocentrum was traditionally placed in Bertolonieae, but falls at the base of the Miconieae and Merianieae (Clausing and Renner, 2001). The presence of Al accumulation in at least part of the Macrocentrum specimens tested can be interpreted as additional support for this position, since most members of the Bertolonieae (Bertolonia, Triolena and Monolena) are non‐accumulators. However, this may also be explained by the occurrence of epiphytes in this group (see below).

The large number of Al accumulators also supports the relationship between the Rhexieae and Microlicieae. The genus Arthrostemma, however, which was placed in the Melastomateae following Renner (1993), shows a conspicuous lack of accumulation, but this is probably due to its herbaceous habit (see below). Species of Arthrostemma are erect or somewhat perennial herbs (Almeda, 1994), but Rhexia frequently comprises woody shrubs.

Hypotheses on the absence of Al accumulation in some Melastomataceae

The lack of Al accumulation in numerous more or less derived clades of the Melastomataceae needs special attention. One possibility is that the habit may be a selective factor for high Al concentrations in the leaves. Except for some remarkable exceptions, it is well known that herbs generally do not accumulate (Chenery, 1948a, b, 1949), but the physiological processes for this relationship are still not understood. The tendency to herbaceousness in several more derived branches of the Melastomataceae tends to be closely related to a relatively low shoot Al content. For example, the tribe Miconieae shows a striking difference in the number of accumulators between the palaeotropical genera (approx. 40 % positive) and the neotropical genera (approx. 80 % positive) (Table 1). The most likely explanation for this contrast is that the palaeotropical Miconieae are more herbaceous and include to a lesser extent trees or treelets. A similar explanation may be given for the two groups in the Sonerileae. The Oxyspora alliance shows many more positive members (76 %) compared with the Sonerila–Bertolonia–Gravesia alliance, in which only 19 % of the specimens tested are positive (Table 1). Nevertheless, several counter examples of herbaceous genera include accumulating specimens [e.g. Phyllagathis (three out of six), Castratella (one out of one), Eriocnema (two out of two), Pterogastra (one out of one)]. Equally, several woody taxa show no accumulation [e.g. Amphiblemma (zero out of two), Comolia (zero out of two), Chaetolepis (zero out of four), Ernestia (zero out of four), Heterocentron (zero out of two), Monochaetum (zero out of 13)]. Hence, it is not a simple matter to determine whether changes in form or habit precede changes in Al response mechanisms.

Besides this difference in Al uptake between the woody and herbaceous habit, there might also be a divergence between the perennial or annual condition. The absence of high Al levels might well be caused by the epiphytic habit. Al concentrations in leaves of mistletoes parasitizing plants from the cerrado belt of Brazil depend on the nature of the host species. The same hemiparasite will show high Al levels if it is growing on Al accumulators, but low Al levels when it is growing on a non‐accumulating host (Lüttge et al., 1998). Genera with epiphytic or hemiepiphytic species include Blakea, Medinilla, Monolena, Topobea and Triolena, and some 300 of the 350 Dissochaeteae known are facultative or obligate epiphytes (Clausing et al., 2000). Most specimens of these genera are non‐accumulators, which is in contrast with the consistent presence in the woody shrubs or root climbers of Diplectria (Fig. 1). It would be interesting to know whether or not epiphytic members of the Melastomataceae are able to accumulate Al when growing on an Al‐accumulating host plant. This may illustrate that Al accumulation has not been lost during evolution, but is simply not expressed in most of the epiphytes analysed in this study.

Two other reasons can be suggested to explain the absence of accumulation in numerous Melastomataceae: (1) differences in environmental conditions (especially soil pH); and (2) the possible acquisition of new Al‐response mechanisms in more derived groups, which may be more cost‐effective and safer, to deal with the toxic Al in acid soil. Since the concentration of soluble and toxic Al depends strongly on the pH of the soil, it is possible that the non‐accumulating taxa grow on less acid soils. Hence, the variation within a genus or species can sometimes be explained by differences in soil acidity. It is not a simple matter, however, to consider the environmental influences without detailed information of growing conditions. Unfortunately, no precise data are available when using herbarium material, and fieldwork is required for further investigation of ecological conditions on Al accumulation. Moreover, in tropical rainforests, Al accumulators and excluders which coexist at the same sites vary greatly in leaf Al concentrations (e.g. Haridasan, 1982; Cuenca and Herrera, 1987, 1988). For example, in leaves from 608 tropical rainforest trees in west Sumatra, the Al content varied from 6 to 36 920 mg kg–1 (Masunaga et al., 1998b, c). This clearly indicates that plants colonizing acid soils may successfully use different strategies and that these are not entirely under environmental control.

Al accumulation in other Myrtales

The distribution of Al accumulators in all families of the Myrtales sensu APG (1998) is summarized in Table 3. Besides Melastomataceae and Memecylaceae, Al accumulation is very common in the Vochysiaceae. All wood samples of the Vochysiaceae tested reacted positively (Kukachka and Miller, 1980), and almost all representatives of the family are accumulators (Chenery, 1948b; Metcalfe and Chalk, 1983). Although the latter authors admitted that some of the tests proved to be negative when tested again, it is clear that very high Al levels are characteristic of this family. Indeed, the greatest amount of Al detected by Kukachka and Miller (1980) was found in Vochysia hondurensis Sprague, which contained 325 500 mg kg–1 in ash or 7779 mg kg–1 in wood. High Al levels are also found in nearly all members of the Crypteroniaceae and in two samples of Rhynchocalyx (Rhynchocalycaceae).

Table 3.

Aluminium accumulation in Myrtales

FamilyGenera studied
AlzateaceaeAlzatea (0/1)6
Combretaceae (0/5)1 (0/6)2 (2/21)5; Combretum (0/1)6; Quisqualis (0/1)6; Strephonema (0/1)6
Crypteroniaceae (7/8)1; Axinandra (1/1)5 (2/2)6; Crypteronia (3/3)6; Dactylocladus (0/1)6
HeteropyxidaceaeHeteropyxis (0/?)1 (0/1)6
Lythraceae(0/10)1
Melastomataceae Numerous representatives positive (see Table 1)
Memecylaceae Almost entirely positive (see Table 1)
Myrtaceae (0/11)1; (0/66)2; Calyptranthes (0/1)6; Eugenia (3/?)4 (26/104)5; Kjellbergiodendron (0/1)6; Lophostemon (0/1)6; Whiteodrendron (0/1)6; Xanthostemon (4/12)5
OliniaceaeOlinia (0/3)1 (0/4)5
Onagraceae(0/7)1 (0/1)2
PenaeaceaeBrachysiphon (0/1)6; Endonema (0/2)6; Glischrocolla (0/1)6; Penaea (0/2)6
PsiloxylaceaePsiloxylon (0/1)6
Rhynchocalycaceae Rhynchocalyx (1/1)5 (1/1)6
Vochysiaceae Callisthene3 (3/3)1; Erisma3 (3/3)1 (4/5)5; Erismadelphus3 (1/1)1 (2/2)5; Qualea3 (6/6)1 (49/59)5; Salvertia3 (1/1)1, 5; Vochysia3 (78/78)1, 5

Data from Chenery (1948a)1, Webb (1954)2, Kukachka and Miller (1980)3, Masunaga et al. (1998c)4, Metcalfe and Chalk (1983)5, own tests6; ? = unknown; if known, the nominator in parentheses gives the number of Al‐accumulating specimens, the denominator is the total number of specimens tested; taxa in bold include Al accumulators; non‐accumulating taxa are not bold.

On the other hand, the feature seems to be completely absent in Alzateaceae, Heteropyxidaceae, Lythraceae, Oliniaceae, Onagraceae, Penaeaceae and Psiloxylaceae. Although most members of the Myrtaceae and Combretaceae appear to be negative, a few specimens at least have been reported to be accumulators. Masunaga et al. (1998c) detected high Al concentrations in leaves of three species of Eugenia (Myrtaceae), but in six other species of this genus the Al content was below 1000 mg kg–1 in the leaves. Positive leaf‐tests were also reported for Eugenia as well as for Xanthostemon (Metcalfe and Chalk, 1983). The latter genus has recently been suggested to occupy the most basal position within the Myrtaceae, but the inclusion of Eugenia in the myrtoid clade suggests a much more derived position (Wilson et al., 2001). Only two positive specimens are known for the Combretaceae (Table ​(Table33).

The distribution of Al accumulators is plotted on a hypothetical tree that is based on recent phylogenetic analyses of rbcL gene sequences (Conti et al., 1997; Savolainen et al., 2000; Wilson et al., 2001; Fig. 2). The present evidence on Al accumulation implies that the character is mainly restricted to the basal families in the Melastomataceae and Myrtaceae lineage, but is absent or very rare in the clade including Onagraceae, Lythraceae s.l. and Combretaceae. It is suggested that Al accumulation has been lost several times within the order: (1) in Onagraceae, Lythraceae s.l. and Combretaceae; (2) in Myrtaceae, Psiloxylaceae and Heteropyxidaceae; and (3) in Oliniaceae, Penaeaceae and Alzateaceae. Furthermore, Al accumulation confirms, to some extent, phylogenetic relationships between Memecylaceae and Melastomataceae, with the Crypteroniaceae and Rhynchocalycaceae as the Al‐accumulating branches in its sister clade. Vochysiaceae possibly take the most basal position within the Myrtaceae alliance. Traditionally, the taxonomic position of the Vochysiaceae is in the Polygalales, and its placement in the Myrtales has been proposed only recently based on molecular data (Conti et al., 1996, 1997). Morphological characters such as vestured pits, bicollateral vascular bundles and several embryological features provide additional support for this position (Boesewinkel and Venturelli, 1987; Baas et al., 2000; Jansen et al., 2001).

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Fig. 2. Al accumulation plotted on a hypothetical tree of the order Myrtales that is based on rbcL gene sequences (Conti et al., 1997; Savolainen et al., 2000; Wilson et al., 2001), with ACCTRAN character state optimatization.

More data are required to comment on the probably very sporadic occurrence of Al accumulation in Combretaceae and Myrtaceae. The distribution of Al accumulators in the Myrtaceae may be associated with the occurrence of typical ectomycorrhizal associations. It is generally considered that most members of this family have dual ectomycorrhizal associations (ECM) and vesicular–arbuscular mycorrhizae (VAM). These mycorrhizal associations possibly limit transport of Al into plant roots since the cell walls of fungi are known to have strong affinities for metallic cations (e.g. Ashida et al., 1963; Duddrige and Wainwright, 1980). Contrary to this, however, mycorrhizal associations may also lead to higher Al concentrations in above‐ground tissues of some plants (e.g. Liriodendron, Magnoliaceae; Lux and Cumming, 2001).

Al accumulation and the colour of fruits, flowers and leaves

It is well known that colour changes of Hydrangea (Hydrangeaceae) flowers are due to changes in internal Al levels: the change from pink to blue is associated with the formation of pigments that include Al (Chenery, 1946a, 1948a; Takeda et al., 1985; Ma et al., 1997). Chenery (1946a, 1948a) suggested that the correlation between blue flowered and/or fruited species holds true for many Al accumulators, but certainly not all plants with blue flowers or fruits are Al accumulators.

It is possible that the high Al content plays at least some role in the formation of blue, pink or purple pigments in the accumulators of Melastomataceae and related families. Most Melastomataceae and Memecylaceae have white to purple petals, varying from pink to magenta. For instance, purple flowers are common in Dichaetanthera, Meriania, Mouriri, Rhynchanthera and Tibouchina, which usually include accumulators, but several examples can be given of accumulators that do not have blue flowers. Experimental work on Melastoma malabathricum did not show changes in flower colour when plants were cultivated on soils of different pH (T. Watanabe et al., pers. comm.). Apparently, variation in flower colour in a species or genus does not depend solely on Al content in the above‐ground plant tissues. In Vochysiaceae, for instance, some Al accumulators show remarkable blue flowers, while others have brilliantly yellow inflorescences in the flowering season (e.g. Lüttge, 1992).

Blue to dark blue, purple or black fruits are more widespread in the Melastomataceae and Memecylaceae than are blue flowers. For instance, they occur in species of Clidemia, Leandra, Miconia and Melastoma. The name of the latter genus comes from the fleshy placentas, which usually are dark blue to black (Greek ‘melanos’) and which stain the mouth (Greek ‘stoma’) intensively when eaten. A more detailed list of Al accumulators with blue flowers and fruits was presented by Chenery (1948a).

Another diagnostic character of Al accumulators is the presence of rather thick, leathery leaves that are typically yellow‐green to dark green (Chenery, 1948a, b). Most of the Al accumulators in the Myrtales (e.g. Vochysiaceae) seem to possess this feature. Nevertheless, application of the Al‐test is recommended to determine more precisely the presence or absence of high Al levels rather than leaf colour alone.

Some physiological aspects of Al accumulation

Organic acids play a central role in alleviating Al toxicity. Some plants detoxify Al by exudation of organic acids which chelate Al in the rhizosphere. Other plants, including Al‐accumulating Melastomataceae, detoxify Al in their leaves by forming complexes with organic acids (Ma, 2000; Ma et al., 2001). In Melastoma malabathricum L., the form of Al in the leaves was identified as monomeric Al3+, Al‐oxalate, Al‐(oxalate)2 and Al‐(oxalate)3 (Watanabe et al., 1998b). The form of Al is also shown to be an Al‐citrate complex during transport from the roots to the shoots, but is transformed into an Al‐oxalate complex for Al storage in the leaves (Watanabe et al., 2001; Watanabe and Osaki, 2001). Primary accumulation sites of Al in the leaves of this genus are considered to be the apoplast and/or vacuole, in which the harmful effects of excess Al may be limited (Watanabe et al., 1998b).

Plants that are adapted to acidic soils and high levels of Al do not usually show symptoms of Al toxicity. For instance, Plucknett et al. (1963) found no Al‐induced root damage in Melastoma malabathricum L. (Melastomataceae) and Rhodomyrtus tomentosa Wight (Myrtaceae) growing in aluminous soils on Hawaii. Moreover, the growth of Melastoma malabathricum is stimulated by Al (Osaki et al., 1997) and this stimulation is primarily caused by the Al element itself in the plant tissue rather than by the stimulation of P uptake (Watanabe et al., 1997, 1998a; Watanabe and Osaki, 2001). It is also concluded that Al drastically changes the organic acid metabolism of Melastoma, which may affect growth (Watanabe and Osaki, 2001). Similarly, Al‐enhanced growth is reported in Miconia albicans (Sw.) Triana (Melastomataceae). The natural environment of this accumulator is the acid latosols of the cerrado region of central Brazil. This species grows poorly on calcareous soils, but when some of its roots are exposed to distilled water containing Al, its growth is improved (Haridasan, 1988). In the same way, Vochysia thyrsoidea Pohl (Vochysiaceae) does not grow in the absence of Al. Hence, Al seems to be a beneficial element for at least some representatives of the Melastomataceae and Vochysiaceae, but its possible role in the metabolism of these Al accumulators requires further investigation. The physiological studies mentioned above are restricted to a small number of species, thus further studies are clearly required to demonstrate whether these results can be generalized to other accumulators in the Melastomataceae and related families.

ACKNOWLEDGEMENTS

We thank Anja Vandeperre (K. U. Leuven) for help with the aluminium tests, Dr K. Meyer (University of Mainz) for useful suggestions and supplying leaf material, and Dr Haridasan for helpful comments. We also thank the director of the National Botanic Garden of Belgium and the Keeper of the Kew Herbarium for the use of herbarium material. Research at the Laboratory of Plant Systematics is supported by grants from the Research Council of the K. U. Leuven (OT/01/25) and the Fund for Scientific Research–Flanders (Belgium) (G.104·01). S.J. is a postdoctoral fellow of the Fund for Scientific Research–Flanders (Belgium) (F.W.O.–Vlaanderen).

APPENDIX

List of material studied

All specimens from the National Botanic Garden of Belgium (BR), unless otherwise noted; specimens in bold are accumulators; non‐accumulators are those not in bold font.

Alzateaceae – Alzatea verticillata Ruiz and Pav., Peru, Rio Negro, Dept. San Martin, F. Woytkowski 6196 (K).

Combretaceae – Combretum grandiflorum G.Don, Sierra Leone, Tiama near Njala, D.Small 392 (K); Quisqualis latialata (Engl. ex Engl. and Diels) Exell, Democratic Republic of Congo‐Kinshasa, Leopoldville, Matadi, Gimbi, L. Toussaint 813 (K); Strephonema pseudo‐cola A.Chev., Liberia, Ganta, W.J. Harley 1020 (K).

Crypteroniaceae – Axinandra zeylanica Thwaites, Robyns 7285; A. zeylanica Thwaites, A.J.Kostermans 24632; Crypteronia cumingii Endl., G.E. Edano 37179; C. paniculata Blume, M.D. Sulit 6990; C. paniculata Blume, Soejarto and Fernando 7457 (MO); Dactylocladus stenostachya Oliv., North Borneo, Beaufort, J. Singh 24338 (K).

Heteropyxidaceae – Heteropyxis natalensis Harv., Zimbabwe, Umtali Distr., N.C. Chase 7934 (K).

Memecylaceae – Lijndenia laurina Zoll. and Morley, Borneo, Tawao, Elphinstone Prov., A.D.E. Elmer 21474; L. capitellata (Arn.) K.Bremer, Sri Lanka, Tawalama, Galle District, N. Balakrishnan 210; Memecylon dichotomum C.B.Clarke ex King, Kedah Peak, BR‐S.P. 810192; M. dichotomum C.B.Clarke ex King, Shah et al. 3777 (C); M. plebejum Kurz, Phenklai et al. 7450 (C); Mouriri collocarpaDucke, Sothers 269 (MO); Spathandra blakeoides (G.Don) Jacq.‐Fél., Gabon, Rabi, G. McPherson 15561; Votomita guianensis Aubl., French Guyana, Montsinéry, De Granville 4988; V. plerocarpa (Morley) Morley, Brazil, Amazonas, São Paulo de Olivença, B.A. Krukoff 8659.

Melastomataceae – Aciotis purpurascens Triana, French Guyana, Bélizon, F. Billiet and B. Jadin 4419; Acisanthera alsinaefolia Triana, Paraguay, T.M. Pedersen 3226; Amphorocalyx rupestris H.Perrier, Madagascar, Fiana rantsoa, P.B. Phillipson et al. 3840; Anaectocalyx latifolia Cogn., Venezuela, Fendler 441; Anerincleistus helferi Hook.f. ex Triana, India, Bengalia, Calcutta, J.W. Helfer 25; Antherotoma naudini Hook.f., Democratic Republic of Congo‐Kinshasa, Garamba, H. De Saeger 1481; Appendicularia thymifolia DC., French Guyana, Cayenne, G. Cremers 8100; Arthrostemma ciliatum Ruiz and Pav., Guatemala, G. Bernoulli 410; A. ciliatum Ruiz and Pav., Mexico, collector unknown; Astronia smilacifolia Triana ex C.B.Clarke, Borneo, Ranau, Clausing 238 (MJG); Axinaea merianiae Triana, Ecuador, Azuay, J.L. Luteyn and E. Cotton 11246; A. costaricensis Cogn., Panama, Cerro Horqueta, Prov. Bocas del Toro, P.H. Alles 4967; Barthea barthei (Hance ex Benth.) Krasser, BR‐S.P. 809961; Beccarianthus ickisii Merr., Philippine Islands, Surigao, C.A. Wenzel 3084; B. sp., Gaerlan et al. PPI 10859 (BRIT); Behuria insignis Cham., Brazil, Parigot de Souza Paraná, G. Hatschbach and E. Barbosa 56161; Bellucia pentamera Naudin, Colombia, Linden 249; Bertolonia acuminata Gardner, E. Ule 1137; Blakea gracilis Hemsl., Costa Rica, San Jose, Cascajal, F. Almeda et al. 2617; Blastus cochinchensis Lour., Taiwan, Taipei, Wulai, M. Tamura et al. 20038; Brachyotum sanguinolentum Triana, Bolivia, M. Bang 2860; Bredia yaeyamensis (Matsum.) H.L.Li, Japan, Yaeyama‐gun, Isl. Iriomote, T. Nakaike 607; Bucquetia glutinosa DC., Colombia, Bogota, J. Linden 776; B. nigritella Triana, origin unknown, W. Jameson 13; Calycogonium glabratum DC., Cuba, Monte Verde, C. Wright 193; Cambessedesia pityrophylla (DC.) B.Martens, Brazil, BR‐S.P. 809966; Catanthera sp., New Guinea, Morobe, Sattelberg, Clemens 1229; Centradenia floribunda Planch. ssp. floribunda, Guatemala, Escuintha, J. Donnell Smith 2216; Chaetolepis cufodontisii Standl., Costa Rica, San Marcos de Dota, H. Pittier 2278; Chaetostoma glaziovii Cogn., Brazil, BR‐S.P. 810194; C. pungens DC., Brazil, Minas Gerais, Glaziou 19194; Charianthus alpinus (Sw.) R.A.Howard, Guadeloupe, Morne Mazeau, F. Billiet and B. Jadin 5036; Clidemia hirta D.Don, A. Glaziou 157; Comolia lanceaeflora Triana, Brazil, Minas Gerais, Widgren s.n., BR‐S.P. 810199; Conostegia macrantha O.Berg ex Triana, Costa Rica, Volcan de Achiote, A. Tonduz 10844; Creochiton novoguineensis (Baker f.) Veldkamp and M.P.Nayar, New Guinea, Morobe, Sattelberg, Wareo, Clemens 1427; Desmoscelis villosa Naudin, Peru, Loreto, Yurimanguas, M. Rimachi Y. 3004; Dichaetanthera corymbosa (Cogn.) Jacq.‐Fél., Democratic Republic of Congo‐Kinshasa, P.N. Odzala, forêt d’Ikolo, D. Champluvier 5320, Br‐S.P. 54661; Dinophora spenneroides Benth., Cameroon, Song Bong, P. Bamps 1366; Dionycha triangularis Jum. and H.Perrier, Madagascar, Antsiranana, Antsatroto, S. Malcomber et al. 1463; Diplectria divaricata Kuntze, Borneo, Sandakan, Myburgh Prov., A. D. E. Elmer 20333; D. viminalis Kuntze, Borneo, Tawao, Elphinstone Prov., A. D. E. Elmer 21649; Dissochaeta bracteata Blume, Borneo, Maingay, de Vriese s.n.; Dissotis grandiflora Benth., A. J. M. Leeuwenberg 3283; D. rotundifolia Triana, Nigeria, Iyamoyong F.R., A. Binuyo 41364; Driessenia axantha Korth., Borneo, BR‐S.P. 810189; Ernestia quadriseta Berg ex Triana, Peru, Loreto, Carretera de Peña Negra, M. Rimachi Y. 8007; Fordiophyton faberi Stapf, China, Yunnan, Tcheu‐Fong, Chavi, BR‐S.P. 809969; Fritzschia erecta Cham., Brazil, Minas Gerais, P. Claussen 384A; Graffenrieda galeottii (Naudin) L.O.Williams, Costa Rica, Rio de la Union, H. Pittier 10584; G. latifolia Triana, Venezuela, Ocana, Schlim 791; Gravesia guttata Triana, Madagascar, BR‐S.P. 809968; Guyonia ciliata Hook.f., Liberia, Nimba Mts, A. J. M. Leeuwenberg et al. 4719; Henrietella glabra Cogn., Brazil, Rio de Janeiro, A. Glaziou 598; H. loretensis Gleason, Peru, Maynas, Rio Monon, M. Rimachi Y. 8508; Henriettea patrisiana DC., French Guyana, Cayenne, F. Billiet and B. Jadin 1015; Heterocentron glandulosum Schrenk var. glandulosum, Costa Rica, Tonduz 1370; H. macrostachyum Naudin, Hawaii, Maui, Keanae, M. C. Carlson 3804; Heterotis rotundifolia (Smith) Jacq.‐Fél., Guinea, Bata‐Bome; Huberia ovalifolia DC., Brazil, Corrego da Onça, Bahia, G. Hatschbach and F. J. Zelma 49503; Kendrickia walkeri Hook.f., Sri Lanka, Kostermans 27677; Lavoisiera cordata Cogn., Brazil, Serra do Cipó, Minas Gerais, G. Hatschbach et al. 28675; Leandra scabra DC., Brazil, Rio de Janeiro Prov., H. Schenck 1414; Loreya umbellata (Gleason) Wurdack, Peru, Maynas, Carretera de Peña Negra, M. Rimachi Y. 6278; Macairea radula DC., Brazil, Minas Gerais, P. Claussen 26; M. thyrsiflora DC., Brazil, Rio Negro, San Carlo, R. Spruce 2952; Macrocentrum cristatum Triana var. microphylla Cogn. in Mart., French Guyana, Cayenne, Montagne de la Trinité, J. J. de Granville et al. 6209; Macrolenes muscosa (Blume) Bakh.f., BR‐S.P. 809965; M. stellulata (Jack) Bakh.f., var stellulata, Borneo, Tawao, Elphinstone Prov., A. D. E. Elmer 20548; Maieta guianensis Aubl., French Guyana, Saut Sacaba, F. Billiet and B. Jadin 1599; M. guianensis Aubl., Brazil, Porto Velho, G.T. Prance et al. 8259; Marcetia mucugensis Wurdack, Brazil, Rio Paraguaçu, Bahia, G. Hatschbach 48221; Mecranium acuminatum (DC.) Skean, Dominican Republic, Paos Bajito; Medinilla fuchsioides Gardner, Sri Lanka, Hakgala Peak, L. C. Wheeler 12369; Melastomastrum capitatum (Vahl) A. and R.Fern., Senegal, Cap Skiving, C. Vanden Berghen 4719; M. segregatum (Benth.) A. and R.Fern., Democratic Republic of Congo‐Kinshasa, Ile des Mimosas, Ngaliema, C. Jeune 4278; M. segregatum (Benth.) A. and R.Fern., Democratic Republic of Congo‐Kinshasha, Schouteden 109; Meriania sipolisii Glaz. and Cogn., Brazil, Minas Gerais, Dio dos Cristais, Diamantina, A. P. Duarte 9653; Miconia laevigata DC., Mexico, H. Galeotti 2910; Microlepis oleaefolia Triana, Brazil, Glaziou 17524; Microlicia euphorbioides Mart. var. jonantha Mart., Brazil, S. Tomé das Letras, Minas Gerais, G. Hatschbach et al. 51192; M. graveolens DC., Brazil, Minas Gerais, Glaziou 19229; Monochaetum compactum Almeda, Panama, Volcan Chiriqui, F. Almeda and R. L. Wilbur 1564; Monolena primulaeflora Hook.f., Ecuador, Napo‐Pastaza Tena, E. Asplund 9210; Myriaspora egensis DC., Brazil, Cuiaba‐Santarem, J. H. Kirkbride and E. Lleras 2765; Myrmidone macrosperma (Mart.) Meisn., Brazil, Itaituba‐Humaita, P. Bamps 5413; Nepsera aquatica Naudin, Dominican Republic, H. von Türckheim; Nerophila gentianoides Naudin, Guinea, route Gaoual‐Kakoni, S. Lisowski 51248; Ochthocharis bornensis Blume, BR‐S.P. 809958; Osbeckia stellata Buch.‐Ham. ex D.Don, Thailand, J. D. Boulanger 1023; Ossaea coriacea Triana, Brazil, Minas Gerais, P. Claussen s.n., BR‐S.P. 810193; Otanthera cyanoides Triana, New Guinea, Heolbrung 618; Oxyspora bullata(Griff.) J.F.Maxwell, Malay Peninsula, Malacca, BR‐S.P. 810200; Pachyanthus poiretii Griseb., Cuba, Wright 2921; Pachycentria tuberculata Korth., Borneo, H. Winkler 2619; Pachyloma setosum Wurdack, Venezuela, Rio Guainia, Maroa, B. Maguire et al. 41708; Phyllagatis cavaleriei Guillaumin, China, Guizhou, Songtao Xian, B. Bartholomew 2259; P. hispida King, Malay Peninsula, Perak, H.N. Ridley, BR‐S.P. 810197; Pilocosta nana (Standl.) Almeda and Whiffin, Columbia, Santa Marta, H. H. Smith 2391; P. oerstedii (Triana) Almeda and Whiffin ssp. oerstedii, Costa Rica, Oersted 19; Pleiochiton setulosum Cogn., Brazil, Rio de Janeiro, A. Glaziou 589; Pogonanthera pulverulenta Blume, Borneo, Tawao, Elphinstone Prov., A. D. E. Elmer 20451; Poikilogyne sp., New Guinea, Morobe, Yunziang, J. and M. S. Clemens 2341; Preussiella kamerunensis Gilg, Cameroon, Forêt de Bakaka, A. J. M. Leeuwenberg 8329; Pseudosbeckia swynnertonii (Baker f.) A. and R.Fern., Zimbabwe, Harare, Chimanimani, J.B. Phipps 702; Pternandra echinata Jack, Malaysia, Kepong, Pahang, Clausing 75 (MJG); Pterogastra divaricata Naudin, Peru, Loreto, Pasto Grande, S. McDaniel and M. Rimachi Y. 16496; Pterolepis sp., French Guyana, La Comté, F. Billiet and B. Jadin 4713; Rhexia lutea Walter, USA, North Carolina, Craven County, N. Harlowe, N. Pence 44855; R. mariana L., USA, Florida, swamps, BR‐S.P. 810188; R. virganica L., Bristol Pa., J.C. Martindale s.n.; Rhynchanthera grandiflora DC., French Guynana, Sinnamary, B. De Granville 5520; Salpinga secunda Schrank and Mart. ex DC., Peru, Loreto, Maynas, S. McDaniel et al. 24798; Sandemania hoehnei (Cogn.) Wurdack, BR‐S.P. 810196; Sarcopyramis napalensis Wall., China, Guizhou, Jiankou Xian, B. Bartholomew et al. 400; Schwackaea cupheoides Cogn. ex Durand, Costa Rica, H. Pittier 4564; Siphanthera cordata Pohl, Brazil, Minas Gerais, Glaziou 19278; Sonerila silvatica Lundin, Sri Lanka, Kitulgala, Kelani Ganga, A. G. Robyns 7220; Stenodon suberosus Naudin, Glaziou 21350; Svitramia hatschbachii Wurdack, Brazil, S. Tomé das Letras, Minas Gerais, G. Hatschbach et al. 51193; Tetrazygia elaeagnoides DC., Porto Rico, P. Sintensis 2945; Tibouchina hieracioides Cogn., Brazil, Minas Gerais, Claussen 317; T. ochypetala Baill., Peru, Pasto Grande, S. McDaniel and M. Rimachi Y. 16468; Tibouchinopsis mirabilis Brade and Markgr., Brazil, Morro do Chapéu, G. Hatschbach 44242; Tococa nitens Triana, Brazil, Cuiaba‐Santarem road, J. H. Kirkbride and E. Lleras 2936; Topobea maurofernandeziana Cogn., Costa Rica, San Jose, A. Tonduz 9921; Trembleya laniflora Cogn., Brazil, Minas Gerais, P. Claussen s.n.; T. phlogiformis DC., Brazil, Minas Gerais, P. Claussen s.n.; Triolena hirsuta Triana, Costa Rica, Talamanca, A. Tonduz 9344; Tristemma mauritianum J.F.Gmel., Democratic Republic of Congo‐Kinshasa, R. Gutzwiller 751.

Myrtaceae – Calyptranthes sp., Surinam, Lely Mts., J. C. Lindeman et al. 327 (K); Kjellbergiodendron sp., S. Sulawesi, Soroako, K. Sidiyasa 1362 (K); Lophostemon grandiflorus (Benth.) Peter G.Wilson ssp. riparius (Domin) Peter G.Wilson and J.T.Waterh., Australia, Darwin, G. Wightman 1816 (K); Whiteodendron moultonianum (W.W.Sm.) Steenis, Brunei, Andulan Forest Reserve, P. S. Ashton s.n. (K).

Oliniaceae – Olinia acuminata Klotzsch, Frazer z75; O. cymosa Thunb., T.C.E. Fries 660; O. emarginata Burtt Davy, Barnard and Mogg 988 (MO); O. rochetiana A.Juss., L. Mwasumbi 13740.

Penaeaceae – Brachysiphon fucatus Gilg, South Africa, N. B. I. Kirstenbosch (K); Endomena lateriflora (L.f.) Gilg, South Africa, E. Esterhuysen 5064 (K); E. retzioides Sond., South Africa, P. Goldblatt 2063 (K); Glischrocolla formosa (Thunb.) R.Dahlgren, South Africa, J.P. Rourke 1046 (K); Penaea cneorum Meerb. ssp. cneorum, South Africa, Humansdorp Flats, Rachelsbosch, Fourcade 358 (K); P. cneorum Meerb. ssp. ruscifolia R.Dahlgren, South Africa, I. Williams 2307 (K).

Psiloxylaceae – Psiloxylon mauritianum Baill., Reunion, Takamaka, J. Bosser 22·106 (K).

Rhynchocalycaceae – Rhynchocalyx lawsonioides Oliv., South Africa, Durban, Transkei, Ntsbane forest, R. G. Strey 9000 (K).

Supplementary Material

Content Snapshot:

Notes

Received: 4 December 2001; Returned for revision: 15 February 2002; Accepted: 18 March 2002

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